Mixed and membrane-separated culturing of synthetic cyanobacteria-yeast consortia reveals metabolic cross-talk mimicking natural cyanolichens

Metabolite exchange mediates crucial interactions in microbial communities, significantly impacting global carbon and nitrogen cycling. Understanding these chemically-mediated interactions is essential for elucidating natural community functions and developing engineered synthetic communities. This...

Full description

Saved in:
Bibliographic Details
Published inScientific reports Vol. 14; no. 1; pp. 25303 - 19
Main Authors Bohutskyi, Pavlo, Pomraning, Kyle R., Jenkins, Jackson P, Kim, Young-Mo, Poirier, Brenton C, Betenbaugh, Michael J, Magnuson, Jon K
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 25.10.2024
Nature Publishing Group
Nature Portfolio
Subjects
Online AccessGet full text

Cover

Loading…
Abstract Metabolite exchange mediates crucial interactions in microbial communities, significantly impacting global carbon and nitrogen cycling. Understanding these chemically-mediated interactions is essential for elucidating natural community functions and developing engineered synthetic communities. This study investigated membrane-separated bioreactors (mBRs) as a novel tool to identify transient metabolites and their producers/consumers in mixed microbial communities. We compared three co-culture methods (direct mixed, 2-chamber mBR, and 3-chamber mBR) to grow a synthetic binary community of the cyanobacterium Synechococcus elongatus PCC 7942 and the fungus Rhodotorula toruloides NBRC 0880, as well as axenic S. elongatus . Despite not being natural lichen constituents, these organisms exhibited interactions resembling those in cyanolichens. S. elongatus fixed CO 2 into sugars as the primary shared metabolite, while R. toruloides secreted various biochemicals, predominantly sugar alcohols, mirroring the metabolite exchange observed in natural lichens. The mBR systems successfully captured metabolite gradients and revealed rapidly consumed compounds, including TCA cycle intermediates and amino acids. Our approach demonstrated that the 2-chamber mBR optimally balanced metabolite exchange and growth dynamics. This study provides insights into cross-species metabolic interactions and presents a valuable tool for investigating and engineering synthetic microbial communities with potential applications in biotechnology and environmental science.
AbstractList Metabolite exchange mediates crucial interactions in microbial communities, significantly impacting global carbon and nitrogen cycling. Understanding these chemically-mediated interactions is essential for elucidating natural community functions and developing engineered synthetic communities. This study investigated membrane-separated bioreactors (mBRs) as a novel tool to identify transient metabolites and their producers/consumers in mixed microbial communities. We compared three co-culture methods (direct mixed, 2-chamber mBR, and 3-chamber mBR) to grow a synthetic binary community of the cyanobacterium Synechococcus elongatus PCC 7942 and the fungus Rhodotorula toruloides NBRC 0880, as well as axenic S. elongatus . Despite not being natural lichen constituents, these organisms exhibited interactions resembling those in cyanolichens. S. elongatus fixed CO 2 into sugars as the primary shared metabolite, while R. toruloides secreted various biochemicals, predominantly sugar alcohols, mirroring the metabolite exchange observed in natural lichens. The mBR systems successfully captured metabolite gradients and revealed rapidly consumed compounds, including TCA cycle intermediates and amino acids. Our approach demonstrated that the 2-chamber mBR optimally balanced metabolite exchange and growth dynamics. This study provides insights into cross-species metabolic interactions and presents a valuable tool for investigating and engineering synthetic microbial communities with potential applications in biotechnology and environmental science.
Abstract Metabolite exchange mediates crucial interactions in microbial communities, significantly impacting global carbon and nitrogen cycling. Understanding these chemically-mediated interactions is essential for elucidating natural community functions and developing engineered synthetic communities. This study investigated membrane-separated bioreactors (mBRs) as a novel tool to identify transient metabolites and their producers/consumers in mixed microbial communities. We compared three co-culture methods (direct mixed, 2-chamber mBR, and 3-chamber mBR) to grow a synthetic binary community of the cyanobacterium Synechococcus elongatus PCC 7942 and the fungus Rhodotorula toruloides NBRC 0880, as well as axenic S. elongatus. Despite not being natural lichen constituents, these organisms exhibited interactions resembling those in cyanolichens. S. elongatus fixed CO2 into sugars as the primary shared metabolite, while R. toruloides secreted various biochemicals, predominantly sugar alcohols, mirroring the metabolite exchange observed in natural lichens. The mBR systems successfully captured metabolite gradients and revealed rapidly consumed compounds, including TCA cycle intermediates and amino acids. Our approach demonstrated that the 2-chamber mBR optimally balanced metabolite exchange and growth dynamics. This study provides insights into cross-species metabolic interactions and presents a valuable tool for investigating and engineering synthetic microbial communities with potential applications in biotechnology and environmental science.
Metabolite exchange mediates crucial interactions in microbial communities, significantly impacting global carbon and nitrogen cycling. Understanding these chemically-mediated interactions is essential for elucidating natural community functions and developing engineered synthetic communities. This study investigated membrane-separated bioreactors (mBRs) as a novel tool to identify transient metabolites and their producers/consumers in mixed microbial communities. We compared three co-culture methods (direct mixed, 2-chamber mBR, and 3-chamber mBR) to grow a synthetic binary community of the cyanobacterium Synechococcus elongatus PCC 7942 and the fungus Rhodotorula toruloides NBRC 0880, as well as axenic S. elongatus. Despite not being natural lichen constituents, these organisms exhibited interactions resembling those in cyanolichens. S. elongatus fixed CO2 into sugars as the primary shared metabolite, while R. toruloides secreted various biochemicals, predominantly sugar alcohols, mirroring the metabolite exchange observed in natural lichens. The mBR systems successfully captured metabolite gradients and revealed rapidly consumed compounds, including TCA cycle intermediates and amino acids. Our approach demonstrated that the 2-chamber mBR optimally balanced metabolite exchange and growth dynamics. This study provides insights into cross-species metabolic interactions and presents a valuable tool for investigating and engineering synthetic microbial communities with potential applications in biotechnology and environmental science.Metabolite exchange mediates crucial interactions in microbial communities, significantly impacting global carbon and nitrogen cycling. Understanding these chemically-mediated interactions is essential for elucidating natural community functions and developing engineered synthetic communities. This study investigated membrane-separated bioreactors (mBRs) as a novel tool to identify transient metabolites and their producers/consumers in mixed microbial communities. We compared three co-culture methods (direct mixed, 2-chamber mBR, and 3-chamber mBR) to grow a synthetic binary community of the cyanobacterium Synechococcus elongatus PCC 7942 and the fungus Rhodotorula toruloides NBRC 0880, as well as axenic S. elongatus. Despite not being natural lichen constituents, these organisms exhibited interactions resembling those in cyanolichens. S. elongatus fixed CO2 into sugars as the primary shared metabolite, while R. toruloides secreted various biochemicals, predominantly sugar alcohols, mirroring the metabolite exchange observed in natural lichens. The mBR systems successfully captured metabolite gradients and revealed rapidly consumed compounds, including TCA cycle intermediates and amino acids. Our approach demonstrated that the 2-chamber mBR optimally balanced metabolite exchange and growth dynamics. This study provides insights into cross-species metabolic interactions and presents a valuable tool for investigating and engineering synthetic microbial communities with potential applications in biotechnology and environmental science.
Metabolite exchange mediates crucial interactions in microbial communities, significantly impacting global carbon and nitrogen cycling. Understanding these chemically-mediated interactions is essential for elucidating natural community functions and developing engineered synthetic communities. This study investigated membrane-separated bioreactors (mBRs) as a novel tool to identify transient metabolites and their producers/consumers in mixed microbial communities. We compared three co-culture methods (direct mixed, 2-chamber mBR, and 3-chamber mBR) to grow a synthetic binary community of the cyanobacterium Synechococcus elongatus PCC 7942 and the fungus Rhodotorula toruloides NBRC 0880, as well as axenic S. elongatus. Despite not being natural lichen constituents, these organisms exhibited interactions resembling those in cyanolichens. S. elongatus fixed CO into sugars as the primary shared metabolite, while R. toruloides secreted various biochemicals, predominantly sugar alcohols, mirroring the metabolite exchange observed in natural lichens. The mBR systems successfully captured metabolite gradients and revealed rapidly consumed compounds, including TCA cycle intermediates and amino acids. Our approach demonstrated that the 2-chamber mBR optimally balanced metabolite exchange and growth dynamics. This study provides insights into cross-species metabolic interactions and presents a valuable tool for investigating and engineering synthetic microbial communities with potential applications in biotechnology and environmental science.
Metabolite exchange mediates crucial interactions in microbial communities, significantly impacting global carbon and nitrogen cycling. Understanding these chemically-mediated interactions is essential for elucidating natural community functions and developing engineered synthetic communities. This study investigated membrane-separated bioreactors (mBRs) as a novel tool to identify transient metabolites and their producers/consumers in mixed microbial communities. We compared three co-culture methods (direct mixed, 2-chamber mBR, and 3-chamber mBR) to grow a synthetic binary community of the cyanobacterium Synechococcus elongatus PCC 7942 and the fungus Rhodotorula toruloides NBRC 0880, as well as axenic S. elongatus. Despite not being natural lichen constituents, these organisms exhibited interactions resembling those in cyanolichens. S. elongatus fixed CO2 into sugars as the primary shared metabolite, while R. toruloides secreted various biochemicals, predominantly sugar alcohols, mirroring the metabolite exchange observed in natural lichens. The mBR systems successfully captured metabolite gradients and revealed rapidly consumed compounds, including TCA cycle intermediates and amino acids. Our approach demonstrated that the 2-chamber mBR optimally balanced metabolite exchange and growth dynamics. This study provides insights into cross-species metabolic interactions and presents a valuable tool for investigating and engineering synthetic microbial communities with potential applications in biotechnology and environmental science.
ArticleNumber 25303
Author Magnuson, Jon K
Kim, Young-Mo
Betenbaugh, Michael J
Pomraning, Kyle R.
Jenkins, Jackson P
Bohutskyi, Pavlo
Poirier, Brenton C
Author_xml – sequence: 1
  givenname: Pavlo
  surname: Bohutskyi
  fullname: Bohutskyi, Pavlo
  email: pavlo.bohutskyi@pnnl.gov
  organization: Earth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Department of Biological Systems Engineering, Washington State University
– sequence: 2
  givenname: Kyle R.
  surname: Pomraning
  fullname: Pomraning, Kyle R.
