Microbial Gut Diversity of Africanized and European Honey Bee Larval Instars
The first step in understanding gut microbial ecology is determining the presence and potential niche breadth of associated microbes. While the core gut bacteria of adult honey bees is becoming increasingly apparent, there is very little and inconsistent information concerning symbiotic bacterial co...
Saved in:
Published in | PloS one Vol. 8; no. 8; p. e72106 |
---|---|
Main Authors | , , , |
Format | Journal Article |
Language | English |
Published |
United States
Public Library of Science
21.08.2013
Public Library of Science (PLoS) |
Subjects | |
Online Access | Get full text |
Cover
Loading…
Abstract | The first step in understanding gut microbial ecology is determining the presence and potential niche breadth of associated microbes. While the core gut bacteria of adult honey bees is becoming increasingly apparent, there is very little and inconsistent information concerning symbiotic bacterial communities in honey bee larvae. The larval gut is the target of highly pathogenic bacteria and fungi, highlighting the need to understand interactions between typical larval gut flora, nutrition and disease progression. Here we show that the larval gut is colonized by a handful of bacterial groups previously described from guts of adult honey bees or other pollinators. First and second larval instars contained almost exclusively Alpha 2.2, a core Acetobacteraceae, while later instars were dominated by one of two very different Lactobacillus spp., depending on the sampled site. Royal jelly inhibition assays revealed that of seven bacteria occurring in larvae, only one Neisseriaceae and one Lactobacillus sp. were inhibited. We found both core and environmentally vectored bacteria with putatively beneficial functions. Our results suggest that early inoculation by Acetobacteraceae may be important for microbial succession in larvae. This assay is a starting point for more sophisticated in vitro models of nutrition and disease resistance in honey bee larvae. |
---|---|
AbstractList | The first step in understanding gut microbial ecology is determining the presence and potential niche breadth of associated microbes. While the core gut bacteria of adult honey bees is becoming increasingly apparent, there is very little and inconsistent information concerning symbiotic bacterial communities in honey bee larvae. The larval gut is the target of highly pathogenic bacteria and fungi, highlighting the need to understand interactions between typical larval gut flora, nutrition and disease progression. Here we show that the larval gut is colonized by a handful of bacterial groups previously described from guts of adult honey bees or other pollinators. First and second larval instars contained almost exclusively Alpha 2.2, a core Acetobacteraceae, while later instars were dominated by one of two very different Lactobacillus spp., depending on the sampled site. Royal jelly inhibition assays revealed that of seven bacteria occurring in larvae, only one Neisseriaceae and one Lactobacillus sp. were inhibited. We found both core and environmentally vectored bacteria with putatively beneficial functions. Our results suggest that early inoculation by Acetobacteraceae may be important for microbial succession in larvae. This assay is a starting point for more sophisticated in vitro models of nutrition and disease resistance in honey bee larvae. The first step in understanding gut microbial ecology is determining the presence and potential niche breadth of associated microbes. While the core gut bacteria of adult honey bees is becoming increasingly apparent, there is very little and inconsistent information concerning symbiotic bacterial communities in honey bee larvae. The larval gut is the target of highly pathogenic bacteria and fungi, highlighting the need to understand interactions between typical larval gut flora, nutrition and disease progression. Here we show that the larval gut is colonized by a handful of bacterial groups previously described from guts of adult honey bees or other pollinators. First and second larval instars contained almost exclusively Alpha 2.2, a core Acetobacteraceae, while later instars were dominated by one of two very different Lactobacillus spp., depending on the sampled site. Royal jelly inhibition assays revealed that of seven bacteria occurring in larvae, only one Neisseriaceae and one Lactobacillus sp. were inhibited. We found both core and environmentally vectored bacteria with putatively beneficial functions. Our results suggest that early inoculation by Acetobacteraceae may be important for microbial succession in larvae. This assay is a starting point for more sophisticated in vitro models of nutrition and disease resistance in honey bee larvae. |
Audience | Academic |
Author | Rehan, Sandra M Smagghe, Guy Anderson, Kirk E Vojvodic, Svjetlana |
AuthorAffiliation | 2 Department of Biology, University of Pennsylvania, Philadelphia, Pennsylvania, United States of America 3 United States Department of Agriculture, Tucson, Arizona, United States of America Ghent University, Belgium 1 Center for Insect Science, Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona, United States of America |
AuthorAffiliation_xml | – name: Ghent University, Belgium – name: 1 Center for Insect Science, Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona, United States of America – name: 3 United States Department of Agriculture, Tucson, Arizona, United States of America – name: 2 Department of Biology, University of Pennsylvania, Philadelphia, Pennsylvania, United States of America |
Author_xml | – sequence: 1 fullname: Vojvodic, Svjetlana – sequence: 2 fullname: Rehan, Sandra M – sequence: 3 fullname: Anderson, Kirk E – sequence: 4 fullname: Smagghe, Guy |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/23991051$$D View this record in MEDLINE/PubMed |
