Disaggregation as an interaction mechanism among intestinal bacteria

The gut microbiome contains hundreds of interacting species that together influence host health and development. The mechanisms by which intestinal microbes can interact, however, remain poorly mapped and are often modeled as spatially unstructured competitions for chemical resources. Recent imaging...

Full description

Saved in:
Bibliographic Details
Published in:Biophysical journal 2022-09, Vol.121 (18), p.3458-3473
Main Authors: Sundarraman, Deepika, Smith, T. Jarrod, Kast, Jade V.Z., Guillemin, Karen, Parthasarathy, Raghuveer
Format: Article
Language:English
Subjects:
Animals
Bacteria
Gastrointestinal Microbiome
Zebrafish - microbiology
Citations: Items that this one cites
Items that cite this one
Online Access:Get full text
Tags: Add Tag
No Tags, Be the first to tag this record!
cited_by cdi_FETCH-LOGICAL-c451t-b8891b3d4bfdda195b06c736917f1f5caa9593265e1a673cf2517549a8b8de533
cites cdi_FETCH-LOGICAL-c451t-b8891b3d4bfdda195b06c736917f1f5caa9593265e1a673cf2517549a8b8de533
container_end_page 3473
container_issue 18
container_start_page 3458
container_title Biophysical journal
container_volume 121
creator Sundarraman, Deepika
Smith, T. Jarrod
Kast, Jade V.Z.
Guillemin, Karen
Parthasarathy, Raghuveer
description The gut microbiome contains hundreds of interacting species that together influence host health and development. The mechanisms by which intestinal microbes can interact, however, remain poorly mapped and are often modeled as spatially unstructured competitions for chemical resources. Recent imaging studies examining the zebrafish gut have shown that patterns of aggregation are central to bacterial population dynamics. In this study, we focus on bacterial species of genera Aeromonas and Enterobacter. Two zebrafish gut-derived isolates, Aeromonas ZOR0001 (AE) and Enterobacter ZOR0014 (EN), when mono-associated with the host, are highly aggregated and located primarily in the intestinal midgut. An Aeromonas isolate derived from the commensal strain, Aeromonas-MB4 (AE-MB4), differs from the parental strain in that it is composed mostly of planktonic cells localized to the anterior gut. When challenged by AE-MB4, clusters of EN rapidly fragment into non-motile, slow-growing, dispersed individual cells with overall abundance two orders of magnitude lower than the mono-association value. In the presence of a certain set of additional gut bacterial species, these effects on EN are dampened. In particular, if AE-MB4 invades an already established multi-species community, EN persists in the form of large aggregates. These observations reveal an unanticipated competition mechanism based on manipulation of bacterial spatial organization, namely dissolution of aggregates, and provide evidence that multi-species communities may facilitate stable intestinal co-existence.