  organization: Energy and Environment Directorate, Pacific Northwest National Laboratory
– sequence: 3
  givenname: Jackson P
  surname: Jenkins
  fullname: Jenkins, Jackson P
  organization: Department of Chemical and Biomolecular Engineering, Johns Hopkins University
– sequence: 4
  givenname: Young-Mo
  surname: Kim
  fullname: Kim, Young-Mo
  organization: Earth and Biological Sciences Directorate, Pacific Northwest National Laboratory
– sequence: 5
  givenname: Brenton C
  surname: Poirier
  fullname: Poirier, Brenton C
  organization: Earth and Biological Sciences Directorate, Pacific Northwest National Laboratory
– sequence: 6
  givenname: Michael J
  surname: Betenbaugh
  fullname: Betenbaugh, Michael J
  organization: Department of Chemical and Biomolecular Engineering, Johns Hopkins University
– sequence: 7
  givenname: Jon K
  surname: Magnuson
  fullname: Magnuson, Jon K
  organization: Energy and Environment Directorate, Pacific Northwest National Laboratory
BackLink https://www.ncbi.nlm.nih.gov/pubmed/39455633$$D View this record in MEDLINE/PubMed
https://www.osti.gov/servlets/purl/2476534$$D View this record in Osti.gov
BookMark eNp9kstu1DAUhiNUREvpC7BAEWzYBHzNxCuEKi6Vith0bx07JzNuE3uwPRXzELwzzqSUlgVRpFjOdz4f2__z6sgHj1X1kpJ3lPDufRJUqq4hTDQrsRK8EU-qE0aEbBhn7OjB-Lg6S-malEcyJah6Vh1zJaRsOT-pfn1zP7Gvwff1hJOJ4LFJuIUIuUzb3Zh30fl1HYY67X3eYHa2tnvwwYDNGB00e4SUaxt8CjE7qCPeIoyp-DKYMM58DCk1GcabenKTszez0UNRw7jICrVBn15UT4dSimd339Pq6vOnq_OvzeX3LxfnHy8bK6nKjbErhStsKSIRTFlsRcuNaKkkvemMwY6wbtVKZZQFLmVHpUQpe1HgwVh-Wl0s2j7Atd5GN0Hc6wBOHyZCXGsoW7Ej6gHanrOhvK0RCqATqmV93ysiusFKKK4Pi2u7MxP2Fn0uu3okffzHu41eh1tNqaRUMVUMrxdDSNnpZF1GuynH6dFmzUTZBxcFenu3TAw_dpiynlyyOI7lwsIuaU4ZJbJT3ex78w96HXbRl_OcKdKq0jst1KuHfd83_CcaBWALcLi9iMM9QomeI6iXCOoSQX2IoJ7b5EtR2s6xwfh37f9U_QY_XOEi
Cites_doi 10.1016/j.jgg.2021.07.007
10.1038/nrmicro2386
10.1038/ismej.2010.36
10.1038/srep27184
10.4319/lo.2001.46.6.1370
10.3354/meps10428
10.1093/nar/gkr988
10.1146/annurev.micro.091208.073248
10.1038/ngeo1486
10.1101/gr.1239303
10.1093/nar/gkp356
10.1038/s41396-020-0603-9
10.1038/nature09826
10.1038/ismej.2011.118
10.3389/fmicb.2020.588778
10.1128/mSystems.00040-18
10.1093/pcp/pct079
10.3390/metabo10040171
10.4319/lo.2004.49.5.1652
10.1039/B606983P
10.1039/C7CS00431A
10.1038/s41396-022-01330-8
10.1111/j.1462-2920.2008.01633.x
10.1038/s41596-022-00710-w
10.1016/j.ymben.2017.10.009
10.1146/annurev.pp.42.060191.003005
10.1002/lno.10302
10.3389/fbioe.2021.603832
10.4319/lo.1997.42.3.0506
10.1080/14789450.2020.1766975
10.1007/978-3-662-10370-8_12
10.1128/msystems.00902-21
10.1016/S0953-7562(09)81109-X
10.1111/j.1469-8137.1979.tb02307.x
10.1073/pnas.0407716102
10.1016/j.seppur.2021.118689
10.1007/s00425-007-0563-6
10.1016/j.algal.2019.101755
10.1111/1462-2920.12242
10.1186/1471-2105-12-436
10.1038/ismej.2016.64
10.1016/j.biortech.2018.02.080
10.1073/pnas.0832439100
10.1111/j.1469-185X.1969.tb00821.x
10.1111/j.1574-6941.2008.00459.x
10.3389/fmicb.2014.00111
10.1080/11263504.2019.1701117
10.1073/pnas.1307701110
10.3389/fmicb.2021.667864
10.1111/1462-2920.12822
10.1016/0098-8472(94)90046-9
10.1007/978-3-642-85243-5_2
10.3354/ame01427
10.1016/j.jphotobiol.2012.03.005
10.1186/s13068-017-0736-x
10.1111/j.1472-765X.1989.tb00258.x
10.1038/nmicrobiol.2017.100
10.4319/lo.1984.29.2.0370
10.1128/aem.01558-22
10.1073/pnas.1514645113
10.1371/journal.pone.0016805
10.1021/ac802689c
10.1126/science.281.5374.237
10.1038/s41564-022-01251-4
10.3354/ame029239
10.1038/ismej.2011.1
10.4319/lo.2005.50.6.1924
10.1038/ngeo2841
10.1016/j.scitotenv.2018.11.026
10.1007/s11120-023-01015-z
10.1111/j.1469-8137.1989.tb00707.x
10.1007/s00253-020-10663-3
10.1038/s41564-019-0567-6
10.1128/mBio.01846-20
10.1126/sciadv.abf4792
10.1126/science.1218344
10.1128/msystems.00181-18
10.1093/jexbot/52.363.2033
10.1038/s41467-020-17612-8
10.1016/j.algal.2019.101580
10.1038/nature14488
10.1093/pcp/pcw169
10.1128/AEM.00212-07
10.1128/AEM.02479-07
10.1073/pnas.0913677107
10.21273/JASHS.127.4.467
10.1128/msystems.00017-21
10.1002/2013GB004705
10.1128/mBio.01614-21
ContentType Journal Article
Copyright Battelle Memorial Institute and The Authors 2024 2024
2024. Battelle Memorial Institute and The Authors 2024.
Battelle Memorial Institute and The Authors 2024 2024. This work is published under http://creativecommons.org/licenses/by-nc-nd/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
Battelle Memorial Institute and The Authors 2024 2024 2024
Copyright_xml – notice: Battelle Memorial Institute and The Authors 2024 2024
– notice: 2024. Battelle Memorial Institute and The Authors 2024.
– notice: Battelle Memorial Institute and The Authors 2024 2024. This work is published under http://creativecommons.org/licenses/by-nc-nd/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
– notice: Battelle Memorial Institute and The Authors 2024 2024 2024
CorporateAuthor Johns Hopkins University, Baltimore, MD (United States)
CorporateAuthor_xml – name: Johns Hopkins University, Baltimore, MD (United States)
DBID C6C
AAYXX
CITATION
CGR
CUY
CVF
ECM
EIF
NPM
3V.
7X7
7XB
88A
88E
88I
8FE
8FH
8FI
8FJ
8FK
ABUWG
AEUYN
AFKRA
AZQEC
BBNVY
BENPR
BHPHI
CCPQU
DWQXO
FYUFA
GHDGH
GNUQQ
HCIFZ
K9.
LK8
M0S
M1P
M2P
M7P
PHGZM
PHGZT
PIMPY
PJZUB
PKEHL
PPXIY
PQEST
PQGLB
PQQKQ
PQUKI
PRINS
Q9U
7X8
OIOZB
OTOTI
5PM
DOA
DOI 10.1038/s41598-024-74743-4
DatabaseName Springer Nature OA Free Journals
CrossRef
Medline
MEDLINE
MEDLINE (Ovid)
MEDLINE
MEDLINE
PubMed
ProQuest Central (Corporate)
Health & Medical Collection
ProQuest Central (purchase pre-March 2016)
Biology Database (Alumni Edition)
Medical Database (Alumni Edition)
Science Database (Alumni Edition)
ProQuest SciTech Collection
ProQuest Natural Science Collection
ProQuest Hospital Collection
Hospital Premium Collection (Alumni Edition)
ProQuest Central (Alumni) (purchase pre-March 2016)
ProQuest Central (Alumni)
ProQuest One Sustainability
ProQuest Central UK/Ireland
ProQuest Central Essentials
Biological Science Collection
ProQuest Central
Natural Science Collection
ProQuest One Community College
ProQuest Central
Health Research Premium Collection
Health Research Premium Collection (Alumni)
ProQuest Central Student
SciTech Premium Collection
ProQuest Health & Medical Complete (Alumni)
Biological Sciences
ProQuest Health & Medical Collection
PML(ProQuest Medical Library)
Science Database
Biological science database
ProQuest Central Premium
ProQuest One Academic
Publicly Available Content Database
ProQuest Health & Medical Research Collection
ProQuest One Academic Middle East (New)
ProQuest One Health & Nursing
ProQuest One Academic Eastern Edition (DO NOT USE)
ProQuest One Applied & Life Sciences
ProQuest One Academic
ProQuest One Academic UKI Edition
ProQuest Central China
ProQuest Central Basic
MEDLINE - Academic
OSTI.GOV - Hybrid
OSTI.GOV
PubMed Central (Full Participant titles)
DOAJ Directory of Open Access Journals
DatabaseTitle CrossRef
MEDLINE
Medline Complete
MEDLINE with Full Text
PubMed
MEDLINE (Ovid)
Publicly Available Content Database
ProQuest Central Student
ProQuest One Academic Middle East (New)
ProQuest Central Essentials
ProQuest Health & Medical Complete (Alumni)
ProQuest Central (Alumni Edition)
SciTech Premium Collection
ProQuest One Community College
ProQuest One Health & Nursing
ProQuest Natural Science Collection
ProQuest Central China
ProQuest Biology Journals (Alumni Edition)
ProQuest Central
ProQuest One Applied & Life Sciences
ProQuest One Sustainability
ProQuest Health & Medical Research Collection
Health Research Premium Collection
Health and Medicine Complete (Alumni Edition)
Natural Science Collection
ProQuest Central Korea
Health & Medical Research Collection
Biological Science Collection
ProQuest Central (New)
ProQuest Medical Library (Alumni)
ProQuest Science Journals (Alumni Edition)
ProQuest Biological Science Collection
ProQuest Central Basic
ProQuest Science Journals
ProQuest One Academic Eastern Edition
ProQuest Hospital Collection
Health Research Premium Collection (Alumni)
Biological Science Database
ProQuest SciTech Collection
ProQuest Hospital Collection (Alumni)
ProQuest Health & Medical Complete
ProQuest Medical Library
ProQuest One Academic UKI Edition
ProQuest One Academic
ProQuest One Academic (New)
ProQuest Central (Alumni)
MEDLINE - Academic
DatabaseTitleList


MEDLINE - Academic
MEDLINE

Publicly Available Content Database
Database_xml – sequence: 1
  dbid: C6C
  name: Springer Nature OA Free Journals
  url: http://www.springeropen.com/
  sourceTypes: Publisher
– sequence: 2
  dbid: DOA
  name: DOAJ Directory of Open Access Journals
  url: https://www.doaj.org/
  sourceTypes: Open Website
– sequence: 3
  dbid: NPM
  name: PubMed
  url: https://proxy.k.utb.cz/login?url=http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed
  sourceTypes: Index Database
– sequence: 4
  dbid: EIF
  name: MEDLINE
  url: https://proxy.k.utb.cz/login?url=https://www.webofscience.com/wos/medline/basic-search
  sourceTypes: Index Database
– sequence: 5
  dbid: BENPR
  name: ProQuest Central
  url: https://www.proquest.com/central
  sourceTypes: Aggregation Database
DeliveryMethod fulltext_linktorsrc
Discipline Biology
EISSN 2045-2322
EndPage 19
ExternalDocumentID oai_doaj_org_article_fa6d32f32f6b49aa84962ddd9048fc5a
PMC11511929
2476534
39455633
10_1038_s41598_024_74743_4
Genre Journal Article
GrantInformation_xml – fundername: Laboratory Directed Research and Development Program at Pacific Northwest National Laboratory
  grantid: Predictive Phenomics Initiative; Predictive Phenomics Initiative; Predictive Phenomics Initiative; Predictive Phenomics Initiative; Predictive Phenomics Initiative
– fundername: U.S. Department of Energy Genomic Science Program
  grantid: DE-SC0019388; DE-SC0019388; DE-SC0019388; DE-SC0019388
– fundername: U.S. Department of Energy Genomic Science Program
  grantid: DE-SC0019388
– fundername: Laboratory Directed Research and Development Program at Pacific Northwest National Laboratory
  grantid: Predictive Phenomics Initiative
GroupedDBID 0R~
3V.
4.4
53G
5VS
7X7
88A
88E
88I
8FE
8FH
8FI
8FJ
AAFWJ
AAJSJ
AAKDD
ABDBF
ABUWG
ACGFS
ACSMW
ACUHS
ADBBV
ADRAZ
AENEX
AEUYN
AFKRA
AJTQC
ALIPV
ALMA_UNASSIGNED_HOLDINGS
AOIJS
AZQEC
BAWUL
BBNVY
BCNDV
BENPR
BHPHI
BPHCQ
BVXVI
C6C
CCPQU
DIK
DWQXO
EBD
EBLON
EBS
ESX
FYUFA
GNUQQ
GROUPED_DOAJ
GX1
HCIFZ
HH5
HMCUK
HYE
KQ8
LK8
M0L
M1P
M2P
M48
M7P
M~E
NAO
OK1
PIMPY
PQQKQ
PROAC
PSQYO
RNT
RNTTT
RPM
SNYQT
UKHRP
AASML
AAYXX
AFPKN
CITATION
PHGZM
PHGZT
CGR
CUY
CVF
ECM
EIF
NPM
7XB
8FK
AARCD
K9.