BookMark | eNqNk99v0zAQxyM0xLbCf4AgEhKChxb_iJP4BamMsVUqmsQYr9bFsVtPqd3ZSUX563FoNxq0B5SHROfPfe98981pcmSdVUnyEqMJpgX-cOs6b6GZrGN4glBBMMqfJCeYUzLOCaJHB9_HyWkItwgxWub5s-SYUM4xYvgkmX810rvKQJNedG362WyUD6bdpk6nU-2NBGt-qToFW6fnnXdrBTa9jCW36Sel0jn4TUyd2dCCD8-TpxqaoF7s36Pk5sv597PL8fzqYnY2nY9lUZJ2DKTMudaSqIJLHjtXpKSIqYqBwoVENa0IVywjjGlZZZorQjhkoDTNuC4pHSWvd7rrxgWxH0QQOKOoKAtC80jMdkTt4FasvVmB3woHRvwJOL8Q4FsjGyUYIMaLEnRdyQw4qjhlVVVnsTuoCtxrfdxX66qVqqWyrYdmIDo8sWYpFm4jaJHFKRdR4N1ewLu7ToVWrEyQqmnAKtf1fRNOMCNxXaPkzT_o47fbUwuIFzBWu1hX9qJimhUlLnOEemryCBWfWq2MjCvUJsYHCe8HCZFp1c92AV0IYnb97f_Zqx9D9u0Bu1TQtMvgmq41zoYhmO3AaMkQvNIPQ8ZI9Ka_n4boTS_2po9prw4X9JB07_K_ftHgBCy8CeLmmiAciyIU_whGfwOo0gYH |
CitedBy_id | crossref_primary_10_1080_00218839_2021_2020950 crossref_primary_10_1371_journal_pone_0118707 crossref_primary_10_1128_genomeA_00165_18 crossref_primary_10_1128_AEM_02043_14 crossref_primary_10_3390_insects11070439 crossref_primary_10_1016_j_cois_2015_04_003 crossref_primary_10_1038_s41598_018_19860_7 crossref_primary_10_1186_s40168_018_0489_1 crossref_primary_10_1111_1744_7917_12155 crossref_primary_10_1111_1744_7917_13365 crossref_primary_10_1128_MRA_01329_19 crossref_primary_10_1371_journal_pone_0078296 crossref_primary_10_1093_aesa_sav079 crossref_primary_10_1111_1744_7917_12271 crossref_primary_10_1371_journal_pone_0095056 crossref_primary_10_3389_fmicb_2017_01942 crossref_primary_10_3390_pathogens12050734 crossref_primary_10_3390_insects11090555 crossref_primary_10_3390_insects14030265 crossref_primary_10_1038_s41598_021_85153_1 crossref_primary_10_1128_AEM_01861_14 crossref_primary_10_3389_fmicb_2022_1099522 crossref_primary_10_3920_JIFF2018_0021 crossref_primary_10_3390_microorganisms11051130 crossref_primary_10_1016_j_jip_2021_107589 crossref_primary_10_1128_mBio_00503_21 crossref_primary_10_1016_j_syapm_2024_126505 crossref_primary_10_2478_jas_2020_0002 crossref_primary_10_1007_s13592_015_0392_8 crossref_primary_10_1128_AEM_00307_15 crossref_primary_10_1002_mnfr_201600520 crossref_primary_10_1038_nrmicro_2016_43 crossref_primary_10_1080_00218839_2024_2343980 crossref_primary_10_1093_gbe_evv079 crossref_primary_10_1186_s12862_014_0260_6 crossref_primary_10_3389_frbee_2024_1410331 crossref_primary_10_1080_00218839_2023_2245211 crossref_primary_10_1098_rstb_2021_0156 crossref_primary_10_1128_AEM_01259_15 crossref_primary_10_3389_fmicb_2020_571903 crossref_primary_10_1016_j_foodcont_2024_110678 crossref_primary_10_1264_jsme2_ME18169 crossref_primary_10_3390_ijms25020741 crossref_primary_10_3390_insects11040250 crossref_primary_10_1007_s42690_023_01147_8 crossref_primary_10_1098_rsos_201805 crossref_primary_10_1038_s41598_019_56699_y crossref_primary_10_1128_AEM_01290_18 crossref_primary_10_1080_2314808X_2021_1902046 crossref_primary_10_1590_1809_4392202000902 crossref_primary_10_3390_pr8091081 crossref_primary_10_1007_s13213_018_1350_2 crossref_primary_10_1016_j_syapm_2016_09_006 crossref_primary_10_1186_s12866_019_1490_y crossref_primary_10_1007_s00248_016_0838_1 crossref_primary_10_1002_ece3_5599 crossref_primary_10_1099_ijsem_0_001921 crossref_primary_10_1016_j_micres_2023_127587 crossref_primary_10_7717_peerj_7478 crossref_primary_10_1128_spectrum_00383_22 crossref_primary_10_1128_aem_01799_23 crossref_primary_10_1371_journal_pone_0174614 crossref_primary_10_1007_s00248_022_02025_5 crossref_primary_10_1038_ismej_2014_68 crossref_primary_10_1016_j_micpath_2019_103793 crossref_primary_10_1111_1462_2920_16379 crossref_primary_10_1038_s41396_022_01268_x crossref_primary_10_1371_journal_pone_0132014 crossref_primary_10_1016_j_celrep_2024_114408 crossref_primary_10_3390_microorganisms12040635 crossref_primary_10_1093_femsre_fuab056 crossref_primary_10_1111_mec_12966 crossref_primary_10_1093_gbe_evz136 crossref_primary_10_1099_ijsem_0_004950 crossref_primary_10_1007_s00248_015_0716_2 crossref_primary_10_1039_C4NP00158C crossref_primary_10_1093_femsre_fux030 crossref_primary_10_1007_s10482_015_0384_8 crossref_primary_10_3390_microorganisms10122359 crossref_primary_10_4081_jear_2022_10316 crossref_primary_10_1016_j_mib_2019_08_001 crossref_primary_10_1021_acs_jafc_8b02212 crossref_primary_10_1016_j_cois_2017_05_020 crossref_primary_10_31467_uluaricilik_701170 crossref_primary_10_1371_journal_pone_0134542 crossref_primary_10_3389_finsc_2021_756690 crossref_primary_10_1038_ismej_2015_253 crossref_primary_10_3390_insects13090772 crossref_primary_10_1007_s42770_021_00539_7 crossref_primary_10_1016_j_jip_2020_107521 crossref_primary_10_1088_1755_1315_924_1_012079 crossref_primary_10_1093_jee_tow012 crossref_primary_10_1080_00218839_2018_1428047 crossref_primary_10_1371_journal_pone_0225845 crossref_primary_10_1186_s12864_019_5844_5 crossref_primary_10_1080_21597081_2015_1080787 crossref_primary_10_1186_s13765_019_0415_7 crossref_primary_10_1016_j_sjbs_2017_01_055 crossref_primary_10_1371_journal_pcbi_1007109 crossref_primary_10_1111_1574_6941_12302 crossref_primary_10_3390_insects11070453 crossref_primary_10_1007_s13592_022_00934_5 crossref_primary_10_1128_mBio_02966_21 crossref_primary_10_1002_edn3_291 crossref_primary_10_1111_1462_2920_12526 crossref_primary_10_1007_s13592_016_0478_y crossref_primary_10_1093_gbe_evaa183 crossref_primary_10_7717_peerj_1329 crossref_primary_10_1111_mec_13862 crossref_primary_10_3390_insects12040301 crossref_primary_10_1016_j_ibmb_2017_06_002 crossref_primary_10_1038_s41598_019_39097_2 crossref_primary_10_1007_s13213_016_1226_2 crossref_primary_10_1016_j_jinsphys_2023_104601 crossref_primary_10_1038_s41684_018_0173_x crossref_primary_10_1093_jisesa_iead013 crossref_primary_10_1016_j_envpol_2023_122200 crossref_primary_10_1002_ecm_1560 crossref_primary_10_1016_j_foodres_2019_108672 crossref_primary_10_1111_1744_7917_12381 crossref_primary_10_1007_s00203_023_03416_z crossref_primary_10_1186_s12866_017_1133_0 crossref_primary_10_3389_fmicb_2023_1117077 |