doi_str_mv 10.1016/j.bpj.2022.08.010
format article
fullrecord <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_9515126</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><els_id>S0006349522006701</els_id><sourcerecordid>2704873442</sourcerecordid><originalsourceid>FETCH-LOGICAL-c451t-b8891b3d4bfdda195b06c736917f1f5caa9593265e1a673cf2517549a8b8de533</originalsourceid><addsrcrecordid>eNp9kE1v1DAQhi0EokvhB3BBOXJJmLFjxxYSEmr5kipxgbM1cZzUq8RZ7Gyl_nvcbqngwmkkzzPvjB_GXiM0CKje7Zv-sG84cN6AbgDhCduhbHkNoNVTtgMAVYvWyDP2Iuc9AHIJ-JydCWk0Vyh37PIyZJqm5CfawhoryhXFKsTNJ3L3L4t31xRDXipa1jjd9_IWIs1VXxCfAr1kz0aas3_1UM_Zz8-fflx8ra--f_l28fGqdq3Ere61NtiLoe3HYSA0sgflOqEMdiOO0hEZaQRX0iOpTriRS-xka0j3evBSiHP24ZR7OPaLH5yPW6LZHlJYKN3alYL9txPDtZ3WG2skSuSqBLx9CEjrr2P5hl1Cdn6eKfr1mC3voNWdaFteUDyhLq05Jz8-rkGwd_bt3hb79s6-BW2L_TLz5u_7Hif-6C7A-xPgi6Wb4JPNLvjo_BCSd5sd1vCf-N90Y5Z5</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2704873442</pqid></control><display><type>article</type><title>Disaggregation as an interaction mechanism among intestinal bacteria</title><source>BACON - Elsevier - GLOBAL_SCIENCEDIRECT-OPENACCESS</source><source>PubMed Central (Open access)</source><creator>Sundarraman, Deepika ; Smith, T. Jarrod ; Kast, Jade V.Z. ; Guillemin, Karen ; Parthasarathy, Raghuveer</creator><creatorcontrib>Sundarraman, Deepika ; Smith, T. Jarrod ; Kast, Jade V.Z. ; Guillemin, Karen ; Parthasarathy, Raghuveer</creatorcontrib><description>The gut microbiome contains hundreds of interacting species that together influence host health and development. The mechanisms by which intestinal microbes can interact, however, remain poorly mapped and are often modeled as spatially unstructured competitions for chemical resources. Recent imaging studies examining the zebrafish gut have shown that patterns of aggregation are central to bacterial population dynamics. In this study, we focus on bacterial species of genera Aeromonas and Enterobacter. Two zebrafish gut-derived isolates, Aeromonas ZOR0001 (AE) and Enterobacter ZOR0014 (EN), when mono-associated with the host, are highly aggregated and located primarily in the intestinal midgut. An Aeromonas isolate derived from the commensal strain, Aeromonas-MB4 (AE-MB4), differs from the parental strain in that it is composed mostly of planktonic cells localized to the anterior gut. When challenged by AE-MB4, clusters of EN rapidly fragment into non-motile, slow-growing, dispersed individual cells with overall abundance two orders of magnitude lower than the mono-association value. In the presence of a certain set of additional gut bacterial species, these effects on EN are dampened. In particular, if AE-MB4 invades an already established multi-species community, EN persists in the form of large aggregates. These observations reveal an unanticipated competition mechanism based on manipulation of bacterial spatial organization, namely dissolution of aggregates, and provide evidence that multi-species communities may facilitate stable intestinal co-existence.</description><identifier>ISSN: 0006-3495</identifier><identifier>ISSN: 1542-0086</identifier><identifier>EISSN: 1542-0086</identifier><identifier>DOI: 10.1016/j.bpj.2022.08.010</identifier><identifier>PMID: 35982615</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Animals ; Bacteria ; Gastrointestinal Microbiome ; Zebrafish - microbiology</subject><ispartof>Biophysical journal, 2022-09, Vol.121 (18), p.3458-3473</ispartof><rights>2022 Biophysical Society</rights><rights>Copyright © 2022 Biophysical Society. Published by Elsevier Inc. All rights reserved.</rights><rights>2022 Biophysical Society. 