PJZUB
PKEHL
PPXIY
PQEST
PQGLB
PQUKI
PRINS
Q9U
7X8
OIOZB
OTOTI
5PM
PUEGO
ID FETCH-LOGICAL-c519t-bc79e7e61ee0429ce6463b46150db8bbe80287659b9ca3558155e55d4429fbc3
IEDL.DBID M48
ISSN 2045-2322
IngestDate Wed Aug 27 01:29:59 EDT 2025
Thu Aug 21 18:43:49 EDT 2025
Mon Jun 23 02:30:29 EDT 2025
Fri Jul 11 10:20:38 EDT 2025
Wed Aug 13 09:12:23 EDT 2025
Wed Feb 19 02:11:38 EST 2025
Tue Jul 01 03:23:19 EDT 2025
Fri Feb 21 02:37:16 EST 2025
IsDoiOpenAccess true
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Issue 1
Keywords Membrane-separated bioreactor
Synthetic lichen
Metabolite exchange
Phototroph-heterotroph co-culture
Cross-feeding
Microbial community
Language English
License 2024. Battelle Memorial Institute and The Authors 2024.
Open Access This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which permits any non-commercial use, sharing, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if you modified the licensed material. You do not have permission under this licence to share adapted material derived from this article or parts of it. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by-nc-nd/4.0/.
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-c519t-bc79e7e61ee0429ce6463b46150db8bbe80287659b9ca3558155e55d4429fbc3
Notes ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 14
content type line 23
SC0019388; AC05-76RL01830
USDOE Laboratory Directed Research and Development (LDRD) Program
None
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OpenAccessLink http://journals.scholarsportal.info/openUrl.xqy?doi=10.1038/s41598-024-74743-4
PMID 39455633
PQID 3120699041
PQPubID 2041939
PageCount 19
ParticipantIDs doaj_primary_oai_doaj_org_article_fa6d32f32f6b49aa84962ddd9048fc5a
pubmedcentral_primary_oai_pubmedcentral_nih_gov_11511929
osti_scitechconnect_2476534
proquest_miscellaneous_3121058989
proquest_journals_3120699041
pubmed_primary_39455633
crossref_primary_10_1038_s41598_024_74743_4
springer_journals_10_1038_s41598_024_74743_4
ProviderPackageCode CITATION
AAYXX
PublicationCentury 2000
PublicationDate 2024-10-25
PublicationDateYYYYMMDD 2024-10-25
PublicationDate_xml – month: 10
  year: 2024
  text: 2024-10-25
  day: 25
PublicationDecade 2020
PublicationPlace London
PublicationPlace_xml – name: London
– name: England
– name: United States
PublicationTitle Scientific reports
PublicationTitleAbbrev Sci Rep
PublicationTitleAlternate Sci Rep
PublicationYear 2024
Publisher Nature Publishing Group UK
Nature Publishing Group
Nature Portfolio
Publisher_xml – name: Nature Publishing Group UK
– name: Nature Publishing Group
– name: Nature Portfolio
References Christie-Oleza, J. A., Sousoni, D., Lloyd, M., Armengaud, J. & Scanlan, D. J. Nutrient recycling facilitates long-term stability of marine microbial phototroph–heterotroph interactions. Nat. Microbiol., (2017). 2(9).
GökalsınBBerberDÖzyiğitoğluGÇYeşiladaESesalNCQuorum sensing attenuation properties of ethnobotanically valuable lichens againstPseudomonas aeruginosaPlant. Biosystems - Int. J. Dealing all Aspects Plant. Biology2019154679279910.1080/11263504.2019.1701117
Ruiz-GonzálezCSimóRVila-CostaMSommarugaRGasolJMSunlight modulates the relative importance of heterotrophic bacteria and picophytoplankton in DMSP-sulphur uptakeISME J.20116365065921955992328013210.1038/ismej.2011.118
Kassambara, A. & Mundt, F. Factoextra: Extract and Visualize the Results of Multivariate Data Analyses. R Package Version 1.0.7. (2020). https://CRAN.R-project.org/package=factoextra
MillotMDi MeoFTomasiSBoustieJTrouillasPPhotoprotective capacities of lichen metabolites: a joint theoretical and experimental studyJ. Photochem. Photobiol., B201211117261:CAS:528:DC%2BC38XlvFOks7o%3D2251689210.1016/j.jphotobiol.2012.03.005
Becker, J. W. et al. Closely Relat. Phytoplankton Species Produce Similar Suites Dissolved Org. Matter Front. Microbiol., 5. (2014).
JiangLEvidence for a mutualistic relationship between the cyanobacteria Nostoc and fungi Aspergilli in different environmentsAppl. Microbiol. Biotechnol.202010414641364261:CAS:528:DC%2BB3cXhtVCks7nF3247217510.1007/s00253-020-10663-3
CoeASurvival of Prochlorococcus in extended darknessLimnol. Oceanogr.2016614137513882016LimOc..61.1375C10.1002/lno.10302
FieldCBBehrenfeldMJRandersonJTFalkowskiPPrimary production of the Biosphere: integrating Terrestrial and Oceanic ComponentsScience199828153742372401998Sci...281..237F1:CAS:528:DyaK1cXksFKitb0%3D965771310.1126/science.281.5374.237
CowanDAGreenTGAWilsonATLichen Metabolism. 2. Aspects of light and dark physiologyNew Phytol.200683376176910.1111/j.1469-8137.1979.tb02307.x
TeiraEJosé PazóMSerretPFernándezEDissolved organic carbon production by microbial populations in the Atlantic OceanLimnol. Oceanogr.2001466137013772001LimOc..46.1370T1:CAS:528:DC%2BD3MXnsVSktbo%3D10.4319/lo.2001.46.6.1370
MartinezJRieraMLalucatJVives-RegoJThymidine incorporation into algal DNA from axenic cultures of Synechococcus, Chlorella and TetraselmisLett. Appl. Microbiol.1989841351381:CAS:528:DyaL1MXkslCmsbg%3D10.1111/j.1472-765X.1989.tb00258.x
LuoYWFriedrichsMAMDoneySCChurchMJDucklowHWOceanic heterotrophic bacterial nutrition by semilabile DOM as revealed by data assimilative modelingAquat. Microb. Ecol.201060327328710.3354/ame01427
Pontiller, B., Martínez-García, S., Lundin, D. & Pinhassi, J. Labile dissolved Organic Matter compound characteristics select for divergence in Marine bacterial activity and transcription. Front. Microbiol., 11. (2020).
PangZUsing MetaboAnalyst 5.0 for LC–HRMS spectra processing, multi-omics integration and covariate adjustment of global metabolomics dataNat. Protoc.2022178173517611:CAS:528:DC%2BB38XhsFCrsL3L3571552210.1038/s41596-022-00710-w
PoradaPWeberBElbertWPöschlUKleidonAEstimating impacts of lichens and bryophytes on global biogeochemical cyclesGlob. Biogeochem. Cycles201428271852014GBioC..28...71P1:CAS:528:DC%2BC2cXks1Sisb4%3D10.1002/2013GB004705
Li, T. et al. Creating a synthetic lichen: Mutualistic co-culture of fungi and extracellular polysaccharide-secreting cyanobacterium Nostoc PCC 7413. Algal Res., 45. (2020).
Cuhel, R. L. & Waterbury, J. B. Biochemical composition and short term nutrient incorporation patterns in a unicellular marine cyanobacterium, Synechococcus (WH7803)1. Limnology and Oceanography, 29(2): pp. 370–374. (1984).
Moran, M. A. et al. Deciphering ocean carbon in a changing world. Proceedings of the National Academy of Sciences, 113(12): pp. 3143–3151. (2016).
OsyczkaPMyśliwa-KurdzielBThe pattern of photosynthetic response and adaptation to changing light conditions in lichens is linked to their ecological rangePhotosynth. Res.2023157121351:CAS:528:DC%2BB3sXmsVaqu7c%3D369764461028204210.1007/s11120-023-01015-z
ChenTZhangHLiuYLiuYXHuangLEVenn: Easy to create repeatable and editable Venn diagrams and Venn networks onlineJ. Genet. Genomics20214898638663445285110.1016/j.jgg.2021.07.007
Flombaum, P. et al. Present and future global distributions of the marine Cyanobacteria Prochlorococcus and Synechococcus. Proceedings of the National Academy of Sciences, 110(24): pp. 9824–9829. (2013).
Biller, S. J., Coe, A., Roggensack, S. E., Chisholm, S. W. & Mason, O. Heterotroph Interact. Alter. Prochlorococcus Transcriptome Dynamics Dur. Ext. Periods Darkn. mSystems, 3(3). (2018).
WilliamsonJDJenningsDBGuoWWPharrDMEhrenshaftMSugar Alcohols, Salt stress, and Fungal Resistance: polyols—multifunctional Plant Protection?J. Am. Soc. Hortic. Sci.200212744674731:CAS:528:DC%2BD38Xlt1Orsr8%3D10.21273/JASHS.127.4.467
PaoliACelussiMDel NegroPFonda UmaniSTalaricoLEcological advantages from light adaptation and heterotrophic-like behavior in Synechococcus harvested from the Gulf of Trieste (Northern Adriatic Sea)FEMS Microbiol. Ecol.20086422192291:CAS:528:DC%2BD1cXlvVKmt7w%3D1833655710.1111/j.1574-6941.2008.00459.x
Bohutskyi, P. et al. Metabolic effects of vitamin B12 on physiology, stress resistance, growth rate and biomass productivity of cyanobacterium stanieri planktonic and biofilm cultures. Algal Res., 42. (2019).
YeltonAPGlobal genetic capacity for mixotrophy in marine picocyanobacteriaISME J.20161012294629571:CAS:528:DC%2BC28XhvFOht7vM27137127514818810.1038/ismej.2016.64
HillerKMetaboliteDetector: Comprehensive Analysis Tool for targeted and nontargeted GC/MS based Metabolome AnalysisAnal. Chem.2009819342934391:CAS:528:DC%2BD1MXktlSlu7o%3D1935859910.1021/ac802689c
ElbertWContribution of cryptogamic covers to the global cycles of carbon and nitrogenNat. Geosci.2012574594622012NatGe...5..459E1:CAS:528:DC%2BC38XnvVynur4%3D10.1038/ngeo1486
WeissbergOAharonovichDSherDPhototroph-heterotroph interactions during growth and long-term starvation across Prochlorococcus and Alteromonas diversityISME J.202217222723736335212986006410.1038/s41396-022-01330-8
WuZSingle-cell Measurements Modelling Reveal. Substantial Org. Carbon Acquisition Prochlorococcus Nat. Microbiol.2022712206820771:CAS:528:DC%2BB38XivVWiu7%2FP36329198
Bertilsson, S., Berglund, O., Pullin, M. & Chisholm, S. Release of Dissolved Organic Matter by Prochlorococcus55p. 225–231 (Vie et Milieu/Life & Environment, 2005).
Vila-CostaMDimethylsulfoniopropionate Uptake Mar. Phytoplankton Sci.20063145799652654
Pomraning, K. R. et al. Integration of Proteomics and Metabolomics Into the Design, Build, Test, Learn Cycle to Improve 3-Hydroxypropionic Acid Production in Aspergillus pseudoterreus. Frontiers in Bioengineering and Biotechnology, 9. (2021).
Li, T. et al. Mimicking lichens: incorporation of yeast strains together with sucrose-secreting cyanobacteria improves survival, growth, ROS removal, and lipid production in a stable mutualistic co-culture production platform. Biotechnol. Biofuels, 10(1). (2017).