Cites_doi | 10.1093/aesa/64.1.315 10.1002/psc.1316 10.1073/pnas.0907926106 10.1051/apido:19790304 10.4159/9780674043404 10.1128/AEM.02839-08 10.1126/science.1149357 10.1111/j.1558-5646.2008.00348.x 10.1111/j.1365-294X.2010.04959.x 10.1016/S0014-5793(02)03272-6 10.1073/pnas.0712205105 10.1371/journal.pone.0041250 10.1128/AEM.07810-11 10.1093/nar/22.22.4673 10.1051/apido:19660302 10.1016/j.cmet.2011.07.012 10.1371/journal.pone.0036393 10.1186/1472-6785-6-4 10.1111/j.1462-2920.2005.00893.x 10.1016/j.jff.2011.12.007 10.1371/journal.pone.0010831 10.1051/apido:19790106 10.1016/S0378-1097(97)00337-6 10.1093/nar/gkf436 10.1021/jf802494e 10.1099/ijs.0.031054-0 10.1051/apido:2008063 10.1146/annurev.ento.49.061802.123416 10.1111/j.0030-1299.2005.13417.x 10.3896/IBRA.4.02.3.02 10.1046/j.1472-765x.2000.00746.x 10.1007/s00284-008-9202-0 10.1073/pnas.0611659104 10.1186/1471-2180-12-S1-S2 10.1016/j.vetmic.2010.10.001 10.1126/science.1212782 10.1111/j.1574-6941.2011.01216.x 10.1128/AEM.30.6.893-896.1975 10.1111/j.1574-6941.2006.00249.x 10.1016/0022-2011(87)90127-3 10.1073/pnas.1202970109 10.1016/j.jip.2003.08.007 10.1007/s00248-011-9854-3 10.1111/j.1365-294X.2012.05496.x 10.1016/j.syapm.2009.08.002 10.1051/apido/2009065 10.1007/s00040-011-0194-6 10.3844/ajassp.2012.807.817 10.1371/journal.pone.0033188 10.1016/j.peptides.2004.03.016 10.1099/00221287-76-1-211 10.1126/science.1146498 10.1007/s00284-012-0186-4 |
ContentType | Journal Article |
Copyright | COPYRIGHT 2013 Public Library of Science 2013. This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2013 |
Copyright_xml | – notice: COPYRIGHT 2013 Public Library of Science – notice: 2013. This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. – notice: 2013 |
DBID | FBQ CGR CUY CVF ECM EIF NPM AAYXX CITATION IOV ISR 3V. 7QG 7QL 7QO 7RV 7SN 7SS 7T5 7TG 7TM 7U9 7X2 7X7 7XB 88E 8AO 8C1 8FD 8FE 8FG 8FH 8FI 8FJ 8FK ABJCF ABUWG AFKRA ARAPS ATCPS AZQEC BBNVY BENPR BGLVJ BHPHI C1K CCPQU D1I DWQXO FR3 FYUFA GHDGH GNUQQ H94 HCIFZ K9. KB. KB0 KL. L6V LK8 M0K M0S M1P M7N M7P M7S NAPCQ P5Z P62 P64 PATMY PDBOC PIMPY PQEST PQQKQ PQUKI PRINS PTHSS PYCSY RC3 7X8 5PM DOA |
DOI | 10.1371/journal.pone.0072106 |
DatabaseName | AGRIS Medline MEDLINE MEDLINE (Ovid) MEDLINE MEDLINE PubMed CrossRef Opposing Viewpoints In Context Gale In Context: Science ProQuest Central (Corporate) Animal Behavior Abstracts Bacteriology Abstracts (Microbiology B) Biotechnology Research Abstracts Nursing & Allied Health Database Ecology Abstracts Entomology Abstracts (Full archive) Immunology Abstracts Meteorological & Geoastrophysical Abstracts Nucleic Acids Abstracts Virology and AIDS Abstracts Agricultural Science Collection Health & Medical Collection ProQuest Central (purchase pre-March 2016) Medical Database (Alumni Edition) ProQuest Pharma Collection Public Health Database Technology Research Database ProQuest SciTech Collection ProQuest Technology Collection ProQuest Natural Science Collection Hospital Premium Collection Hospital Premium Collection (Alumni Edition) ProQuest Central (Alumni) (purchase pre-March 2016) Materials Science & Engineering Collection ProQuest Central (Alumni) ProQuest Central Advanced Technologies & Aerospace Database (1962 - current) Agricultural & Environmental Science Collection ProQuest Central Essentials Biological Science Collection ProQuest Central Technology Collection ProQuest Natural Science Collection Environmental Sciences and Pollution Management ProQuest One Community College ProQuest Materials Science Collection ProQuest Central Korea Engineering Research Database Health Research Premium Collection Health Research Premium Collection (Alumni) ProQuest Central Student AIDS and Cancer Research Abstracts SciTech Premium Collection ProQuest Health & Medical Complete (Alumni) Materials Science Database Nursing & Allied Health Database (Alumni Edition) Meteorological & Geoastrophysical Abstracts - Academic ProQuest Engineering Collection Biological Sciences Agricultural Science Database Health & Medical Collection (Alumni Edition) PML(ProQuest Medical Library) Algology Mycology and Protozoology Abstracts (Microbiology C) Biological Science Database Engineering Database Nursing & Allied Health Premium Advanced Technologies & Aerospace Database ProQuest Advanced Technologies & Aerospace Collection Biotechnology and BioEngineering Abstracts Environmental Science Database Materials Science Collection Publicly Available Content Database ProQuest One Academic Eastern Edition (DO NOT USE) ProQuest One Academic ProQuest One Academic UKI Edition ProQuest Central China Engineering Collection Environmental Science Collection Genetics Abstracts MEDLINE - Academic PubMed Central (Full Participant titles) Directory of Open Access Journals |
DatabaseTitle | MEDLINE Medline Complete MEDLINE with Full Text PubMed MEDLINE (Ovid) CrossRef Agricultural Science Database Publicly Available Content Database ProQuest Central Student ProQuest Advanced Technologies & Aerospace Collection ProQuest Central Essentials Nucleic Acids Abstracts SciTech Premium Collection ProQuest Central China Environmental Sciences and Pollution Management Health Research Premium Collection Meteorological & Geoastrophysical Abstracts Natural Science Collection Biological Science Collection ProQuest Medical Library (Alumni) Engineering Collection Advanced Technologies & Aerospace Collection Engineering Database Virology and AIDS Abstracts ProQuest Biological Science Collection ProQuest One Academic Eastern Edition Agricultural Science Collection ProQuest Hospital Collection ProQuest Technology Collection Health Research Premium Collection (Alumni) Biological Science Database Ecology Abstracts ProQuest Hospital Collection (Alumni) Biotechnology and BioEngineering Abstracts Environmental Science Collection Entomology Abstracts Nursing & Allied Health Premium ProQuest Health & Medical Complete ProQuest One Academic UKI Edition Environmental Science Database ProQuest Nursing & Allied Health Source (Alumni) Engineering Research Database ProQuest One Academic Meteorological & Geoastrophysical Abstracts - Academic Technology Collection Technology Research Database Materials Science Collection ProQuest Health & Medical Complete (Alumni) ProQuest Central (Alumni Edition) ProQuest One Community College ProQuest Natural Science Collection ProQuest Pharma Collection ProQuest Central Genetics Abstracts ProQuest Engineering Collection Biotechnology Research Abstracts Health and Medicine Complete (Alumni Edition) ProQuest Central Korea Bacteriology Abstracts (Microbiology B) Algology Mycology and Protozoology Abstracts (Microbiology C) Agricultural & Environmental Science Collection AIDS and Cancer Research Abstracts Materials Science Database ProQuest Materials Science Collection ProQuest Public Health ProQuest Nursing & Allied Health Source ProQuest SciTech Collection Advanced Technologies & Aerospace Database ProQuest Medical Library Animal Behavior Abstracts Materials Science & Engineering Collection Immunology Abstracts ProQuest Central (Alumni) MEDLINE - Academic |
