Forfeiting the priority effect: turnover defines biofilm community succession

Microbial community succession is a fundamental process that affects underlying functions of almost all ecosystems; yet the roles and fates of the most abundant colonizers are often poorly understood. Does early abundance spur long term persistence? How do deterministic and stochastic processes infl...

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Published inThe ISME Journal Vol. 13; no. 7; pp. 1865 - 1877
Main Authors Brislawn, Colin J., Graham, Emily B., Dana, Karl, Ihardt, Peter, Fansler, Sarah J., Chrisler, William B., Cliff, John B., Stegen, James C., Moran, James J., Bernstein, Hans C.
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 01.07.2019
Oxford University Press
Springer Nature
Subjects
Online AccessGet full text
ISSN1751-7362
1751-7370
1751-7370
DOI10.1038/s41396-019-0396-x

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Abstract Microbial community succession is a fundamental process that affects underlying functions of almost all ecosystems; yet the roles and fates of the most abundant colonizers are often poorly understood. Does early abundance spur long term persistence? How do deterministic and stochastic processes influence the ecological contribution of colonizers? We performed a succession experiment within a hypersaline ecosystem to investigate how different processes contributed to the turnover of founder species. Bacterial and eukaryotic colonizers were identified during primary succession and tracked through a defined, 79-day biofilm maturation period using 16S and 18S rRNA gene sequencing in combination with high resolution imaging that utilized stable isotope tracers to evaluate successional patterns of primary producers and nitrogen fixers. The majority of the founder species did not maintain high abundance throughout succession. Species replacement (versus loss) was the dominant process shaping community succession. We also asked if different ecological processes acted on bacteria versus Eukaryotes during succession and found deterministic and stochastic forces corresponded more with microeukaryote and bacterial colonization, respectively. Our results show that taxa and functions belonging to different kingdoms, which share habitat in the tight spatial confines of a biofilm, were influenced by different ecological processes and time scales of succession.
AbstractList Microbial community succession is a fundamental process that affects underlying functions of almost all ecosystems; yet the roles and fates of the most abundant colonizers are often poorly understood. Does early abundance spur long term persistence? How do deterministic and stochastic processes influence the ecological contribution of colonizers? We performed a succession experiment within a hypersaline ecosystem to investigate how different processes contributed to the turnover of founder species. Bacterial and eukaryotic colonizers were identified during primary succession and tracked through a defined, 79-day biofilm maturation period using 16S and 18S rRNA gene sequencing in combination with high resolution imaging that utilized stable isotope tracers to evaluate successional patterns of primary producers and nitrogen fixers. The majority of the founder species did not maintain high abundance throughout succession. Species replacement (versus loss) was the dominant process shaping community succession. We also asked if different ecological processes acted on bacteria versus Eukaryotes during succession and found deterministic and stochastic forces corresponded more with microeukaryote and bacterial colonization, respectively. Our results show that taxa and functions belonging to different kingdoms, which share habitat in the tight spatial confines of a biofilm, were influenced by different ecological processes and time scales of succession.
Microbial community succession is a fundamental process that affects underlying functions of almost all ecosystems; yet the roles and fates of the most abundant colonizers are often poorly understood. Does early abundance spur long term persistence? How do deterministic and stochastic processes influence the ecological contribution of colonizers? We performed a succession experiment within a hypersaline ecosystem to investigate how different processes contributed to the turnover of founder species. Bacterial and eukaryotic colonizers were identified during primary succession and tracked through a defined, 79-day biofilm maturation period using 16S and 18S rRNA gene sequencing in combination with high resolution imaging that utilized stable isotope tracers to evaluate successional patterns of primary producers and nitrogen fixers. The majority of the founder species did not maintain high abundance throughout succession. Species replacement (versus loss) was the dominant process shaping community succession. We also asked if different ecological processes acted on bacteria versus Eukaryotes during succession and found deterministic and stochastic forces corresponded more with microeukaryote and bacterial colonization, respectively. Our results show that taxa and functions belonging to different kingdoms, which share habitat in the tight spatial confines of a biofilm, were influenced by different ecological processes and time scales of succession.Microbial community succession is a fundamental process that affects underlying functions of almost all ecosystems; yet the roles and fates of the most abundant colonizers are often poorly understood. Does early abundance spur long term persistence? How do deterministic and stochastic processes influence the ecological contribution of colonizers? We performed a succession experiment within a hypersaline ecosystem to investigate how different processes contributed to the turnover of founder species. Bacterial and eukaryotic colonizers were identified during primary succession and tracked through a defined, 79-day biofilm maturation period using 16S and 18S rRNA gene sequencing in combination with high resolution imaging that utilized stable isotope tracers to evaluate successional patterns of primary producers and nitrogen fixers. The majority of the founder species did not maintain high abundance throughout succession. Species replacement (versus loss) was the dominant process shaping community succession. We also asked if different ecological processes acted on bacteria versus Eukaryotes during succession and found deterministic and stochastic forces corresponded more with microeukaryote and bacterial colonization, respectively. Our results show that taxa and functions belonging to different kingdoms, which share habitat in the tight spatial confines of a biofilm, were influenced by different ecological processes and time scales of succession.
Author Cliff, John B.
Brislawn, Colin J.
Ihardt, Peter
Fansler, Sarah J.
Stegen, James C.
Graham, Emily B.
Moran, James J.
Dana, Karl
Bernstein, Hans C.
Chrisler, William B.
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/30886318$$D View this record in MEDLINE/PubMed
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PublicationCentury 2000
PublicationDate 2019-07-01
PublicationDateYYYYMMDD 2019-07-01
PublicationDate_xml – month: 07
  year: 2019
  text: 2019-07-01
  day: 01
PublicationDecade 2010
PublicationPlace London
PublicationPlace_xml – name: London
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PublicationSubtitle Multidisciplinary Journal of Microbial Ecology
PublicationTitle The ISME Journal
PublicationTitleAbbrev ISME J
PublicationTitleAlternate ISME J
PublicationYear 2019
Publisher Nature Publishing Group UK
Oxford University Press
Springer Nature
Publisher_xml – name: Nature Publishing Group UK
– name: Oxford University Press
– name: Springer Nature
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Snippet Microbial community succession is a fundamental process that affects underlying functions of almost all ecosystems; yet the roles and fates of the most...
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SubjectTerms 45/23
45/77
631/158/855
631/326/171
Abundance
Bacteria
Bacteria - classification
Bacteria - genetics
Basale biofag: 470
Basic biosciences: 470
Biofilms
Biomedical and Life Sciences
Colonization
Communities
Ecological effects
Ecological succession
Ecology
Ecosystems
Eukaryotes
Evolutionary Biology
Gene sequencing
General microbiology: 472
Generell mikrobiologi: 472
Image resolution
Life Sciences
Matematikk og Naturvitenskap: 400
Mathematics and natural science: 400
Microbial Ecology
Microbial Genetics and Genomics
Microbiology
Microbiota
Microorganisms
rRNA 16S
rRNA 18S
Species
Stable isotopes
Stochastic Processes
Tracers
VDP
Title Forfeiting the priority effect: turnover defines biofilm community succession
URI https://link.springer.com/article/10.1038/s41396-019-0396-x
https://www.ncbi.nlm.nih.gov/pubmed/30886318
https://www.proquest.com/docview/2244140290
https://www.proquest.com/docview/2194138684
http://hdl.handle.net/10037/16570
https://pubmed.ncbi.nlm.nih.gov/PMC6775999
Volume 13
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