MorrisJJKirkegaardRSzulMJJohnsonZIZinserERFacilitation of Robust Growth of Prochlorococcus colonies and dilute liquid cultures by helper heterotrophic BacteriaAppl. Environ. Microbiol.20087414453045342008ApEnM..74.4530M1:CAS:528:DC%2BD1cXptVeit7Y%3D18502916249317310.1128/AEM.02479-07
AminSAInteraction and signalling between a cosmopolitan phytoplankton and associated bacteriaNature20155227554981012015Natur.522...98A1:CAS:528:DC%2BC2MXhtFeitLrN2601730710.1038/nature14488
Jo, C. et al. Construction and modeling of a coculture microplate for real-time measurement of Microbial interactions. mSystems, 8(2). (2023).
Rothman, D. H., Hayes, J. M. & Summons, R. E. Dynamics of the Neoproterozoic carbon cycle. Proceedings of the National Academy of Sciences, 100(14): pp. 8124–8129. (2003).
HoneggerRFunctional aspects of the Lichen SymbiosisAnnu. Rev. Plant Physiol. Plant Mol. Biol.19914215535781:CAS:528:DyaK3MXltFSms7s%3D10.1146/annurev.pp.42.060191.003005
Li, B. et al. Catalytic promiscuity in the biosynthesis of cyclic peptide secondary metabolites in planktonic marine cyanobacteria. Proceedings of the National Academy of Sciences, 107(23): pp. 10430–10435. (2010).
MarañónECermeñoPFernándezERodríguezJZabalaLSignificance and mechanisms of photosynthetic production of dissolved organic carbon in a coastal eutrophic ecosystemLimnol. Oceanogr.2004495165216662004LimOc..49.1652M10.4319/lo.2004.49.5.1652
BohutskyiPProduction of lipid-containing algal-bacterial polyculture in wastewater and biomethanation of lipid extracted residues: enhancing methane yield through hydrothermal pretreatment and relieving solvent toxicity through co-digestionSci. Total Environ.2019653137713942019ScTEn.653.1377B1:CAS:528:DC%2BC1cXit1SnsrrP3075957710.1016/j.scitotenv.2018.11.026
Huneck, S. & Yoshimura, I. Identification of Lichen Substances, in Identification of Lichen Substances. pp. 11–123. (1996).
JardillierLZubkovMVPearmanJScanlanDJSignificant CO2 fixation by small prymnesiophytes in the subtropical and tropical northeast Atlantic OceanISME J.201049118011921:CAS:528:DC%2BC3cXhtVKgsr7E2039357510.1038/ismej.2010.36
Wang, J. et al. Construction of fungi-microalgae Symbiotic System and Adsorption Study of Heavy Metal ions268 (Separation and Purification Technology, 2021).
BohutskyiPConversion of stranded waste-stream carbon and nutrients into value-added products via metabolically coupled binary heterotroph-photoautotroph systemBioresour. Technol.201826068751:CAS:528:DC%2BC1cXjt1yqsLc%3D2961445310.1016/j.biortech.2018.02.080
Zuñiga, C. et al. Synthetic microbial communities of heterotrophs and phototrophs facilitate sustainable growth. Nature Communications, 11(1). (2020).
De PerezLAlseekhSBrotmanYFernieARNetwork-based strategies in metabolomics data analysis and interpretation: from molecular networking to biological interpretationExpert Rev. Proteomics202017424325510.1080/14789450.2020.1766975
LandaMPhylogenetic and structural response of heterotrophic bacteria to disso
74743_CR83
74743_CR84
74743_CR85
Z Pang (74743_CR92) 2022; 17
VK Michelou (74743_CR62) 2007; 73
M Vila-Costa (74743_CR64) 2006; 314
C Ruiz-González (74743_CR65) 2011; 6
74743_CR81
M Kosugi (74743_CR47) 2013; 54
74743_CR76
74743_CR73
74743_CR74
E Stocker-Wörgötter (74743_CR44) 2008; 25
74743_CR75
R Honegger (74743_CR38) 1993; 97
JA Christie-Oleza (74743_CR21) 2015; 17
R Honegger (74743_CR17) 1991; 42
A Paoli (74743_CR56) 2008; 64
YW Luo (74743_CR19) 2010; 60
74743_CR70
MC Muñoz-Marín (74743_CR60) 2020; 14
XAG Morán (74743_CR18) 2013; 489
74743_CR23
XAG Morán (74743_CR7) 2002; 29
74743_CR20
CB Field (74743_CR2) 1998; 281
P Osyczka (74743_CR87) 2023; 157
74743_CR25
N Jiao (74743_CR10) 2010; 8
74743_CR26
DA Cowan (74743_CR88) 2006; 83
D Fahselt (74743_CR39) 1994; 17
MC Muñoz-Marín (74743_CR57) 2022; 7
I Mary (74743_CR61) 2008; 10
E Marañón (74743_CR8) 2004; 49
P Porada (74743_CR15) 2014; 28
A Coe (74743_CR32) 2016; 61
E Teira (74743_CR9) 2001; 46
74743_CR12
74743_CR94
74743_CR95
74743_CR96
74743_CR14
TL Weiss (74743_CR72) 2017; 44
D Sher (74743_CR27) 2011; 5
74743_CR90
B Biddanda (74743_CR5) 1997; 42
74743_CR43
JJ Morris (74743_CR28) 2008; 74
74743_CR40
RMW Amon (74743_CR11) 2016; 9
74743_CR42
P Bohutskyi (74743_CR78) 2019; 653
M Millot (74743_CR49) 2012; 111
74743_CR48
AP Yelton (74743_CR59) 2016; 10
JD Williamson (74743_CR46) 2002; 127
OL Lange (74743_CR86) 2001; 52
L Jardillier (74743_CR3) 2010; 4
74743_CR33
74743_CR34
74743_CR35
PD Straight (74743_CR50) 2009; 63
RR Malmstrom (74743_CR63) 2005; 50
74743_CR30
74743_CR31
Z Wu (74743_CR58) 2022; 7
EI Friedmann (74743_CR54) 1988; 58
BW Abramson (74743_CR89) 2016; 57
O Weissberg (74743_CR29) 2022; 17
C Zuñiga (74743_CR77) 2019; 4
D Smith (74743_CR36) 1969; 44
T Chen (74743_CR97) 2021; 48
M Landa (74743_CR22) 2014; 16
J Martinez (74743_CR67) 1989; 8
CEM Lines (74743_CR37) 1989; 111
S Aubert (74743_CR41) 2007; 226
74743_CR4
74743_CR66
74743_CR1
74743_CR68
H Teeling (74743_CR24) 2012; 336
74743_CR69
J Xia (74743_CR93) 2009; 37
L De Perez (74743_CR82) 2020; 17
P Shannon (74743_CR80) 2003; 13
P Bohutskyi (74743_CR79) 2018; 260
K Hiller (74743_CR91) 2009; 81
L Jiang (74743_CR71) 2020; 104
PF Sexton (74743_CR13) 2011; 471
SA Amin (74743_CR53) 2015; 522
74743_CR52
M Kanehisa (74743_CR98) 2011; 40
H Li (74743_CR55) 2016; 6
W Elbert (74743_CR16) 2012; 5
MJ Calcott (74743_CR45) 2018; 47
74743_CR6
B Gökalsın (74743_CR51) 2019; 154
References_xml – reference: PangZUsing MetaboAnalyst 5.0 for LC–HRMS spectra processing, multi-omics integration and covariate adjustment of global metabolomics dataNat. Protoc.2022178173517611:CAS:528:DC%2BB38XhsFCrsL3L3571552210.1038/s41596-022-00710-w
– reference: DiMucci, D., Kon, M., Segrè, D. & Typas, N. Machine learning reveals Missing edges and Putative Interaction mechanisms in Microbial Ecosystem Networks. mSystems, 3(5). (2018).
– reference: Moran, M. A. et al. Deciphering ocean carbon in a changing world. Proceedings of the National Academy of Sciences, 113(12): pp. 3143–3151. (2016).
– reference: Huneck, S. & Yoshimura, I. Identification of Lichen Substances, in Identification of Lichen Substances. pp. 11–123. (1996).
– reference: Rothman, D. H., Hayes, J. M. & Summons, R. E. Dynamics of the Neoproterozoic carbon cycle. Proceedings of the National Academy of Sciences, 100(14): pp. 8124–8129. (2003).
– reference: MoránXAGDucklowHWEricksonMCarbon fluxes through estuarine bacteria reflect coupling with phytoplanktonMar. Ecol. Prog. Ser.201348975852013MEPS..489...75M10.3354/meps10428
– reference: Blighe, K., Rana, S. & Lewis, M. EnhancedVolcano: Publication-ready volcano plots with enhanced colouring and labeling. R package version 1.16.0. (2022). https://github.com/kevinblighe/EnhancedVolcano.
– reference: FriedmannEIHuaMOcampo-FriedmannR3.6 cryptoendolithic lichen and cyanobacterial communities of the Ross Desert, AntarcticaPolarforschung1988582/32512591:STN:280:DC%2BD3Mnls12jtw%3D%3D11538357
– reference: PaoliACelussiMDel NegroPFonda UmaniSTalaricoLEcological advantages from light adaptation and heterotrophic-like behavior in Synechococcus harvested from the Gulf of Trieste (Northern Adriatic Sea)FEMS Microbiol. Ecol.20086422192291:CAS:528:DC%2BD1cXlvVKmt7w%3D1833655710.1111/j.1574-6941.2008.00459.x
– reference: MartinezJRieraMLalucatJVives-RegoJThymidine incorporation into algal DNA from axenic cultures of Synechococcus, Chlorella and TetraselmisLett. Appl. Microbiol.1989841351381:CAS:528:DyaL1MXkslCmsbg%3D10.1111/j.1472-765X.1989.tb00258.x
– reference: LiHWeiJCFunctional analysis of thioredoxin from the desert lichen-forming fungus, endocarpon pusillum Hedwig, reveals its role in stress toleranceSci. Rep.20166271842016NatSR...627184L1:CAS:528:DC%2BC28XptFChsLc%3D27251605489003710.1038/srep27184
– reference: AminSAInteraction and signalling between a cosmopolitan phytoplankton and associated bacteriaNature20155227554981012015Natur.522...98A1:CAS:528:DC%2BC2MXhtFeitLrN2601730710.1038/nature14488
– reference: Muñoz-MarínMCMixotrophy in depthNat. Microbiol.2022712194919503632919910.1038/s41564-022-01251-4
– reference: MarañónECermeñoPFernándezERodríguezJZabalaLSignificance and mechanisms of photosynthetic production of dissolved organic carbon in a coastal eutrophic ecosystemLimnol. Oceanogr.2004495165216662004LimOc..49.1652M10.4319/lo.2004.49.5.1652
– reference: Ruiz-GonzálezCSimóRVila-CostaMSommarugaRGasolJMSunlight modulates the relative importance of heterotrophic bacteria and picophytoplankton in DMSP-sulphur uptakeISME J.20116365065921955992328013210.1038/ismej.2011.118
– reference: WuZSingle-cell Measurements Modelling Reveal. Substantial Org. Carbon Acquisition Prochlorococcus Nat. Microbiol.2022712206820771:CAS:528:DC%2BB38XivVWiu7%2FP36329198
– reference: ElbertWContribution of cryptogamic covers to the global cycles of carbon and nitrogenNat. Geosci.2012574594622012NatGe...5..459E1:CAS:528:DC%2BC38XnvVynur4%3D10.1038/ngeo1486
– reference: OsyczkaPMyśliwa-KurdzielBThe pattern of photosynthetic response and adaptation to changing light conditions in lichens is linked to their ecological rangePhotosynth. Res.2023157121351:CAS:528:DC%2BB3sXmsVaqu7c%3D369764461028204210.1007/s11120-023-01015-z
– reference: Bertilsson, S., Berglund, O., Pullin, M. & Chisholm, S. Release of Dissolved Organic Matter by Prochlorococcus55p. 225–231 (Vie et Milieu/Life & Environment, 2005).
– reference: Zhang, Z. et al. Long-term survival of Synechococcus and heterotrophic Bacteria without external nutrient supply after changes in their relationship from antagonism to Mutualism. mBio, 12(4). (2021).
– reference: Morris, J. H. et al. clusterMaker: a multi-algorithm clustering plugin for Cytoscape. BMC Bioinform., 12(1). (2011).