DatabaseTitleList | MEDLINE MEDLINE - Academic Agricultural Science Database |
Database_xml | – sequence: 1 dbid: DOA name: Directory of Open Access Journals url: https://www.doaj.org/ sourceTypes: Open Website – sequence: 2 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: 3 dbid: EIF name: MEDLINE url: https://proxy.k.utb.cz/login?url=https://www.webofscience.com/wos/medline/basic-search sourceTypes: Index Database – sequence: 4 dbid: 8FG name: ProQuest Technology Collection url: https://search.proquest.com/technologycollection1 sourceTypes: Aggregation Database – sequence: 5 dbid: FBQ name: AGRIS url: http://www.fao.org/agris/Centre.asp?Menu_1ID=DB&Menu_2ID=DB1&Language=EN&Content=http://www.fao.org/agris/search?Language=EN sourceTypes: Publisher |
DeliveryMethod | fulltext_linktorsrc |
Discipline | Sciences (General) Ecology Biology |
DocumentTitleAlternate | Gut Microbiota of Honey Bee Larvae |
EISSN | 1932-6203 |
Editor | Smagghe, Guy |
Editor_xml | – sequence: 1 givenname: Guy surname: Smagghe fullname: Smagghe, Guy |
EndPage | e72106 |
ExternalDocumentID | 1430787236 oai_doaj_org_article_5a05978afdbc4a90b935bbd42e7ab716 3066046081 A478186006 10_1371_journal_pone_0072106 23991051 US201600008665 |
Genre | Journal Article Research Support, N.I.H., Extramural |
GeographicLocations | Europe Africa United States--US Arizona |
GeographicLocations_xml | – name: Africa – name: Europe – name: United States--US – name: Arizona |
GrantInformation_xml | – fundername: NIGMS NIH HHS grantid: K12 GM000708 |
GroupedDBID | --- 123 29O 2WC 3V. 53G 5VS 7RV 7X2 7X7 7XC 88E 8AO 8C1 8CJ 8FE 8FG 8FH 8FI 8FJ A8Z AAFWJ ABDBF ABIVO ABJCF ABPTK ABUWG ACGFO ACIHN ACIWK ACPRK ADBBV ADRAZ AEAQA AENEX AFKRA AFPKN AFRAH AHMBA ALMA_UNASSIGNED_HOLDINGS AOIJS APEBS ARAPS ATCPS BAWUL BBNVY BBORY BCNDV BENPR BGLVJ BHPHI BKEYQ BPHCQ BVXVI BWKFM CCPQU CS3 D1I D1J D1K DIK DU5 E3Z EAP EAS EBD EMOBN ESTFP ESX EX3 F5P FBQ FPL FYUFA GROUPED_DOAJ GX1 HCIFZ HH5 HMCUK HYE IAO IEA IHR IHW INH INR IOV IPNFZ IPY ISE ISR ITC K6- KB. KQ8 L6V LK5 LK8 M0K M1P M48 M7P M7R M7S M~E NAPCQ O5R O5S OK1 P2P P62 PATMY PDBOC PIMPY PQQKQ PROAC PSQYO PTHSS PV9 PYCSY RIG RNS RPM RZL SV3 TR2 UKHRP WOQ WOW ~02 ~KM ALIPV CGR CUY CVF ECM EIF NPM AAYXX CITATION 7QG 7QL 7QO 7SN 7SS 7T5 7TG 7TM 7U9 7XB 8FD 8FK AZQEC C1K DWQXO FR3 GNUQQ H94 K9. KL. M7N P64 PQEST PQUKI PRINS RC3 7X8 5PM AAPBV N95 |
ID | FETCH-LOGICAL-c782t-a2869ffc2e79c9072e28305eb5ae17c0d3b29e54255fcb4f9e229a4aef349f833 |
IEDL.DBID | RPM |
ISSN | 1932-6203 |
IngestDate | Sun Jun 04 06:37:10 EDT 2023 Tue Oct 22 14:58:10 EDT 2024 Tue Sep 17 21:14:45 EDT 2024 Fri Oct 25 02:02:41 EDT 2024 Thu Oct 10 14:32:18 EDT 2024 Fri Feb 23 00:05:39 EST 2024 Fri Feb 02 04:06:16 EST 2024 Thu Aug 01 19:13:18 EDT 2024 Thu Aug 01 20:37:02 EDT 2024 Tue Aug 20 22:09:26 EDT 2024 Fri Aug 23 00:30:20 EDT 2024 Sat Nov 02 12:21:47 EDT 2024 Wed Dec 27 19:15:07 EST 2023 |
IsDoiOpenAccess | true |
IsOpenAccess | true |
IsPeerReviewed | true |
IsScholarly | true |
Issue | 8 |
Language | English |
License | This is an open-access article distributed under the terms of the Creative Commons Public Domain declaration, which stipulates that, once placed in the public domain, this work may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. Creative Commons CC0 public domain |
LinkModel | DirectLink |
MergedId | FETCHMERGED-LOGICAL-c782t-a2869ffc2e79c9072e28305eb5ae17c0d3b29e54255fcb4f9e229a4aef349f833 |
Notes | http://dx.doi.org/10.1371/journal.pone.0072106 ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Competing Interests: The authors have declared that no competing interests exist. Conceived and designed the experiments: SV KEA. Performed the experiments: SV. Analyzed the data: SV SMR KEA. Contributed reagents/materials/analysis tools: SV SMR KEA. Wrote the paper: SV SMR KEA. |
OpenAccessLink | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3749107/ |
PMID | 23991051 |
PQID | 1430787236 |
PQPubID | 1436336 |
PageCount | e72106 |
ParticipantIDs | plos_journals_1430787236 doaj_primary_oai_doaj_org_article_5a05978afdbc4a90b935bbd42e7ab716 pubmedcentral_primary_oai_pubmedcentral_nih_gov_3749107 proquest_miscellaneous_1429215219 proquest_journals_1430787236 gale_infotracmisc_A478186006 gale_infotracacademiconefile_A478186006 gale_incontextgauss_ISR_A478186006 gale_incontextgauss_IOV_A478186006 gale_healthsolutions_A478186006 crossref_primary_10_1371_journal_pone_0072106 pubmed_primary_23991051 fao_agris_US201600008665 |
PublicationCentury | 2000 |
PublicationDate | 2013-08-21 |
PublicationDateYYYYMMDD | 2013-08-21 |
PublicationDate_xml | – month: 08 year: 2013 text: 2013-08-21 day: 21 |
PublicationDecade | 2010 |
PublicationPlace | United States |
PublicationPlace_xml | – name: United States – name: San Francisco – name: San Francisco, USA |
PublicationTitle | PloS one |
PublicationTitleAlternate | PLoS One |
PublicationYear | 2013 |
Publisher | Public Library of Science Public Library of Science (PLoS) |
Publisher_xml | – name: Public Library of Science – name: Public Library of Science (PLoS) |