2022 Biophysical Society</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c451t-b8891b3d4bfdda195b06c736917f1f5caa9593265e1a673cf2517549a8b8de533</citedby><cites>FETCH-LOGICAL-c451t-b8891b3d4bfdda195b06c736917f1f5caa9593265e1a673cf2517549a8b8de533</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC9515126/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC9515126/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,315,733,786,790,891,27957,27958,53827,53829</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/35982615$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Sundarraman, Deepika</creatorcontrib><creatorcontrib>Smith, T. Jarrod</creatorcontrib><creatorcontrib>Kast, Jade V.Z.</creatorcontrib><creatorcontrib>Guillemin, Karen</creatorcontrib><creatorcontrib>Parthasarathy, Raghuveer</creatorcontrib><title>Disaggregation as an interaction mechanism among intestinal bacteria</title><title>Biophysical journal</title><addtitle>Biophys J</addtitle><description>The gut microbiome contains hundreds of interacting species that together influence host health and development. The mechanisms by which intestinal microbes can interact, however, remain poorly mapped and are often modeled as spatially unstructured competitions for chemical resources. Recent imaging studies examining the zebrafish gut have shown that patterns of aggregation are central to bacterial population dynamics. In this study, we focus on bacterial species of genera Aeromonas and Enterobacter. Two zebrafish gut-derived isolates, Aeromonas ZOR0001 (AE) and Enterobacter ZOR0014 (EN), when mono-associated with the host, are highly aggregated and located primarily in the intestinal midgut. An Aeromonas isolate derived from the commensal strain, Aeromonas-MB4 (AE-MB4), differs from the parental strain in that it is composed mostly of planktonic cells localized to the anterior gut. When challenged by AE-MB4, clusters of EN rapidly fragment into non-motile, slow-growing, dispersed individual cells with overall abundance two orders of magnitude lower than the mono-association value. In the presence of a certain set of additional gut bacterial species, these effects on EN are dampened. In particular, if AE-MB4 invades an already established multi-species community, EN persists in the form of large aggregates. These observations reveal an unanticipated competition mechanism based on manipulation of bacterial spatial organization, namely dissolution of aggregates, and provide evidence that multi-species communities may facilitate stable intestinal co-existence.</description><subject>Animals</subject><subject>Bacteria</subject><subject>Gastrointestinal Microbiome</subject><subject>Zebrafish - microbiology</subject><issn>0006-3495</issn><issn>1542-0086</issn><issn>1542-0086</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><recordid>eNp9kE1v1DAQhi0EokvhB3BBOXJJmLFjxxYSEmr5kipxgbM1cZzUq8RZ7Gyl_nvcbqngwmkkzzPvjB_GXiM0CKje7Zv-sG84cN6AbgDhCduhbHkNoNVTtgMAVYvWyDP2Iuc9AHIJ-JydCWk0Vyh37PIyZJqm5CfawhoryhXFKsTNJ3L3L4t31xRDXipa1jjd9_IWIs1VXxCfAr1kz0aas3_1UM_Zz8-fflx8ra--f_l28fGqdq3Ere61NtiLoe3HYSA0sgflOqEMdiOO0hEZaQRX0iOpTriRS-xka0j3evBSiHP24ZR7OPaLH5yPW6LZHlJYKN3alYL9txPDtZ3WG2skSuSqBLx9CEjrr2P5hl1Cdn6eKfr1mC3voNWdaFteUDyhLq05Jz8-rkGwd_bt3hb79s6-BW2L_TLz5u_7Hif-6C7A-xPgi6Wb4JPNLvjo_BCSd5sd1vCf-N90Y5Z5</recordid><startdate>20220920</startdate><enddate>20220920</enddate><creator>Sundarraman, Deepika</creator><creator>Smith, T. Jarrod</creator><creator>Kast, Jade V.Z.</creator><creator>Guillemin, Karen</creator><creator>Parthasarathy, Raghuveer</creator><general>Elsevier Inc</general><general>The Biophysical Society</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20220920</creationdate><title>Disaggregation as an interaction mechanism among intestinal bacteria</title><author>Sundarraman, Deepika ; Smith, T. Jarrod ; Kast, Jade V.Z. ; Guillemin, Karen ; Parthasarathy, Raghuveer</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c451t-b8891b3d4bfdda195b06c736917f1f5caa9593265e1a673cf2517549a8b8de533</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Animals</topic><topic>Bacteria</topic><topic>Gastrointestinal Microbiome</topic><topic>Zebrafish - microbiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Sundarraman, Deepika</creatorcontrib><creatorcontrib>Smith, T. Jarrod</creatorcontrib><creatorcontrib>Kast, Jade V.Z.