– reference: Christie-Oleza, J. A., Sousoni, D., Lloyd, M., Armengaud, J. & Scanlan, D. J. Nutrient recycling facilitates long-term stability of marine microbial phototroph–heterotroph interactions. Nat. Microbiol., (2017). 2(9).
– reference: Zuñiga, C. et al. Synthetic microbial communities of heterotrophs and phototrophs facilitate sustainable growth. Nature Communications, 11(1). (2020).
– reference: ChenTZhangHLiuYLiuYXHuangLEVenn: Easy to create repeatable and editable Venn diagrams and Venn networks onlineJ. Genet. Genomics20214898638663445285110.1016/j.jgg.2021.07.007
– reference: Li, B. et al. Catalytic promiscuity in the biosynthesis of cyclic peptide secondary metabolites in planktonic marine cyanobacteria. Proceedings of the National Academy of Sciences, 107(23): pp. 10430–10435. (2010).
– reference: LuoYWFriedrichsMAMDoneySCChurchMJDucklowHWOceanic heterotrophic bacterial nutrition by semilabile DOM as revealed by data assimilative modelingAquat. Microb. Ecol.201060327328710.3354/ame01427
– reference: MichelouVKCottrellMTKirchmanDLLight-stimulated bacterial production and amino acid assimilation by Cyanobacteria and other microbes in the North Atlantic OceanAppl. Environ. Microbiol.20077317553955462007ApEnM..73.5539M1:CAS:528:DC%2BD2sXhtVeht7zM17630296204207810.1128/AEM.00212-07
– reference: CowanDAGreenTGAWilsonATLichen Metabolism. 2. Aspects of light and dark physiologyNew Phytol.200683376176910.1111/j.1469-8137.1979.tb02307.x
– reference: AbramsonBWKachelBKramerDMDucatDCIncreased photochemical efficiency in Cyanobacteria via an Engineered sucrose SinkPlant Cell Physiol.20165712245124601:CAS:528:DC%2BC2sXkt1aisb8%3D2774288310.1093/pcp/pcw169
– reference: LandaMPhylogenetic and structural response of heterotrophic bacteria to dissolved organic matter of different chemical composition in a continuous culture studyEnviron. Microbiol.2014166166816811:CAS:528:DC%2BC2cXpsVenu7s%3D2402067810.1111/1462-2920.12242
– reference: Kranner, I. et al. Antioxidants and photoprotection in a lichen as compared with its isolated symbiotic partners. Proceedings of the National Academy of Sciences, 102(8): pp. 3141–3146. (2005).
– reference: Nazem-Bokaee, H., Hom, E. F. Y., Warden, A. C., Mathews, S. & Gueidan, C. Towards a Systems Biology Approach to Understanding the Lichen Symbiosis: Opportunities and Challenges of Implementing Network Modelling12 (Frontiers in Microbiology, 2021).
– reference: AmonRMWOcean dissolved organics matterNat. Geosci.20169128648652016NatGe...9..864A1:CAS:528:DC%2BC28XhvVGiurvN10.1038/ngeo2841
– reference: AubertSJugeCBoissonAMGoutEBlignyRMetabolic processes sustaining the reviviscence of lichen Xanthoria elegans (Link) in high mountain environmentsPlanta20072265128712971:CAS:528:DC%2BD2sXhtVWjsbvI17574473238690710.1007/s00425-007-0563-6
– reference: GökalsınBBerberDÖzyiğitoğluGÇYeşiladaESesalNCQuorum sensing attenuation properties of ethnobotanically valuable lichens againstPseudomonas aeruginosaPlant. Biosystems - Int. J. Dealing all Aspects Plant. Biology2019154679279910.1080/11263504.2019.1701117
– reference: Pomraning, K. R. et al. Integration of Proteomics and Metabolomics Into the Design, Build, Test, Learn Cycle to Improve 3-Hydroxypropionic Acid Production in Aspergillus pseudoterreus. Frontiers in Bioengineering and Biotechnology, 9. (2021).
– reference: Team, R. C. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL (2022). https://www.R-project.org/
– reference: FahseltDCarbon Metabolism in LichensSymbiosis1994171271821:CAS:528:DyaK2MXksFanur0%3D
– reference: Armstrong, R. A. & Smith, S. N. The Levels of Ribitol, Arabitol and Mannitol in Individual Lobes of the Lichen Parmelia Conspersa (Ehrh. ex Ach.) ACH34p. 253–260 (Environmental and Experimental Botany, 1994). 3.
– reference: CalcottMJAckerleyDFKnightAKeyzersRAOwenJGSecondary metabolism in the lichen symbiosisChem. Soc. Rev.2018475173017601:CAS:528:DC%2BC2sXhslGrurvN2909412910.1039/C7CS00431A
– reference: JiaoNMicrobial production of recalcitrant dissolved organic matter: long-term carbon storage in the global oceanNat. Rev. Microbiol.2010885935991:CAS:528:DC%2BC3cXotlWku70%3D2060196410.1038/nrmicro2386
– reference: Xu, J. et al. You Exude What You Eat: How Carbon-, Nitrogen-, and Sulfur-Rich Organic Substrates Shape Microbial Community Composition and the Dissolved Organic Matter Pool (Applied and Environmental Microbiology, 2022). 88(23).
– reference: JiangLEvidence for a mutualistic relationship between the cyanobacteria Nostoc and fungi Aspergilli in different environmentsAppl. Microbiol. Biotechnol.202010414641364261:CAS:528:DC%2BB3cXhtVCks7nF3247217510.1007/s00253-020-10663-3
– reference: HillerKMetaboliteDetector: Comprehensive Analysis Tool for targeted and nontargeted GC/MS based Metabolome AnalysisAnal. Chem.2009819342934391:CAS:528:DC%2BD1MXktlSlu7o%3D1935859910.1021/ac802689c
– reference: Christie-OlezaJAArmengaudJGuerinPScanlanDJFunctional distinctness in the exoproteomes of marineSynechococcusEnviron. Microbiol.20151710378137941:CAS:528:DC%2BC2MXhslCltbvL25727668494970710.1111/1462-2920.12822
– reference: Morris, J. J., Johnson, Z. I., Szul, M. J., Keller, M. & Zinser, E. R. Dependence of the Cyanobacterium Prochlorococcus on Hydrogen Peroxide Scavenging Microbes for Growth at the Ocean’s Surface. PLoS ONE, 6(2). (2011).
– reference: MalmstromRRKieneRPVilaMKirchmanDLDimethylsulfoniopropionate (DMSP) assimilation by Synechococcus in the Gulf of Mexico and northwest Atlantic OceanLimnol. Oceanogr.2005506192419312005LimOc..50.1924M1:CAS:528:DC%2BD2MXhtlWrsb7F10.4319/lo.2005.50.6.1924
– reference: Birer-Williams, C. M. C., Chu, R. K., Anderton, C. R., Wright, E. S. & Bernstein, H. C. SubTap, a versatile 3D printed platform for eavesdropping on extracellular interactions. mSystems, 6(4). (2021).
– reference: Li, T. et al. Mimicking lichens: incorporation of yeast strains together with sucrose-secreting cyanobacteria improves survival, growth, ROS removal, and lipid production in a stable mutualistic co-culture production platform. Biotechnol. Biofuels, 10(1). (2017).
– reference: Honegger, R. Metabolic Interactions at the Mycobiont-Photobiont Interface in Lichens, in Plant Relationships. pp. 209–221. (1997).
– reference: PoradaPWeberBElbertWPöschlUKleidonAEstimating impacts of lichens and bryophytes on global biogeochemical cyclesGlob. Biogeochem. Cycles201428271852014GBioC..28...71P1:CAS:528:DC%2BC2cXks1Sisb4%3D10.1002/2013GB004705
– reference: KanehisaMGotoSSatoYFurumichiMTanabeMKEGG for integration and interpretation of large-scale molecular data setsNucleic Acids Res.201140D1D109D11422080510324502010.1093/nar/gkr988
– reference: SmithDMuscatineLLewisDCarbohydrate movement from autotrophs to heterotrophs in parasitic and mutualistic symbiosisBiol. Rev.196944117851:CAS:528:DyaF1MXhtFags78%3D489011810.1111/j.1469-185X.1969.tb00821.x
– reference: Nair, S. et al. Inherent tendency of Synechococcus and heterotrophic bacteria for mutualism on long-term coexistence despite environmental interference. Sci. Adv., 8(39). (2022).
– reference: HoneggerRKutasiVRuffnerHPPolyol patterns in eleven species of aposymbiotically cultured lichen mycobiontsMycol. Res.199397135391:CAS:528:DyaK3sXks1Ontro%3D10.1016/S0953-7562(09)81109-X
– reference: SextonPFEocene global warming events driven by ventilation of oceanic dissolved organic carbonNature201147173383493522011Natur.471..349S1:CAS:528:DC%2BC3MXjsVOjtbk%3D2141233610.1038/nature09826
– reference: BiddandaBBennerRCarbon, nitrogen, and carbohydrate fluxes during the production of particulate and dissolved organic matter by marine phytoplanktonLimnol. Oceanogr.19974235065181997LimOc..42..506B1:CAS:528:DyaK2sXmsF2ht7o%3D10.4319/lo.1997.42.3.0506
– reference: Vila-CostaMDimethylsulfoniopropionate Uptake Mar. Phytoplankton Sci.20063145799652654
– reference: De PerezLAlseekhSBrotmanYFernieARNetwork-based strategies in metabolomics data analysis and interpretation: from molecular networking to biological interpretationExpert Rev. Proteomics202017424325510.1080/14789450.2020.1766975
– reference: WilliamsonJDJenningsDBGuoWWPharrDMEhrenshaftMSugar Alcohols, Salt stress, and Fungal Resistance: polyols—multifunctional Plant Protection?J. Am. Soc. Hortic. Sci.200212744674731:CAS:528:DC%2BD38Xlt1Orsr8%3D10.21273/JASHS.127.4.467
– reference: XiaJPsychogiosNYoungNWishartDMetaboAnalyst: a web server for metabolomic data analysis and interpretationNucleic Acids Res.200937Web ServerW652W6601:CAS:528:DC%2BD1MXosFSkt7c%3D19429898270387810.1093/nar/gkp356
– reference: BohutskyiPConversion of stranded waste-stream carbon and nutrients into value-added products via metabolically coupled binary heterotroph-photoautotroph systemBioresour. Technol.201826068751:CAS:528:DC%2BC1cXjt1yqsLc%3D2961445310.1016/j.biortech.2018.02.080
– reference: Kassambara, A. & Mundt, F. Factoextra: Extract and Visualize the Results of Multivariate Data Analyses. R Package Version 1.0.7. (2020). https://CRAN.R-project.org/package=factoextra
– reference: MillotMDi MeoFTomasiSBoustieJTrouillasPPhotoprotective capacities of lichen metabolites: a joint theoretical and experimental studyJ. Photochem. Photobiol., B201211117261:CAS:528:DC%2BC38XlvFOks7o%3D2251689210.1016/j.jphotobiol.2012.03.005
– reference: LangeOLGreenTGAHeberUHydration-dependent photosynthetic production of lichens: what do laboratory studies tell us about field performance?J. Exp. Bot.200152363203320421:CAS:528:DC%2BD3MXns1Wkt7g%3D1155973910.1093/jexbot/52.363.2033
– reference: Pontiller, B., Martínez-García, S., Lundin, D. & Pinhassi, J. Labile dissolved Organic Matter compound characteristics select for divergence in Marine bacterial activity and transcription. Front. Microbiol., 11. (2020).
– reference: LinesCEMRatcliffeRGReesTAVSouthonTEA 13 C NMR study of photosynthate transport and metabolism in the lichen Xanthoria Calcicola OxnerNew Phytol.198911134474561:CAS:528:DyaL1MXkt1Wjs78%3D3387400710.1111/j.1469-8137.1989.tb00707.x
– reference: Roth-Rosenberg, D. et al. Prochlorococcus cells rely on microbial interactions rather than on chlorotic resting stages to survive long-term nutrient starvation. mBio, 11(4). (2020).
– reference: Teiser, M. L. O. Extracellular low Molecular Weight Organic Compounds Produced by Synechococcus sp. and Their Roles in the food web of Alkaline hot Spring Microbial mat Communities, in Department of Biology (University of Oregon, 1993).