References | ref56 E Crotti (ref64) 2009; 11 JG Lundgren (ref2) 2010; 5(5) MC García (ref47) 2010; 2 RJ Dillon (ref63) 2004; 49 G Storelli (ref9) 2011; 14 MF Ramadan (ref44) 2012; 4 JD Thompson (ref37) 1994; 22 MM Aween (ref55) 2012; 9 H Koch (ref59) 2011; 62 KI Mohr (ref17) 2006; 8 M Gilliam (ref22) 1979; 10 TC Olofsson (ref58) 2008; 57 E Forsgren (ref11) 2010; 41 VG Martinson (ref14) 2012; 78 T Rodriguez-Navarro (ref50) 1973; 76 J Pain (ref10) 1966; 9 R Fontana (ref27) 2004; 25 A Endo (ref54) 2011; 62 M Gilliam (ref18) 1971; 4 TR Shamala (ref52) 2000; 30 M Gilliam (ref21) 1997; 155 ref42 NA Moran (ref1) 2007; 104 B Chouaia (ref7) 2012; 12 P Engel (ref39) 2012; 109 S Rauch (ref33) 2009; 75 JW McCreadie (ref5) 2005; 108 VG Martinson (ref15) 2011; 20 M Gilliam (ref23) 1979; 10 S Vojvodic (ref32) 2010; 149 T Disayathanoowat (ref60) 2012; 79 Q McFrederick (ref12) 2012; 21 ref34 CI Pavel (ref48) 2011; 44 ref31 ref30 SC Shin (ref8) 2011; 334 JR Liu (ref46) 2008; 56 ref38 A Jeyaprakash (ref61) 2003; 84 A Romanelli (ref45) 2011; 17 D Babendreier (ref57) 2007; 59 M Gilliam (ref19) 1987; 49 J-H Ryu (ref6) 2008; 319 DP Neveling (ref40) 2012; 65 J Simpson (ref65) 1955; 96 A Koeppel (ref43) 2008; 105 TA Hall (ref35) 1999; 41 K Bilikova (ref26) 2002; 528 T Rodriguez-Navarro (ref51) 1975; 30 JD Evans (ref20) 2006; 6 ref24 ref25 LR Batra (ref66) 1973; 49 A Vásquez (ref41) 2009; 40 JA Russell (ref3) 2009; 106 ref28 ref29 A Endo (ref53) 2009; 32 NA Moran (ref13) 2012; 4 M Katoh (ref36) 2002; 30 ref62 DL Cox-Foster (ref16) 2007; 318 KE Anderson (ref49) 2011; 58 EM Janson (ref4) 2008; 62 |
References_xml | – volume: 4 start-page: 315 year: 1971 ident: ref18 article-title: Microbial sterility of the intestinal content of the immature honey bee Apis mellifera publication-title: Ann Entomol Sac Am doi: 10.1093/aesa/64.1.315 contributor: fullname: M Gilliam – volume: 17 start-page: 348 year: 2011 ident: ref45 article-title: Peptides from royal jelly: studies on the antimicrobial activity of jelleins, jelleins analogs and synergy with temporins publication-title: J Pept Sci doi: 10.1002/psc.1316 contributor: fullname: A Romanelli – volume: 106 start-page: 21236 year: 2009 ident: ref3 article-title: Bacterial gut symbionts are tightly linked with the evolution of herbivory in ants publication-title: Proc Natl Acad Sci USA doi: 10.1073/pnas.0907926106 contributor: fullname: JA Russell – volume: 10 start-page: 269 year: 1979 ident: ref23 article-title: Microbiology of pollen and bee bread: the genus Bacillus publication-title: Apidologie doi: 10.1051/apido:19790304 contributor: fullname: M Gilliam – ident: ref30 doi: 10.4159/9780674043404 – volume: 75 start-page: 3344 year: 2009 ident: ref33 article-title: Negative correlation between individual-insect-level virulence and colony-level virulence of Paenibacillus larvae, the etiological agent of American foulbrood of honeybees publication-title: Appl Environ Microbiol doi: 10.1128/AEM.02839-08 contributor: fullname: S Rauch – volume: 96 start-page: 117 year: 1955 ident: ref65 article-title: The significance of the presence of pollen in the food of worker larvae of the honey-bee publication-title: QJ Microsc Sci contributor: fullname: J Simpson – ident: ref24 – volume: 319 start-page: 777 year: 2008 ident: ref6 article-title: Innate immune homeostasis by the homeobox gene Caudal and commensal-gut mutualism in Drosophila. publication-title: Science doi: 10.1126/science.1149357 contributor: fullname: J-H Ryu – volume: 11 start-page: 3252 year: 2009 ident: ref64 article-title: Asaia, a versatile acetic acid bacterial symbiont, capable of cross-colonizing insects of phylogenetically distant genera and orders. Environ publication-title: Microbiol contributor: fullname: E Crotti – volume: 62 start-page: 997 year: 2008 ident: ref4 article-title: Phytophagous insectmicrobe mutualisms and adaptive evolutionary diversification publication-title: Evolution doi: 10.1111/j.1558-5646.2008.00348.x contributor: fullname: EM Janson – volume: 20 start-page: 619 year: 2011 ident: ref15 article-title: A simple and distinctive microbiota associated with honey bees and bumble bees publication-title: Mol Ecol doi: 10.1111/j.1365-294X.2010.04959.x contributor: fullname: VG Martinson – volume: 528 start-page: 125 year: 2002 ident: ref26 article-title: Apisimin, a new serine-valine-rich peptide from honeybee (Apis mellifera L.) royal jelly: purification and molecular characterization publication-title: FEBS Lett doi: 10.1016/S0014-5793(02)03272-6 contributor: fullname: K Bilikova – volume: 105 start-page: 2504 year: 2008 ident: ref43 article-title: Identifying the fundamental units of bacterial diversity: a paradigm shift to incorporate ecology into bacterial systematics publication-title: Proc Natl Acad Sci USA doi: 10.1073/pnas.0712205105 contributor: fullname: A Koeppel – ident: ref62 doi: 10.1371/journal.pone.0041250 – volume: 78 start-page: 2830 year: 2012 ident: ref14 article-title: Establishment of characteristic gut bacteria during development of the honey bee worker publication-title: Appl Environ Microbiol doi: 10.1128/AEM.07810-11 contributor: fullname: VG Martinson – volume: 22 start-page: 4673 year: 1994 ident: ref37 article-title: CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice publication-title: Nucleic Acids Res doi: 10.1093/nar/22.22.4673 contributor: fullname: JD Thompson – ident: ref34 – volume: 9 start-page: 209 year: 1966 ident: ref10 article-title: Recherches biochimiques et physiologiques sur le pollen emmagasine par les abeilles publication-title: Ann Abeille doi: 10.1051/apido:19660302 contributor: fullname: J Pain – volume: 14 start-page: 403 year: 2011 ident: ref9 article-title: Lactobacillus plantarum Promotes Drosophila Systemic Growth by Modulating Hormonal Signals through TOR-Dependent Nutrient Sensing publication-title: Cell Metabolism doi: 10.1016/j.cmet.2011.07.012 contributor: fullname: G Storelli – volume: 4 start-page: e36393 year: 2012 ident: ref13 article-title: Distinctive gut microbiota of honey bees assessed using deep sampling from Individual worker bees publication-title: PLoS ONE 7 doi: 10.1371/journal.pone.0036393 contributor: fullname: NA Moran – volume: 6 start-page: 4 year: 2006 ident: ref20 article-title: Antagonistic interactions between honey bee bacterial symbionts and implications