</creatorcontrib><creatorcontrib>Guillemin, Karen</creatorcontrib><creatorcontrib>Parthasarathy, Raghuveer</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Biophysical journal</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Sundarraman, Deepika</au><au>Smith, T. Jarrod</au><au>Kast, Jade V.Z.</au><au>Guillemin, Karen</au><au>Parthasarathy, Raghuveer</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Disaggregation as an interaction mechanism among intestinal bacteria</atitle><jtitle>Biophysical journal</jtitle><addtitle>Biophys J</addtitle><date>2022-09-20</date><risdate>2022</risdate><volume>121</volume><issue>18</issue><spage>3458</spage><epage>3473</epage><pages>3458-3473</pages><issn>0006-3495</issn><issn>1542-0086</issn><eissn>1542-0086</eissn><notes>ObjectType-Article-1</notes><notes>SourceType-Scholarly Journals-1</notes><notes>ObjectType-Feature-2</notes><notes>content type line 23</notes><abstract>The gut microbiome contains hundreds of interacting species that together influence host health and development. The mechanisms by which intestinal microbes can interact, however, remain poorly mapped and are often modeled as spatially unstructured competitions for chemical resources. Recent imaging studies examining the zebrafish gut have shown that patterns of aggregation are central to bacterial population dynamics. In this study, we focus on bacterial species of genera Aeromonas and Enterobacter. Two zebrafish gut-derived isolates, Aeromonas ZOR0001 (AE) and Enterobacter ZOR0014 (EN), when mono-associated with the host, are highly aggregated and located primarily in the intestinal midgut. An Aeromonas isolate derived from the commensal strain, Aeromonas-MB4 (AE-MB4), differs from the parental strain in that it is composed mostly of planktonic cells localized to the anterior gut. When challenged by AE-MB4, clusters of EN rapidly fragment into non-motile, slow-growing, dispersed individual cells with overall abundance two orders of magnitude lower than the mono-association value. In the presence of a certain set of additional gut bacterial species, these effects on EN are dampened. In particular, if AE-MB4 invades an already established multi-species community, EN persists in the form of large aggregates. These observations reveal an unanticipated competition mechanism based on manipulation of bacterial spatial organization, namely dissolution of aggregates, and provide evidence that multi-species communities may facilitate stable intestinal co-existence.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>35982615</pmid><doi>10.1016/j.bpj.2022.08.010</doi><tpages>16</tpages><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 0006-3495
ispartof Biophysical journal, 2022-09, Vol.121 (18), p.3458-3473
issn 0006-3495
1542-0086
1542-0086
language eng
recordid cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_9515126
source BACON - Elsevier - GLOBAL_SCIENCEDIRECT-OPENACCESS; PubMed Central (Open access)
subjects Animals
Bacteria
Gastrointestinal Microbiome
Zebrafish - microbiology
title Disaggregation as an interaction mechanism among intestinal bacteria
url http://sfxeu10.hosted.exlibrisgroup.com/loughborough?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-09-23T07%3A28%3A33IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Disaggregation%20as%20an%20interaction%20mechanism%20among%20intestinal%20bacteria&rft.jtitle=Biophysical%20journal&rft.au=Sundarraman,%20Deepika&rft.date=2022-09-20&rft.volume=121&rft.issue=18&rft.spage=3458&rft.epage=3473&rft.pages=3458-3473&rft.issn=0006-3495&rft.eissn=1542-0086&rft_id=info:doi/10.1016/j.bpj.2022.08.010&rft_dat=%3Cproquest_pubme%3E2704873442%3C/proquest_pubme%3E%3Cgrp_id%3Ecdi_FETCH-LOGICAL-c451t-b8891b3d4bfdda195b06c736917f1f5caa9593265e1a673cf2517549a8b8de533%3C/grp_id%3E%3Coa%3E%3C/oa%3E%3Curl%3E%3C/url%3E&rft_id=info:oai/&rft_pqid=2704873442&rft_id=info:pmid/35982615&rfr_iscdi=true