– reference: Biller, S. J., Coe, A., Roggensack, S. E., Chisholm, S. W. & Mason, O. Heterotroph Interact. Alter. Prochlorococcus Transcriptome Dynamics Dur. Ext. Periods Darkn. mSystems, 3(3). (2018).
– reference: WeissbergOAharonovichDSherDPhototroph-heterotroph interactions during growth and long-term starvation across Prochlorococcus and Alteromonas diversityISME J.202217222723736335212986006410.1038/s41396-022-01330-8
– reference: MaryIDiel rhythmicity in amino acid uptake byProchlorococcusEnviron. Microbiol.2008108212421311:CAS:528:DC%2BD1cXpsFOqt7k%3D1843001910.1111/j.1462-2920.2008.01633.x
– reference: MoránXAGGasolJMPedrós-AlióCEstradaMPartitioning of phytoplanktonic organic carbon production and bacterial production along a coastal-offshore gradient in the NE Atlantic during different hydrographic regimesAquat. Microb. Ecol.20022923925210.3354/ame029239
– reference: TeiraEJosé PazóMSerretPFernándezEDissolved organic carbon production by microbial populations in the Atlantic OceanLimnol. Oceanogr.2001466137013772001LimOc..46.1370T1:CAS:528:DC%2BD3MXnsVSktbo%3D10.4319/lo.2001.46.6.1370
– reference: YeltonAPGlobal genetic capacity for mixotrophy in marine picocyanobacteriaISME J.20161012294629571:CAS:528:DC%2BC28XhvFOht7vM27137127514818810.1038/ismej.2016.64
– reference: Bohutskyi, P. et al. Metabolic effects of vitamin B12 on physiology, stress resistance, growth rate and biomass productivity of cyanobacterium stanieri planktonic and biofilm cultures. Algal Res., 42. (2019).
– reference: CoeASurvival of Prochlorococcus in extended darknessLimnol. Oceanogr.2016614137513882016LimOc..61.1375C10.1002/lno.10302
– reference: Wang, J. et al. Construction of fungi-microalgae Symbiotic System and Adsorption Study of Heavy Metal ions268 (Separation and Purification Technology, 2021).
– reference: HoneggerRFunctional aspects of the Lichen SymbiosisAnnu. Rev. Plant Physiol. Plant Mol. Biol.19914215535781:CAS:528:DyaK3MXltFSms7s%3D10.1146/annurev.pp.42.060191.003005
– reference: Jo, C. et al. Construction and modeling of a coculture microplate for real-time measurement of Microbial interactions. mSystems, 8(2). (2023).
– reference: Becker, J. W. et al. Closely Relat. Phytoplankton Species Produce Similar Suites Dissolved Org. Matter Front. Microbiol., 5. (2014).
– reference: ZuñigaCEnvironmental stimuli drive a transition from cooperation to competition in synthetic phototrophic communitiesNat. Microbiol.2019412218421913159155410.1038/s41564-019-0567-6
– reference: JardillierLZubkovMVPearmanJScanlanDJSignificant CO2 fixation by small prymnesiophytes in the subtropical and tropical northeast Atlantic OceanISME J.201049118011921:CAS:528:DC%2BC3cXhtVKgsr7E2039357510.1038/ismej.2010.36
– reference: TeelingHSubstrate-controlled succession of Marine Bacterioplankton populations Induced by a Phytoplankton BloomScience201233660816086112012Sci...336..608T1:CAS:528:DC%2BC38Xmt1Gntrw%3D2255625810.1126/science.1218344
– reference: KosugiMArabitol provided by Lichenous Fungi Enhances Ability To Dissipate Excess Light Energy in a Symbiotic Green Alga under DesiccationPlant Cell Physiol.2013548131613251:CAS:528:DC%2BC3sXht1Wlur%2FJ2373750110.1093/pcp/pct079
– reference: Stocker-WörgötterEMetabolic diversity of lichen-forming ascomycetous fungi: culturing, polyketide and shikimatemetabolite production, and PKS genesNat. Prod. Rep.20082511882001825090210.1039/B606983P
– reference: Li, T. et al. Creating a synthetic lichen: Mutualistic co-culture of fungi and extracellular polysaccharide-secreting cyanobacterium Nostoc PCC 7413. Algal Res., 45. (2020).
– reference: WeissTLYoungEJDucatDCA synthetic, light-driven consortium of cyanobacteria and heterotrophic bacteria enables stable polyhydroxybutyrate productionMetab. Eng.2017442362451:CAS:528:DC%2BC2sXhsleltb%2FF2906149210.1016/j.ymben.2017.10.009
– reference: ShannonPCytoscape: a Software Environment for Integrated Models of Biomolecular Interaction NetworksGenome Res.20031311249825041:CAS:528:DC%2BD3sXovFWrtr4%3D1459765840376910.1101/gr.1239303
– reference: MorrisJJKirkegaardRSzulMJJohnsonZIZinserERFacilitation of Robust Growth of Prochlorococcus colonies and dilute liquid cultures by helper heterotrophic BacteriaAppl. Environ. Microbiol.20087414453045342008ApEnM..74.4530M1:CAS:528:DC%2BD1cXptVeit7Y%3D18502916249317310.1128/AEM.02479-07
– reference: BohutskyiPProduction of lipid-containing algal-bacterial polyculture in wastewater and biomethanation of lipid extracted residues: enhancing methane yield through hydrothermal pretreatment and relieving solvent toxicity through co-digestionSci. Total Environ.2019653137713942019ScTEn.653.1377B1:CAS:528:DC%2BC1cXit1SnsrrP3075957710.1016/j.scitotenv.2018.11.026
– reference: FieldCBBehrenfeldMJRandersonJTFalkowskiPPrimary production of the Biosphere: integrating Terrestrial and Oceanic ComponentsScience199828153742372401998Sci...281..237F1:CAS:528:DyaK1cXksFKitb0%3D965771310.1126/science.281.5374.237
– reference: Cuhel, R. L. & Waterbury, J. B. Biochemical composition and short term nutrient incorporation patterns in a unicellular marine cyanobacterium, Synechococcus (WH7803)1. Limnology and Oceanography, 29(2): pp. 370–374. (1984).
– reference: Flombaum, P. et al. Present and future global distributions of the marine Cyanobacteria Prochlorococcus and Synechococcus. Proceedings of the National Academy of Sciences, 110(24): pp. 9824–9829. (2013).
– reference: SherDThompsonJWKashtanNCroalLChisholmSWResponse of Prochlorococcus ecotypes to co-culture with diverse marine bacteriaISME J.201157112511321:CAS:528:DC%2BC3MXnvVaqsLg%3D21326334314628810.1038/ismej.2011.1
– reference: Jahagirdar, S. & Saccenti, E. On the use of correlation and MI as a measure of Metabolite—Metabolite Association for Network Differential Connectivity Analysis. Metabolites, 10(4). (2020).
– reference: StraightPDKolterRInterspecies Chemical Communication in Bacterial DevelopmentAnnu. Rev. Microbiol.2009631991181:CAS:528:DC%2BD1MXhtlSitLvN1956642110.1146/annurev.micro.091208.073248
– reference: Muñoz-MarínMCMixotrophy in Marine picocyanobacteria: use of organic compounds by Prochlorococcus and SynechococcusISME J.20201451065107332034281717436510.1038/s41396-020-0603-9
– volume: 48
  start-page: 863
  issue: 9
  year: 2021
  ident: 74743_CR97
  publication-title: J. Genet. Genomics
  doi: 10.1016/j.jgg.2021.07.007
– volume: 8
  start-page: 593
  issue: 8
  year: 2010
  ident: 74743_CR10
  publication-title: Nat. Rev. Microbiol.
  doi: 10.1038/nrmicro2386
– volume: 4
  start-page: 1180
  issue: 9
  year: 2010
  ident: 74743_CR3
  publication-title: ISME J.
  doi: 10.1038/ismej.2010.36
– volume: 6
  start-page: 27184
  year: 2016
  ident: 74743_CR55
  publication-title: Sci. Rep.
  doi: 10.1038/srep27184
– volume: 46
  start-page: 1370
  issue: 6
  year: 2001
  ident: 74743_CR9
  publication-title: Limnol. Oceanogr.
  doi: 10.4319/lo.2001.46.6.1370
– volume: 489
  start-page: 75
  year: 2013
  ident: 74743_CR18
  publication-title: Mar. Ecol. Prog. Ser.
  doi: 10.3354/meps10428
– volume: 40
  start-page: D109
  issue: D1
  year: 2011
  ident: 74743_CR98
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gkr988
– volume: 63
  start-page: 99
  issue: 1
  year: 2009
  ident: 74743_CR50
  publication-title: Annu. Rev. Microbiol.
  doi: 10.1146/annurev.micro.091208.073248
– volume: 5
  start-page: 459
  issue: 7
  year: 2012
  ident: 74743_CR16
  publication-title: Nat. Geosci.
  doi: 10.1038/ngeo1486
– volume: 13
  start-page: 2498
  issue: 11
  year: 2003
  ident: 74743_CR80
  publication-title: Genome Res.
  doi: 10.1101/gr.1239303
– volume: 37
  start-page: W652
  issue: Web Server
  year: 2009
  ident: 74743_CR93
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gkp356
– volume: 14
  start-page: 1065
  issue: 5
  year: 2020
  ident: 74743_CR60
  publication-title: ISME J.
  doi: 10.1038/s41396-020-0603-9
– volume: 471
  start-page: 349
  issue: 7338
  year: 2011
  ident: 74743_CR13
  publication-title: Nature
  doi: 10.1038/nature09826
– volume: 6
  start-page: 650
  issue: 3
  year: 2011
  ident: 74743_CR65
  publication-title: ISME J.
  doi: 10.1038/ismej.2011.118
– ident: 74743_CR25
  doi: 10.3389/fmicb.2020.588778
– ident: 74743_CR33
  doi: 10.1128/mSystems.00040-18
– volume: 54
  start-page: 1316
  issue: 8
  year: 2013
  ident: 74743_CR47
  publication-title: Plant Cell Physiol.
  doi: 10.1093/pcp/pct079
– ident: 74743_CR83
  doi: 10.3390/metabo10040171
– volume: 49
  start-page: 1652
  issue: 5
  year: 2004
  ident: 74743_CR8
  publication-title: Limnol. Oceanogr.
  doi: 10.4319/lo.2004.49.5.1652
– volume: 25
  start-page: 188
  issue: 1
  year: 2008
  ident: 74743_CR44
  publication-title: Nat. Prod. Rep.
  doi: 10.1039/B606983P
– volume: 47
  start-page: 1730
  issue: 5
  year: 2018
  ident: 74743_CR45
  publication-title: Chem. Soc. Rev.
  doi: 10.1039/C7CS00431A
– volume: 17
  start-page: 227
  issue: 2
  year: 2022
  ident: 74743_CR29
  publication-title: ISME J.
  doi: 10.1038/s41396-022-01330-8
– volume: 10
  start-page: 2124
  issue: 8
  year: 2008
  ident: 74743_CR61
  publication-title: Environ. Microbiol.
  doi: 10.1111/j.1462-2920.2008.01633.x
– volume: 17
  start-page: 1735
  issue: 8
  year: 2022
  ident: 74743_CR92
  publication-title: Nat. Protoc.
  doi: 10.1038/s41596-022-00710-w
– volume: 44
  start-page: 236
  year: 2017
  ident: 74743_CR72
  publication-title: Metab. Eng.
  doi: 10.1016/j.ymben.2017.10.009
– ident: 74743_CR95
– volume: 42
  start-page: 553
  issue: 1
  year: 1991
  ident: 74743_CR17
  publication-title: Annu. Rev. Plant Physiol. Plant Mol. Biol.
  doi: 10.1146/annurev.pp.42.060191.003005
– volume: 61
  start-page: 1375
  issue: 4
  year: 2016
  ident: 74743_CR32
  publication-title: Limnol. Oceanogr.
  doi: 10.1002/lno.10302
– ident: 74743_CR90
  doi: 10.3389/fbioe.2021.603832
– volume: 42
  start-page: 506
  issue: 3
  year: 1997
  ident: 74743_CR5
  publication-title: Limnol. Oceanogr.