for disease publication-title: BMC Ecol doi: 10.1186/1472-6785-6-4 contributor: fullname: JD Evans – volume: 8 start-page: 258 year: 2006 ident: ref17 article-title: Diversity and phylotype consistency of bacteria in the guts of three bee species (Apoidea) at an oilseed rape field publication-title: Environ Microbiol doi: 10.1111/j.1462-2920.2005.00893.x contributor: fullname: KI Mohr – volume: 4 start-page: 39 year: 2012 ident: ref44 article-title: Bioactive compounds and health-promoting properties of royal jelly: A review publication-title: J Funct Food doi: 10.1016/j.jff.2011.12.007 contributor: fullname: MF Ramadan – volume: 5(5) start-page: e10831 year: 2010 ident: ref2 article-title: Bacterial gut symbionts contribute to seed digestion in an omnivorous beetle publication-title: PLoS ONE doi: 10.1371/journal.pone.0010831 contributor: fullname: JG Lundgren – volume: 10 start-page: 43 year: 1979 ident: ref22 article-title: Microbiology of pollen and bee bread: the yeasts publication-title: Apidologie doi: 10.1051/apido:19790106 contributor: fullname: M Gilliam – volume: 155 start-page: 1 year: 1997 ident: ref21 article-title: Identification and roles of non-pathogenic microflora associated with honey bees publication-title: FEMS Microbiol Lett doi: 10.1016/S0378-1097(97)00337-6 contributor: fullname: M Gilliam – volume: 41 start-page: 95 year: 1999 ident: ref35 article-title: Bioedit: a user friendly biological sequence alignment editor and alignment program for Windows 95/98 NT publication-title: Nucleic Acid Symposium Series contributor: fullname: TA Hall – volume: 30 start-page: 3059 year: 2002 ident: ref36 article-title: MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform publication-title: Nucleic Acids Res doi: 10.1093/nar/gkf436 contributor: fullname: M Katoh – volume: 56 start-page: 11447 year: 2008 ident: ref46 article-title: Antioxidant properties of royal jelly associated with larval age and time of harvest publication-title: J Agricul Food Chem doi: 10.1021/jf802494e contributor: fullname: JR Liu – volume: 62 start-page: 500 year: 2011 ident: ref54 article-title: Characterization and emended description of Lactobacillus kunkeei as a fructophilic lactic acid bacterium publication-title: Int J Syst Evol Microbiol doi: 10.1099/ijs.0.031054-0 contributor: fullname: A Endo – volume: 40 start-page: 26 year: 2009 ident: ref41 article-title: Scientific note on the lactic acid bacterial flora in honeybees in the USA – A comparison with bees from Sweden publication-title: Apidologie doi: 10.1051/apido:2008063 contributor: fullname: A Vásquez – volume: 49 start-page: 71 year: 2004 ident: ref63 article-title: The gut bacteria of insects: nonpathogenic interactions publication-title: Annu Rev Entomol doi: 10.1146/annurev.ento.49.061802.123416 contributor: fullname: RJ Dillon – volume: 108 start-page: 362 year: 2005 ident: ref5 article-title: Context dependent symbiosis between black flies (Diptera: Simuliidae) and trichomycete fungi (Harpellales: Legeriomycetaceae) publication-title: Oikos doi: 10.1111/j.0030-1299.2005.13417.x contributor: fullname: JW McCreadie – volume: 2 start-page: 93 year: 2010 ident: ref47 article-title: Antibacterial activity of Royal Jelly against bacteria capable of infecting cutaneous wounds publication-title: Journal of ApiProduct and ApiMedical Science doi: 10.3896/IBRA.4.02.3.02 contributor: fullname: MC García – volume: 30 start-page: 453 year: 2000 ident: ref52 article-title: Stimulatory effect of honey on multiplication of lactic acid bacteria under in vitro and in vivo conditions publication-title: Lett Appl Microbiol doi: 10.1046/j.1472-765x.2000.00746.x contributor: fullname: TR Shamala – volume: 57 start-page: 356 year: 2008 ident: ref58 article-title: Detection and identification of a novel lactic acid bacterial flora within the honey stomach of the honeybee Apis mellifera publication-title: Curr Microbiol doi: 10.1007/s00284-008-9202-0 contributor: fullname: TC Olofsson – volume: 104 start-page: 8627 year: 2007 ident: ref1 article-title: Symbiosis as an adaptive process and source of phenotypic complexity publication-title: Proc Natl Acad Sci USA doi: 10.1073/pnas.0611659104 contributor: fullname: NA Moran – volume: 12 start-page: S2 year: 2012 ident: ref7 article-title: Delayed larval development in Anopheles mosquitoes deprived of Asaia bacterial symbionts publication-title: BMC Microbiol doi: 10.1186/1471-2180-12-S1-S2 contributor: fullname: B Chouaia – volume: 149 start-page: 200 year: 2010 ident: ref32 article-title: Opposing temperature-dependent mortality after infection with an obligate and facultative fungal pathogen of honeybees publication-title: Vet Microbiol doi: 10.1016/j.vetmic.2010.10.001 contributor: fullname: S Vojvodic – ident: ref29 – volume: 334 start-page: 670 year: 2011 ident: ref8 article-title: Drosophila microbiome modulates host developmental and metabolic homeostasis via insulin signaling publication-title: Science doi: 10.1126/science.1212782 contributor: fullname: SC Shin – volume: 79 start-page: 273 year: 2012 ident: ref60 article-title: T-RFLP analysis of bacterial communities in the midguts of Apis mellifera and Apis cerana honey bees in Thailand publication-title: FEMS Microbiol Ecol doi: 10.1111/j.1574-6941.2011.01216.x contributor: fullname: T Disayathanoowat – volume: 30 start-page: 893 year: 1975 ident: ref51 article-title: Microbiology of ripening honey publication-title: Appl Microbiol doi: 10.1128/AEM.30.6.893-896.1975 contributor: fullname: T Rodriguez-Navarro – ident: ref25 – volume: 44 start-page: 108 year: 2011 ident: ref48 article-title: Biological Activities of Royal Jelly – Review. Animal Science and Biotechnologies contributor: fullname: CI Pavel – volume: 59 start-page: 600 year: 2007 ident: ref57 article-title: Bacterial community structures in honeybee intestines and their response to two insecticidal proteins publication-title: FEMS Microbiol Ecol doi: 10.1111/j.1574-6941.2006.00249.x contributor: fullname: D Babendreier – volume: 49 start-page: 70 