Cargando…

Cooperative microbial interactions drive spatial segregation in porous environments

The role of microbial interactions and the underlying mechanisms that shape complex biofilm communities are poorly understood. Here we employ a microfluidic chip to represent porous subsurface environments and show that cooperative microbial interactions between free-living and biofilm-forming bacte...

Descripción completa

Detalles Bibliográficos
Autores principales: Wu, Yichao, Fu, Chengxia, Peacock, Caroline L., Sørensen, Søren J., Redmile-Gordon, Marc A., Xiao, Ke-Qing, Gao, Chunhui, Liu, Jun, Huang, Qiaoyun, Li, Zixue, Song, Peiyi, Zhu, Yongguan, Zhou, Jizhong, Cai, Peng
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10349867/
https://www.ncbi.nlm.nih.gov/pubmed/37454222
http://dx.doi.org/10.1038/s41467-023-39991-4
_version_ 1785074017944731648
author Wu, Yichao
Fu, Chengxia
Peacock, Caroline L.
Sørensen, Søren J.
Redmile-Gordon, Marc A.
Xiao, Ke-Qing
Gao, Chunhui
Liu, Jun
Huang, Qiaoyun
Li, Zixue
Song, Peiyi
Zhu, Yongguan
Zhou, Jizhong
Cai, Peng
author_facet Wu, Yichao
Fu, Chengxia
Peacock, Caroline L.
Sørensen, Søren J.
Redmile-Gordon, Marc A.
Xiao, Ke-Qing
Gao, Chunhui
Liu, Jun
Huang, Qiaoyun
Li, Zixue
Song, Peiyi
Zhu, Yongguan
Zhou, Jizhong
Cai, Peng
author_sort Wu, Yichao
collection PubMed
description The role of microbial interactions and the underlying mechanisms that shape complex biofilm communities are poorly understood. Here we employ a microfluidic chip to represent porous subsurface environments and show that cooperative microbial interactions between free-living and biofilm-forming bacteria trigger active spatial segregation to promote their respective dominance in segregated microhabitats. During initial colonization, free-living and biofilm-forming microbes are segregated from the mixed planktonic inoculum to occupy the ambient fluid and grain surface. Contrary to spatial exclusion through competition, the active spatial segregation is induced by cooperative interactions which improves the fitness of both biofilm and planktonic populations. We further show that free-living Arthrobacter induces the surface colonization by scavenging the biofilm inhibitor, D-amino acids and receives benefits from the public goods secreted by the biofilm-forming strains. Collectively, our results reveal how cooperative microbial interactions may contribute to microbial coexistence in segregated microhabitats and drive subsurface biofilm community succession.
format Online
Article
Text
id pubmed-10349867
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher Nature Publishing Group UK
record_format MEDLINE/PubMed
spelling pubmed-103498672023-07-17 Cooperative microbial interactions drive spatial segregation in porous environments Wu, Yichao Fu, Chengxia Peacock, Caroline L. Sørensen, Søren J. Redmile-Gordon, Marc A. Xiao, Ke-Qing Gao, Chunhui Liu, Jun Huang, Qiaoyun Li, Zixue Song, Peiyi Zhu, Yongguan Zhou, Jizhong Cai, Peng Nat Commun Article The role of microbial interactions and the underlying mechanisms that shape complex biofilm communities are poorly understood. Here we employ a microfluidic chip to represent porous subsurface environments and show that cooperative microbial interactions between free-living and biofilm-forming bacteria trigger active spatial segregation to promote their respective dominance in segregated microhabitats. During initial colonization, free-living and biofilm-forming microbes are segregated from the mixed planktonic inoculum to occupy the ambient fluid and grain surface. Contrary to spatial exclusion through competition, the active spatial segregation is induced by cooperative interactions which improves the fitness of both biofilm and planktonic populations. We further show that free-living Arthrobacter induces the surface colonization by scavenging the biofilm inhibitor, D-amino acids and receives benefits from the public goods secreted by the biofilm-forming strains. Collectively, our results reveal how cooperative microbial interactions may contribute to microbial coexistence in segregated microhabitats and drive subsurface biofilm community succession. Nature Publishing Group UK 2023-07-15 /pmc/articles/PMC10349867/ /pubmed/37454222 http://dx.doi.org/10.1038/s41467-023-39991-4 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, 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 license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license 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 license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Wu, Yichao
Fu, Chengxia
Peacock, Caroline L.
Sørensen, Søren J.
Redmile-Gordon, Marc A.
Xiao, Ke-Qing
Gao, Chunhui
Liu, Jun
Huang, Qiaoyun
Li, Zixue
Song, Peiyi
Zhu, Yongguan
Zhou, Jizhong
Cai, Peng
Cooperative microbial interactions drive spatial segregation in porous environments
title Cooperative microbial interactions drive spatial segregation in porous environments
title_full Cooperative microbial interactions drive spatial segregation in porous environments
title_fullStr Cooperative microbial interactions drive spatial segregation in porous environments
title_full_unstemmed Cooperative microbial interactions drive spatial segregation in porous environments
title_short Cooperative microbial interactions drive spatial segregation in porous environments
title_sort cooperative microbial interactions drive spatial segregation in porous environments
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10349867/
https://www.ncbi.nlm.nih.gov/pubmed/37454222
http://dx.doi.org/10.1038/s41467-023-39991-4
work_keys_str_mv AT wuyichao cooperativemicrobialinteractionsdrivespatialsegregationinporousenvironments
AT fuchengxia cooperativemicrobialinteractionsdrivespatialsegregationinporousenvironments
AT peacockcarolinel cooperativemicrobialinteractionsdrivespatialsegregationinporousenvironments
AT sørensensørenj cooperativemicrobialinteractionsdrivespatialsegregationinporousenvironments
AT redmilegordonmarca cooperativemicrobialinteractionsdrivespatialsegregationinporousenvironments
AT xiaokeqing cooperativemicrobialinteractionsdrivespatialsegregationinporousenvironments
AT gaochunhui cooperativemicrobialinteractionsdrivespatialsegregationinporousenvironments
AT liujun cooperativemicrobialinteractionsdrivespatialsegregationinporousenvironments
AT huangqiaoyun cooperativemicrobialinteractionsdrivespatialsegregationinporousenvironments
AT lizixue cooperativemicrobialinteractionsdrivespatialsegregationinporousenvironments
AT songpeiyi cooperativemicrobialinteractionsdrivespatialsegregationinporousenvironments
AT zhuyongguan cooperativemicrobialinteractionsdrivespatialsegregationinporousenvironments
AT zhoujizhong cooperativemicrobialinteractionsdrivespatialsegregationinporousenvironments
AT caipeng cooperativemicrobialinteractionsdrivespatialsegregationinporousenvironments