  doi: 10.4319/lo.1997.42.3.0506
– volume: 17
  start-page: 243
  issue: 4
  year: 2020
  ident: 74743_CR82
  publication-title: Expert Rev. Proteomics
  doi: 10.1080/14789450.2020.1766975
– ident: 74743_CR42
  doi: 10.1007/978-3-662-10370-8_12
– ident: 74743_CR84
  doi: 10.1128/msystems.00902-21
– volume: 97
  start-page: 35
  issue: 1
  year: 1993
  ident: 74743_CR38
  publication-title: Mycol. Res.
  doi: 10.1016/S0953-7562(09)81109-X
– volume: 83
  start-page: 761
  issue: 3
  year: 2006
  ident: 74743_CR88
  publication-title: New Phytol.
  doi: 10.1111/j.1469-8137.1979.tb02307.x
– ident: 74743_CR48
  doi: 10.1073/pnas.0407716102
– ident: 74743_CR68
  doi: 10.1016/j.seppur.2021.118689
– volume: 226
  start-page: 1287
  issue: 5
  year: 2007
  ident: 74743_CR41
  publication-title: Planta
  doi: 10.1007/s00425-007-0563-6
– ident: 74743_CR69
  doi: 10.1016/j.algal.2019.101755
– volume: 16
  start-page: 1668
  issue: 6
  year: 2014
  ident: 74743_CR22
  publication-title: Environ. Microbiol.
  doi: 10.1111/1462-2920.12242
– ident: 74743_CR81
  doi: 10.1186/1471-2105-12-436
– volume: 10
  start-page: 2946
  issue: 12
  year: 2016
  ident: 74743_CR59
  publication-title: ISME J.
  doi: 10.1038/ismej.2016.64
– volume: 260
  start-page: 68
  year: 2018
  ident: 74743_CR79
  publication-title: Bioresour. Technol.
  doi: 10.1016/j.biortech.2018.02.080
– ident: 74743_CR14
  doi: 10.1073/pnas.0832439100
– volume: 44
  start-page: 17
  issue: 1
  year: 1969
  ident: 74743_CR36
  publication-title: Biol. Rev.
  doi: 10.1111/j.1469-185X.1969.tb00821.x
– volume: 64
  start-page: 219
  issue: 2
  year: 2008
  ident: 74743_CR56
  publication-title: FEMS Microbiol. Ecol.
  doi: 10.1111/j.1574-6941.2008.00459.x
– ident: 74743_CR23
  doi: 10.3389/fmicb.2014.00111
– volume: 154
  start-page: 792
  issue: 6
  year: 2019
  ident: 74743_CR51
  publication-title: Plant. Biosystems - Int. J. Dealing all Aspects Plant. Biology
  doi: 10.1080/11263504.2019.1701117
– ident: 74743_CR6
– ident: 74743_CR1
  doi: 10.1073/pnas.1307701110
– ident: 74743_CR52
  doi: 10.3389/fmicb.2021.667864
– volume: 17
  start-page: 3781
  issue: 10
  year: 2015
  ident: 74743_CR21
  publication-title: Environ. Microbiol.
  doi: 10.1111/1462-2920.12822
– ident: 74743_CR40
  doi: 10.1016/0098-8472(94)90046-9
– ident: 74743_CR43
  doi: 10.1007/978-3-642-85243-5_2
– volume: 60
  start-page: 273
  issue: 3
  year: 2010
  ident: 74743_CR19
  publication-title: Aquat. Microb. Ecol.
  doi: 10.3354/ame01427
– volume: 111
  start-page: 17
  year: 2012
  ident: 74743_CR49
  publication-title: J. Photochem. Photobiol., B
  doi: 10.1016/j.jphotobiol.2012.03.005
– ident: 74743_CR70
  doi: 10.1186/s13068-017-0736-x
– volume: 8
  start-page: 135
  issue: 4
  year: 1989
  ident: 74743_CR67
  publication-title: Lett. Appl. Microbiol.
  doi: 10.1111/j.1472-765X.1989.tb00258.x
– ident: 74743_CR96
– ident: 74743_CR30
  doi: 10.1038/nmicrobiol.2017.100
– ident: 74743_CR66
  doi: 10.4319/lo.1984.29.2.0370
– ident: 74743_CR26
  doi: 10.1128/aem.01558-22
– ident: 74743_CR12
  doi: 10.1073/pnas.1514645113
– ident: 74743_CR34
  doi: 10.1371/journal.pone.0016805
– volume: 81
  start-page: 3429
  issue: 9
  year: 2009
  ident: 74743_CR91
  publication-title: Anal. Chem.
  doi: 10.1021/ac802689c
– volume: 281
  start-page: 237
  issue: 5374
  year: 1998
  ident: 74743_CR2
  publication-title: Science
  doi: 10.1126/science.281.5374.237
– volume: 7
  start-page: 1949
  issue: 12
  year: 2022
  ident: 74743_CR57
  publication-title: Nat. Microbiol.
  doi: 10.1038/s41564-022-01251-4
– volume: 29
  start-page: 239
  year: 2002
  ident: 74743_CR7
  publication-title: Aquat. Microb. Ecol.
  doi: 10.3354/ame029239
– volume: 5
  start-page: 1125
  issue: 7
  year: 2011
  ident: 74743_CR27
  publication-title: ISME J.
  doi: 10.1038/ismej.2011.1
– ident: 74743_CR4
– volume: 50
  start-page: 1924
  issue: 6
  year: 2005
  ident: 74743_CR63
  publication-title: Limnol. Oceanogr.
  doi: 10.4319/lo.2005.50.6.1924
– volume: 9
  start-page: 864
  issue: 12
  year: 2016
  ident: 74743_CR11
  publication-title: Nat. Geosci.
  doi: 10.1038/ngeo2841
– volume: 653
  start-page: 1377
  year: 2019
  ident: 74743_CR78
  publication-title: Sci. Total Environ.
  doi: 10.1016/j.scitotenv.2018.11.026
– volume: 157
  start-page: 21
  issue: 1
  year: 2023
  ident: 74743_CR87
  publication-title: Photosynth. Res.
  doi: 10.1007/s11120-023-01015-z
– volume: 7
  start-page: 2068
  issue: 12
  year: 2022
  ident: 74743_CR58
  publication-title: Single-cell Measurements Modelling Reveal. Substantial Org. Carbon Acquisition Prochlorococcus Nat. Microbiol.
– volume: 111
  start-page: 447
  issue: 3
  year: 1989
  ident: 74743_CR37
  publication-title: New Phytol.
  doi: 10.1111/j.1469-8137.1989.tb00707.x
– volume: 104
  start-page: 6413
  issue: 14
  year: 2020
  ident: 74743_CR71
  publication-title: Appl. Microbiol. Biotechnol.
  doi: 10.1007/s00253-020-10663-3
– volume: 314
  start-page: 652
  issue: 5799
  year: 2006
  ident: 74743_CR64
  publication-title: Dimethylsulfoniopropionate Uptake Mar. Phytoplankton Sci.
– volume: 4
  start-page: 2184
  issue: 12
  year: 2019
  ident: 74743_CR77
  publication-title: Nat. Microbiol.
  doi: 10.1038/s41564-019-0567-6
– ident: 74743_CR31
  doi: 10.1128/mBio.01846-20
– volume: 17
  start-page: 127
  year: 1994
  ident: 74743_CR39
  publication-title: Symbiosis
– ident: 74743_CR76
  doi: 10.1126/sciadv.abf4792
– volume: 336
  start-page: 608
  issue: 6081
  year: 2012
  ident: 74743_CR24
  publication-title: Science
  doi: 10.1126/science.1218344
– ident: 74743_CR74
  doi: 10.1128/msystems.00181-18
– volume: 52
  start-page: 2033
  issue: 363
  year: 2001
  ident: 74743_CR86
  publication-title: J. Exp. Bot.
  doi: 10.1093/jexbot/52.363.2033
– ident: 74743_CR73
  doi: 10.1038/s41467-020-17612-8
– ident: 74743_CR35
  doi: 10.1016/j.algal.2019.101580
– ident: 74743_CR94
– volume: 522
  start-page: 98
  issue: 7554
  year: 2015
  ident: 74743_CR53
  publication-title: Nature
  doi: 10.1038/nature14488
– volume: 57
  start-page: 2451
  issue: 12
  year: 2016
  ident: 74743_CR89
  publication-title: Plant Cell Physiol.
  doi: 10.1093/pcp/pcw169
– volume: 73
  start-page: 5539
  issue: 17
  year: 2007
  ident: 74743_CR62
  publication-title: Appl. Environ. Microbiol.
  doi: 10.1128/AEM.00212-07
– volume: 74
  start-page: 4530
  issue: 14
  year: 2008
  ident: 74743_CR28
  publication-title: Appl. Environ. Microbiol.
  doi: 10.1128/AEM.02479-07
– volume: 58
  start-page: 251
  issue: 2/3
  year: 1988
  ident: 74743_CR54
  publication-title: Polarforschung
– ident: 74743_CR20
  doi: 10.1073/pnas.0913677107
– volume: 127
  start-page: 467
  issue: 4
  year: 2002
  ident: 74743_CR46
  publication-title: J. Am. Soc. Hortic. Sci.
  doi: 10.21273/JASHS.127.4.467
– ident: 74743_CR85
  doi: 10.1128/msystems.00017-21
– volume: 28
  start-page: 71
  issue: 2
  year: 2014
  ident: 74743_CR15
  publication-title: Glob. Biogeochem. Cycles
  doi: 10.1002/2013GB004705
– ident: 74743_CR75
  doi: 10.1128/mBio.01614-21
SSID ssj0000529419
Score 2.4316602
Snippet Metabolite exchange mediates crucial interactions in microbial communities, significantly impacting global carbon and nitrogen cycling. Understanding these...
Abstract Metabolite exchange mediates crucial interactions in microbial communities, significantly impacting global carbon and nitrogen cycling. Understanding...