year: 1987 ident: ref19 article-title: Microbiology of feces of the larval honey bee, Apis mellifera publication-title: J Invertebr Pathol doi: 10.1016/0022-2011(87)90127-3 contributor: fullname: M Gilliam – volume: 109 start-page: 11002 year: 2012 ident: ref39 article-title: Functional diversity within the simple gut microbiota of the honey bee publication-title: Proc Natl Acad Sci USA doi: 10.1073/pnas.1202970109 contributor: fullname: P Engel – ident: ref38 – volume: 84 start-page: 96 year: 2003 ident: ref61 article-title: Bacterial diversity in worker adults of Apis mellifera capensis and Apis mellifera scutellata (Insecta: Hymenoptera) assessed using 16S rRNA sequences publication-title: J Invertebr Pathol doi: 10.1016/j.jip.2003.08.007 contributor: fullname: A Jeyaprakash – volume: 62 start-page: 121 year: 2011 ident: ref59 article-title: Bacterial communities in central European bumblebees: low diversity and high specificity publication-title: Microb Ecol doi: 10.1007/s00248-011-9854-3 contributor: fullname: H Koch – volume: 21 start-page: 1754 year: 2012 ident: ref12 article-title: Environment or kin: whence do bees obtain acidophilic bacteria? publication-title: Mol Ecol doi: 10.1111/j.1365-294X.2012.05496.x contributor: fullname: Q McFrederick – ident: ref28 – ident: ref42 – volume: 32 start-page: 593 year: 2009 ident: ref53 article-title: Isolation and characterization of fructophilic lactic acid bacteria from fructose-rich niches publication-title: Syst Appl Microbiol doi: 10.1016/j.syapm.2009.08.002 contributor: fullname: A Endo – volume: 41 start-page: 99 year: 2010 ident: ref11 article-title: Novel lactic acid bacteria inhibiting Paenibacillus larvae in honey bee larvae publication-title: Apidologie doi: 10.1051/apido/2009065 contributor: fullname: E Forsgren – volume: 58 start-page: 431 year: 2011 ident: ref49 article-title: An emerging paradigm of colony health: microbial balance of the honey bee and hive (Apis mellifera) publication-title: Insectes Sociaux doi: 10.1007/s00040-011-0194-6 contributor: fullname: KE Anderson – volume: 9 start-page: 807 year: 2012 ident: ref55 article-title: Evaluating on antibacterial activity of Lactobacillus acidophilus strains isolated from honey publication-title: Am J Applied Sci doi: 10.3844/ajassp.2012.807.817 contributor: fullname: MM Aween – ident: ref56 doi: 10.1371/journal.pone.0033188 – volume: 49 start-page: 13 year: 1973 ident: ref66 article-title: The mycoflora of domesticated and wild bees (Apoidea) publication-title: Mycopathologia contributor: fullname: LR Batra – volume: 25 start-page: 919 year: 2004 ident: ref27 article-title: Jelleines: a family of antimicrobial peptides from the royal jelly of honeybees (Apis mellifera). publication-title: Peptides doi: 10.1016/j.peptides.2004.03.016 contributor: fullname: R Fontana – volume: 76 start-page: 211 year: 1973 ident: ref50 article-title: Gluconic acid producing bacteria from honey bee and ripening honey publication-title: J Gen Microbiol doi: 10.1099/00221287-76-1-211 contributor: fullname: T Rodriguez-Navarro – volume: 318 start-page: 283 year: 2007 ident: ref16 article-title: A metagenomic survey of microbes in honey bee colony collapse disorder publication-title: Science doi: 10.1126/science.1146498 contributor: fullname: DL Cox-Foster – volume: 65 start-page: 507 year: 2012 ident: ref40 article-title: Fructophilic Lactobacillus kunkeei and Lactobacillus brevis isolated from fresh flowers, bees and bee-hives publication-title: Curr Microbiol doi: 10.1007/s00284-012-0186-4 contributor: fullname: DP Neveling – ident: ref31 |
SSID | ssj0053866 |
Score | 2.5240877 |
Snippet | The first step in understanding gut microbial ecology is determining the presence and potential niche breadth of associated microbes. While the core gut... |
SourceID | plos doaj pubmedcentral proquest gale crossref pubmed fao |
SourceType | Open Website Open Access Repository Aggregation Database Index Database Publisher |
StartPage | e72106 |
SubjectTerms | Acetobacteraceae Acetobacteraceae - genetics Acetobacteraceae - physiology Acids Adults Africa Animals Apis mellifera Bacteria Bacteria - classification Bacteria - genetics Bacteria - isolation & purification bacterial communities Bees Bees - microbiology Biodiversity Biology digestive system disease course Disease resistance DNA Barcoding, Taxonomic DNA, Bacterial - chemistry DNA, Bacterial - genetics Ecology Europe European honeybee Evolutionary biology Firmicutes Flora Food Fungi Gastrointestinal Tract - microbiology Genetic Variation Honey honey bees Inoculation insect larvae Insects Instars Intestinal microflora intestinal microorganisms Lactobacillus Lactobacillus - genetics Lactobacillus - physiology Larva - microbiology Larvae Microbiota Microbiota (Symbiotic organisms) Microorganisms Molecular Sequence Data Neisseriaceae Neisseriaceae - genetics Neisseriaceae - physiology Niche breadth Nutrition Physiology Pollinators RNA, Ribosomal, 16S - genetics Royal jelly Sequence Analysis, DNA Studies Symbiosis |
SummonAdditionalLinks | – databaseName: Directory of Open Access Journals dbid: DOA link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwrV1Lb9NAEF6hnLggyiumBRaEBBxM7fVjvceCqAqiIFGCelvtM40U2VGdHODXM7N-KEaV4MA1O0608x5n5htCXnKVgVSViHNrdJyDOcVVlZpYKVcqIwzjFgeFz7-UZ4v802VxubfqC3vCOnjgjnHHhYIEgFfKW21yJRItskJrmzPHlYZkP3jfRAzFVOeDwYrLsh-Uy3h63Mvl7aapXQDLTnHD0V4gCnj9EF68akbfPNusm_amxPPP_sm9gHR6l9zpM0l60t3ggNxy9T1y0NtqS1_3gNJv7pPP56sAtwTUy92W2qEVgzaednuC6tUvZ6mqLR3eztMruMRPqp2ja1wftKYrTCSv2wdkcfrh-_uzuN-iEBuI_ttYsaoU3htgmDBQCjOHmF-F04VyKTeJzTQTrgDbLbzRuReOMaFy5XyWC19l2UMyq-En54Ri8Cp1mjiR2dxqpotEGeyS5QWHVE5HJB5YKjcdWIYM_5hxKDI6rkgUgexFEJF3yPeRFqGuwwegALJXAPk3BYjIHKQm1RKcolxcMITMC5VaWUTkGYpSdiOloy3LE5yvrYAMHn4RKBAJo8ZWm6Xata38-PXHPxBdfJsQveqJfANKYVQ_3gDXRYStCeXRhBLs2UyO56h4A8NaKM7AD1ecZfjkoIw3Hz8fj_FLsX2uds0OaZjABcapiMijTndHpuNwMyTZaUT4RKsnUpme1KurAESecTDuhD_-H2I8JLdZ2DQCjjs9IrPt9c49gXxvq58G0_4N9exRIQ priority: 102 providerName: Directory of Open Access Journals – databaseName: ProQuest Technology Collection