SourceID doaj
pubmedcentral
osti
proquest
pubmed
crossref
springer
SourceType Open Website
Open Access Repository
Aggregation Database
Index Database
Publisher
StartPage 25303
SubjectTerms 631/326/2565
631/326/2565/855
Alcohols
Amino acids
BASIC BIOLOGICAL SCIENCES
Bioreactors
Bioreactors - microbiology
Biotechnology
Carbon cycle
Carbon dioxide
Coculture Techniques - methods
Cross-feeding
Cyanobacteria - genetics
Cyanobacteria - metabolism
Environmental science
Germfree
Humanities and Social Sciences
Intermediates
Lichens
Lichens - metabolism
Lichens - microbiology
Membrane-separated bioreactor
Metabolic engineering
Metabolism
Metabolite exchange
Metabolites
Microbial activity
Microbial communities
Microbial community
Microbial Consortia
Microbial ecology
Microbial Interactions
Microbiomes
multidisciplinary
Nitrogen cycle
Phototroph-heterotroph co-culture
Rhodotorula - genetics
Rhodotorula - metabolism
Science
Science (multidisciplinary)
Sugar
Synechococcus - genetics
Synechococcus - metabolism
Synthetic lichen
Tricarboxylic acid cycle
Yeast
SummonAdditionalLinks – databaseName: DOAJ Directory of Open Access Journals
  dbid: DOA
  link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwrV1bi9QwFA6yIPgi3q27SgTfNGzbnHaaRxWXRVifVti30FyKxZ2O2FlwfoT_2e-knXHHC74IpYU2PU1yzun50qTfEeIFQDCF6Baq0D5XVGNnusopR4sy5D5vfPrgdvahPv1I7y-qi2upvnhN2EQPPHXccdfWQZcdttqRaduGTF2GEAxMr_NVgkaIedcGUxOrd2moMPNfMrlujkdEKv6brCQFBE1a0V4kSoT9OKzgWH8Cm7-vmfxl4jTFo5M74vYMJOXrqQF3xY043BM3p9SSm_vi-1n_LQbZDkEu4xJD4iGqMSaib5ye-DYgV646OW4GoECIkX7TDvDvxN_cqg2n9ZEYL4-A6H0rmewJxgp5a1jOJZfnhinA989y2S97z5_dZaIKRc2SsEteaTqMD8T5ybvzt6dqTr2gPCDdWjm_MHER6yJGjlg-1lRrR8weH1zjXGyASxZ1ZZzxLTO0A5bEqgqEwp3z-qE4GFZDfCwkubzEHYWjtiKKHd4gMe8ihq2Bp2y7TLzcasF-mQg2bJoY142ddGahM5t0ZikTb1hRu5JMjp1OwGTsbDL2XyaTiUNWswXGYKJczyuK_NqWhAZpPOJoq307-_NodVHmNQI3FZl4vrsMT-TpFWhwdZXKFJyksTGZeDQZy66e2hAzselMNHtmtNeQ_StD_ymxfQOyF4DhEPpqa3E_6_X3nnryP3rqUNwq2WMQq8vqSBysv17FpwBha_cs-dsPkNQxbA
  priority: 102
  providerName: Directory of Open Access Journals
– databaseName: Health & Medical Collection
  dbid: 7X7
  link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwfV3db9MwELdgCIkXxPfCBjISb2AtsS9O8oQAMU1I42lIfbP8FahYk7FkEv0j-J-5c9JO5UuqWilxr3bvzvezz_kdYy8RBEOIrhKF8rkAjW9NWzrhoJIh93nt04bb6Sd98hk-LsrFvOE2zMcqN3NimqhD72mP_EgVMtc4dULx5uK7oKpRlF2dS2jcZLeIuoysulpU2z0WymJB0czPyuSqPhowXtEzZRIE4mhQAnbiUaLtx48e3etvkPPPk5O_pU9TVDq-x-7OcJK_nfR_n92I3QN2eyowuX7Ifp4uf8TAbRf4Kq5wYdxFMcRE942XJ9YNlMv7lg_rDrEgiuF-bTv08sTibMWaivtwXDUPCNSXlhPlE5osyhvRfs6pPQ1MIIj_xlfL1dLT5jtPhKHYsyTsnM6bdsMjdnb84ez9iZgLMAiPwG4UzldNrKIuYqS45aMGrRwQh3xwtXOxRnRS6bJxjbfE047gJJZlAGzcOq8es72u7-I-4-Byid8oHNgSILY4j8S8jbh4DZS4bTP2aqMFczHRbJiUHle1mXRmUGcm6cxAxt6RorYtiSI7Xegvv5jZ40xrdVCyxZd20FhbQ6NlCAFNqG59aTN2QGo2iDSILtfTuSI_Ggk4IIU_cbjRvpm9ejDXNpixF9vb6I-UZEEN9lepTUGlGusmY08mY9n2UzVAfGwqY_WOGe0MZPdOt_yaOL8RuKOFSxT6emNx1_369z_19P_DOGB3JPkCxmJZHrK98fIqPkOQNbrnyZN-AdbyJ_g
  priority: 102
  providerName: ProQuest
– databaseName: Springer Nature HAS Fully OA
  dbid: AAJSJ
  link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwlV3fb9MwELbGJiReEL_JNpCReAOLJL6kyWNBTFOl8cKQ9mbFPwIVa4qWTqJ_xP5nvnPSosJ4QKpaKbm4du7O99lnfxbiNUAw-WAnKtMuVVTiq24LqyxNcp-6tHJxwu3sU3n6hWYXxcWeyDd7YeKi_UhpGbvpzeqwdz0CDW8Gy0kBAJNWdEccMFU7bPtgOp19nm1nVjh3RVk97pBJdXXLwztRKJL142cJp7oNaP69XvKPpGmMRScPxP0RRMrpUO2HYi90j8Td4VjJ9WNxczb_GbxsOi8XYYHhcBdUHyLJNy4PXBsoVy5b2a87IEAUI9266eDbkbu5UWs-0kdirNwDns8byURPMFSUt4LVXLI8N0wBun-Xi_li7njKXcZ3iprFwi55lWnXPxHnJx_PP5yq8dgF5QDnVsq6SR0mocxC4GjlQkmltsTM8d5W1oYKmGRSFrWtXcPs7IAkoSg8Qbi1Tj8V-92yC8-FJJvmeCKz1BREoUXvEdI2YMjqOV3bJuLNRgvmx0CuYWJSXFdm0JmBzkzUmaFEvGdFbSWZGDteWF59NaOhmLYpvc5bfEpLddNUVJe5975GT9W6oknEEavZAF8wSa7j1URuZXJCgzT-4nijfTP6cm90lqclgjZliXi1vQ0v5NQKNLi8jjIZH9BY1Yl4NhjLtp66JmZh04modsxopyG7d7r5t8j0DbieAYKj0Lcbi_tdr3-_qcP_Ez8S93L2DUTkvDgW-6ur6_ACUGtlX46-9QtB1Sc9
  priority: 102
  providerName: Springer Nature
Title Mixed and membrane-separated culturing of synthetic cyanobacteria-yeast consortia reveals metabolic cross-talk mimicking natural cyanolichens
URI https://link.springer.com/article/10.1038/s41598-024-74743-4
https://www.ncbi.nlm.nih.gov/pubmed/39455633
https://www.proquest.com/docview/3120699041
https://www.proquest.com/docview/3121058989
https://www.osti.gov/servlets/purl/2476534
https://pubmed.ncbi.nlm.nih.gov/PMC11511929
https://doaj.org/article/fa6d32f32f6b49aa84962ddd9048fc5a
Volume 14
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
link http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwfV1ba9swFBa9MNjL2H1uu-DB3jZttizfHsZIQ0sJpIythbwJS5a3sMRZ4xSaH7H_vO_ITka2bBBikJUTSedI59PtO4y9BgiWpdUpDyMTcJngK69izbVMRRmYIDNuwW10mVxcy-E4Hu-xdbijrgGbnVM7iid1vZi-u7tZfUSH_9BeGc_eN3BCdFFMSA5wLCMu99khPFNKEQ1GHdxvub5FLl2sDyJh5wATortHs1vMlq9ylP54zNH1dsHRv09V_rG16jzW-UP2oIOafr-1jUdsz9aP2b02-OTqCfs5mtzZ0i_q0p_ZGSbNteWNdVTgSG4ZOSDXn1d-s6qBEyHGN6uixgjgGJ4LvqLAPz5m1A3ab1L4RAeFZoW8JWxrSvmpYhxt-92fTWYTQwvzviMTRcmcsCmdRa2bp-zq_OxqcMG74AzcAPQtuTZpblObhNaSTzM2kUmkJfHLlzrT2mZALmkS5zo3BXG4A7jYOC4lMlfaRM_YQT2v7QvmSx0I_CLUsoiltBXGGBtUFhPbkjZ1K4-9WWtB_WgpOJTbOo8y1epMQWfK6UxJj52SojY5iT7bJcwXX1XXG1VVJGUkKnwSLfOiyGSeiLIsc4xnlYkLjx2TmhVQCFHpGjpzZJZKSFQowl-crLWv1garolAECVy7DD32avMafZU2YKDB-a3LE1IYxyz32PPWWDbljHJJXG2Rx7ItM9qqyPabevLN8YED1IcA6hD6dm1xv8v175Y6-m8lj9l9QV0BblrEJ-xgubi1L4G_lrrH9tNx2mOH_f7wyxDP07PLT5-ROkgGPbem0XPd7hdwTzLo
linkProvider Scholars Portal
linkToHtml http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwtV1Jb9NAFB6VIgQXxI5pgUGCE4zqZbwdEGKrWtr0FKTcRp7FENHYpU4F-RH8FP4j3xvHqcJ2qxQlkj15mcnb542_x9hTBMHSOp2LKDGhkBneyjrVQss8tqEJC-M33EZH2d5H-WGSTjbYz-FZGDpWOdhEb6hta2iPfCeJ4jCD6ZTRq5OvgrpGUXV1aKHRi8WBW3xDyta93H8H_j6L493347d7YtlVQBhEK3OhTV663GWRc2SMjctklmhJwOhWF1q7Ai43z9JSl6Yi8HF4XJemVmJwrU0CspfYZfjdkHK9fJKvtnSoaCajcvloTpgUOx3cIz3CFkuBsF0mQq65P98lAB8ttPlvEe6fBzV_q9Z6J7h7g11fRq_8dS9uN9mGa26xK30_y8Vt9mM0_e4srxrLZ26GPLxxonMeXRyXe5AP0OVtzbtFg9ATZLhZVA2MigeNrsSCeglxJOkd8oJpxQlhChoCenOI6zGNp4UJ5Axf-Gw6mxra6-cenxQz88SO6Xhr091h44vgzF222bSNu8-41GGMb0RaVqmUrobZcmHtkCtbqhPXAXs-cEGd9Kgeylfjk0L1PFPgmfI8UzJgb4hRq5GEyO0vtKef1FLBVV1lNolrvDIty6oqZJnF1lpIbFGbtArYFrFZIbAhdF5Dx5jMXMUSC0rwE9sD99XSiHTqXOQD9mR1G-pPNR1wsD3zYyLqDFmUAbvXC8tqnkkpCf4tCVixJkZrC1m_00w_e4hx5AkRYn8QfTFI3Pm8_v1PPfj_Mh6zq3vj0aE63D862GLXYtILhAFxus0256dn7iHiu7l-5LWKM3XBWvwLL7Bjnw
linkToPdf http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwtV1Zb9QwELbKViBeEDehBYwET2BtYjvXA0KUdtVSuqpQkfpmxUdgRTcpzVaQH8EP4t8x4yRbLddbpdWulDizdubwjMf-hpBn4ARL63TKImFCJhP4ystYMy1TbkMTZsYvuB1Mk92P8t1xfLxGfg5nYXBb5WATvaG2tcE18rGIeJiA6ZTRuOy3RRxuT16ffmVYQQozrUM5jU5E9l37DcK35tXeNvD6OeeTnaO3u6yvMMAMeC4Lpk2au9QlkXNomI1LZCK0RJB0qzOtXQbTb5rEuc5NgUDkMPu6OLYSGpfaCCB7haynGBSNyPrWzvTww3KBB1NoMsr7gzqhyMYNTJZ4oI1LBk68FEyuTIa-ZgD81KDbf_N3_9y2-Vvu1k-Jk5vkRu_L0jed8N0ia666Ta521S3bO-THwey7s7SoLJ27OUTllWON81jjcLmD_AC6tC5p01bgiAIZatqiAhPjIaQL1mJlIQohewNRwqygiDcF-gL0FiC8J9geB8YggvhC57P5zODKP_VopdAzT-wEN7tWzV1ydBm8uUdGVV25B4RKHXJ4ItKyiKV0JRgxF5YOImeLWeMyIC8GLqjTDuND-dy8yFTHMwU8U55nSgZkCxm1bIn43P5CffZJ9equyiKxgpfwSbTMiyKTecKttSC_WWniIiAbyGYFbg5i9Rrc1GQWiksYkIC_2By4r3qT0qgLBQjI0-VtMAaY4QEO1ue-TYR1IrM8IPc7YVn2U-QSweBEQLIVMVoZyOqdavbZA45D1BBBJABEXw4Sd9Gvf7-ph_8fxhNyDTRYvd-b7m-Q6xzVAnwCHm-S0eLs3D0CZ2-hH_dqRYm6ZEX-Bb67aTo
openUrl ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Mixed+and+membrane-separated+culturing+of+synthetic+cyanobacteria-yeast+consortia+reveals+metabolic+cross-talk+mimicking+natural+cyanolichens&rft.jtitle=Scientific+reports&rft.au=Bohutskyi%2C+Pavlo&rft.au=Pomraning%2C+Kyle+R.&rft.au=Jenkins%2C+Jackson+P.&rft.au=Kim%2C+Young-Mo&rft.date=2024-10-25&rft.pub=Nature+Publishing+Group&rft.issn=2045-2322&rft.eissn=2045-2322&rft.volume=14&rft.issue=1&rft_id=info:doi/10.1038%2Fs41598-024-74743-4&rft.externalDocID=2476534
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=2045-2322&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=2045-2322&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=2045-2322&client=summon