dbid: 8FG link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwjV3db9MwELegCIkXxMZHAwMMQgIesiXOh-MntMG6gjaQGEV7s2zHKZWmpCztw_jruXOcsqAJ8Vpf2tr37dz9jpBXXCXAVSXCtDQ6TEGdwqKITaiUzZURhvESG4VPPufTWfrpLDvzF26tL6vsbaIz1GVj8I58D_w6eDPOkvzd8meIU6Pw7aofoXGT3IoZ55h8FZOj3hKDLue5b5dLeLznubO7bGrrILNjnHN0xR051H5wMpVqNhZ6tDxv2uvCz7-rKK-4pck9ctfHk3S_E4AtcsPW2-T2ocOivtwmW153W_rGA0y_vU-OTxYOfgmeO1qv6Ie-NIM2Fe3mBtWLX7akqi5pf1tPp7CdS3pgLT3GcULnFMsMICt-QGaTw2_vp6GfqhAaiAZWoWJFLqrKMMuFgdSYWcQAy6zOlI25icpEM2Ez0OWsMjqthGVMqFTZKklFVSTJQzKq4SfHhKIzy3UcWZGUaamZziJlsGqWZxxCOx2QsD9cuezAM6R7g8Yh6ejORyIzpGdGQA6QAxtahL52HzQXc-k1SWYKIkJeqKrUJlUi0iLJtC5T2I_SkP0FZAz8k2oORlLOThlC6LnMLc8C8hyZKrsW041uy33sty2ADB5-6SgQGaPG0pu5Wret_Pjl-38QnX4dEL32RFUD4mGUb3eA7SLi1oByZ0AJ-m0Gy2MUwf7AWvlHE-DJXiyvX36xWcYvxXK62jZrpGECBxrHIiCPOineHDo2O0PQHQeED-R7wJXhSr344YDJEw7KHvHH__5bT8gd5maKgImOd8hodbG2TyGyW-lnTn1_A4RTSfo priority: 102 providerName: ProQuest – databaseName: Scholars Portal Open Access Journals dbid: M48 link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwjV1Lb9QwELaq5cIFUV6bUsAgJOCQKnGcOD4g1AJlQS1IlEW9WbbjLCutkmUfEuXXM-M8RNAi9RqPE3ke9kw88w0hz4VOQKpahrywJuRgTmGexzbU2mXaSstEgYXC55-zyZR_ukwv90jXs7Vl4HpnaIf9pKarxdGvn1dvwOBf-64NIu4mHS3rynko7BgxuG8wDrE6JvPx_l4BrNvfXqLXEmYsStpiuv-9ZXBYeUx_OIJKXff792i5qNe7nNN_cyz_OrROb5NbrbdJjxv12Cd7rrpD9lt7XtOXLej0q7vk7HzuIZmA-sN2Q9916Rq0LmnTS6ia_3YF1VVBuz_4dAKLuKInztEzbDG0oJh6AOy8R6an77-9nYRtp4XQgoewCTXLM1mWljkhLYTLzCEuWOpMql0sbFQkhkmXgn2npTW8lI4xqbl2ZcJlmSfJfTKq4JNjQvGAy0wcOZkUvDDMpJG2mEkrUgHunglI2LFULRtADeVv1QQEIg1XFIpAtSIIyAnyvadFOGz_oF7NVGtdKtXgJYpcl4WxXMvIyCQ1puCwHm0gIgzIGKSm9Aw2TjW9YAir56O5LA3IExSlaspOe3tXx1iDmwMZTH7mKRAto8J0nJnertfq45fv1yC6-DogetESlTUohdVtCQQsF1G4BpSHA0qweTsYHqPidQxbQwAHe3UuWIIzO2XcPfy0H8aXYopd5eot0jCJTY5jGZAHje72TMcCaHDE44CIgVYPpDIcqeY_PFh5ImADiMTBdfjzkNxkvtsIbN7xIRltVlv3CHy-jXnszfgPHhRQtQ priority: 102 providerName: Scholars Portal |
Title | Microbial Gut Diversity of Africanized and European Honey Bee Larval Instars |
URI | https://www.ncbi.nlm.nih.gov/pubmed/23991051 https://www.proquest.com/docview/1430787236 https://search.proquest.com/docview/1429215219 https://pubmed.ncbi.nlm.nih.gov/PMC3749107 https://doaj.org/article/5a05978afdbc4a90b935bbd42e7ab716 http://dx.doi.org/10.1371/journal.pone.0072106 |
Volume | 8 |
hasFullText | 1 |
inHoldings | 1 |
isFullTextHit | |
isPrint | |
link | http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV3db9MwELe2IiReEBsfDWzFICTgIW3jfDh-XMu6gtYxbRT1LbIdp1TqkmptH8ZfvzsnqQjaA-LFD_U5rX0fvkvvfkfIBy594KoUbpBq5QagTm4ce9qV0kRSC814ioXCk4toPA2-zcLZHgnrWhibtK_Vopsvb7r54pfNrVzd6F6dJ9a7nAx9Dg_t894-2QcBrUP00vyCAkdRVSPnc69XsaS7KnJjcbIhBkIEYLiYwbXwGteRRe2HSyaTxc5Ct1bLYv2Q-_l3FuUf19LoGXla-ZP0pPzdB2TP5Ifkcdlh8u6QHFS6u6afKoDpz8_J-WRh4Zdg3dl2Q7_UqRm0yGjZNyhf_DYplXlK67f1dAw7u6MDY-g5thNaUkwzgKj4BZmOTn8Mx27VVcHV4A1sXMniSGSZZoYLDaExM4gBFhoVSuNx3U99xYQJQZfDTKsgE4YxIQNpMj8QWez7L0krh69sE4qXWaS8vhF-GqSKqbAvNWbN8pCDa6cc4taHm6xK8IzE_oPGIegozydBviQVXxwyQA7saBH62n5Q3M6TSgCSUIJHyGOZpUoHUvSV8EOl0gD2IxVEfw5pA_8SOQcjmUyvGULo2cgtCh3yFpmalCWmO91OTrDeNgYyWPzeUiAyRo6pN3O5Xa-Tr99__gPR9VWD6GNFlBUgHlpW5Q6wXUTcalAeNShBv3Vjuo0iWB_YGoI1sMsxZz6urMXy4el3u2l8KKbT5abYIg0T2NDYEw55VUrx7tBrzXAIb8h3gyvNGdBTC0xe6eXr_175hjxhtt0IWG_viLQ2t1tzDE7fRnVA1Wccxnjo4Tg665BHg9OLy6uOfY0C4ySIO9YU3AOfB1ju |
link.rule.ids | 230,315,730,783,787,867,888,2109,2228,12068,12235,12777,21400,24330,27936,27937,31731,31732,33278,33279,33385,33386,33756,33757,43322,43591,43612,43817,53804,53806,74079,74348,74369,74636 |
linkProvider | National Library of Medicine |
linkToHtml | http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwjV3db9MwELegCMELYuOjgcEMQgIewhrnw_ET2mBdB92Q2DrtzbIdp1SakrK2D-Ov585xyoImxGt9Tmrfp5273xHyhqsYuKpEmBRGhwmoU5jnkQmVspkywjBeYKHw0XE2miRfztNzf-G28GmVrU10hrqoDd6R74BfB2_GWZx9nP8MsWsUfl31LTRukztJDL4aK8WHB60lBl3OMl8uF_Nox3Pnw7yurIPMjrDP0TV35FD7wcmUql5b6N78ol7cFH7-nUV5zS0NH5IHPp6ku40AbJBbttokd_cdFvXVJtnwurug7zzA9PtHZHw0c_BLMO9gtaSf29QMWpe06RtUzX7ZgqqqoO1tPR3Bcq7onrV0jO2ELiimGcCp-DGZDPdPP41C31UhNBANLEPF8kyUpWGWCwNHY2YRAyy1OlU24mZQxJoJm4Iup6XRSSksY0IlypZxIso8jp-QXgWv7BOKzizT0cCKuEgKzXQ6UAazZnnKIbTTAQnbzZXzBjxDui9oHA4dzf5IZIb0zAjIHnJgTYvQ1-6H-nIqvSbJVEFEyHNVFtokSgy0iFOtiwTWozSc_gLSB_5JNQUjKScnDCH03MktSwOyjUyVTYnpWrflLtbb5kAGk187CkTGqDD1ZqpWi4U8_Hb2H0Qn3ztEbz1RWYN4GOXLHWC5iLjVodzqUIJ-m85wH0Ww3bCF_KMJMLMVy5uHX62H8aGYTlfZeoU0TGBD40gE5GkjxetNx2JnCLqjgPCOfHe40h2pZj8cMHnMQdkH_Nm__9Y2uTc6PRrL8eHx1-fkPnP9RcBcR1ukt7xc2RcQ5S31S6fKvwH_iUzc |
linkToPdf | http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwjV3db9MwELegCMQLYuOjgcEMQgIeQhvnw_ET2icddAMxivZm2Y5TKk1JWdqH8ddzlzhhQRPitT63te9-vnNy9ztCXnEVglaV8KPMaD8COPlpGhhfKZsoIwzjGRYKH58kk1n08Sw-c_lPlUurbM_E-qDOSoPPyEfg18GbcRYmo9ylRXzZP3y__OljByl80-raadwkt8ArRpjele516R6A6yRxpXMhD0ZOU--WZWFr-uwAex5dcU01gz84nFyV3Wk9WJ6X1XWh6N8ZlVdc1OF9cs_FlnSnMYYNcsMWm-T2Qc1LfblJNhyOK_rGkU2_fUCmx4uaignmfViv6H6bpkHLnDY9hIrFL5tRVWS0fXJPJ7CcS7prLZ1ia6FziikHcEN-SGaHB9_2Jr7rsOAbiAxWvmJpIvLcMMuFgWsys8gHFlsdKxtwM85CzYSNAddxbnSUC8uYUJGyeRiJPA3DR2RQwE8OCUXHluhgbEWYRZlmOh4rgxm0POYQ5mmP-O3mymVDpCHrt2kcLiDN_khUhnTK8MguaqCTRRrs-oPyYi4dqmSsIDrkqcozbSIlxlqEsdZZBOtRGm6CHhmC_qSaw4EpZ6cM6fTqW1wSe2QblSqbctMO53IHa29TEIPJL2sJZMko0N7mal1V8ujz9_8QOv3aE3rthPISzMMoV_oAy0X2rZ7kVk8SsG56w0M0wXbDKvkHFTCzNcvrh190w_ilmFpX2HKNMkxgc-NAeORxY8XdpmPhMwTggUd4z757WumPFIsfNUl5yAH4Y_7k339rm9wBFMvp0cmnp-Quq1uNwMkdbJHB6mJtn0HAt9LPayT_BrdQUOU |
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=Microbial+Gut+Diversity+of+Africanized+and+European+Honey+Bee+Larval+Instars&rft.jtitle=PloS+one&rft.au=Vojvodic%2C+Svjetlana&rft.au=Rehan%2C+Sandra+M&rft.au=Anderson%2C+Kirk+E&rft.date=2013-08-21&rft.pub=Public+Library+of+Science&rft.issn=1932-6203&rft.eissn=1932-6203&rft.volume=8&rft.issue=8&rft.spage=e72106&rft_id=info:doi/10.1371%2Fjournal.pone.0072106&rft.externalDBID=ISR&rft.externalDocID=A478186006 |
thumbnail_l | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1932-6203&client=summon |
thumbnail_m | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1932-6203&client=summon |
thumbnail_s | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1932-6203&client=summon |