Metabolic interactions affect the biomass of synthetic bacterial biofilm communities

ABSTRACTMicrobes typically reside in communities containing multiple species, whose interactions have considerable impacts on the robustness and functionality of such communities. To manage microbial communities, it is essential to understand the factors driving their assemblage and maintenance. Eve...

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Main Authors: Xinli Sun, Jiyu Xie, Daoyue Zheng, Riyan Xia, Wei Wang, Weibing Xun, Qiwei Huang, Ruifu Zhang, Ákos T. Kovács, Zhihui Xu, Qirong Shen
Format: Article
Language:English
Published: American Society for Microbiology 2023-12-01
Series:mSystems
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/msystems.01045-23
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author Xinli Sun
Jiyu Xie
Daoyue Zheng
Riyan Xia
Wei Wang
Weibing Xun
Qiwei Huang
Ruifu Zhang
Ákos T. Kovács
Zhihui Xu
Qirong Shen
author_facet Xinli Sun
Jiyu Xie
Daoyue Zheng
Riyan Xia
Wei Wang
Weibing Xun
Qiwei Huang
Ruifu Zhang
Ákos T. Kovács
Zhihui Xu
Qirong Shen
author_sort Xinli Sun
collection DOAJ
description ABSTRACTMicrobes typically reside in communities containing multiple species, whose interactions have considerable impacts on the robustness and functionality of such communities. To manage microbial communities, it is essential to understand the factors driving their assemblage and maintenance. Even though the community composition could be easily assessed, interspecies interactions during community establishment remain poorly understood. Here, we combined co-occurrence network analysis with quantitative PCR to examine the importance of each species within synthetic communities (SynComs) of pellicle biofilms. Genome-scale metabolic models and in vitro experiments indicated that the biomass of SynComs was primarily affected by keystone species that are acting either as metabolic facilitators or as competitors. Our study sets an example of how to construct a SynCom and investigate interspecies interactions.IMPORTANCECo-occurrence network analysis is an effective tool for predicting complex networks of microbial interactions in the natural environment. Using isolates from a rhizosphere, we constructed multi-species biofilm communities and investigated co-occurrence patterns between microbial species in genome-scale metabolic models and in vitro experiments. According to our results, metabolic exchanges and resource competition may partially explain the co-occurrence network analysis results found in synthetic bacterial biofilm communities.
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spelling doaj.art-d9e42fec3e3a4f1a8ab7f2d248c0dedc2023-12-21T14:02:34ZengAmerican Society for MicrobiologymSystems2379-50772023-12-018610.1128/msystems.01045-23Metabolic interactions affect the biomass of synthetic bacterial biofilm communitiesXinli Sun0Jiyu Xie1Daoyue Zheng2Riyan Xia3Wei Wang4Weibing Xun5Qiwei Huang6Ruifu Zhang7Ákos T. Kovács8Zhihui Xu9Qirong Shen10Key lab of organic-based fertilizers of China and Jiangsu provincial key lab for solid organic waste utilization, Nanjing Agricultural University, Nanjing, Jiangsu, ChinaKey lab of organic-based fertilizers of China and Jiangsu provincial key lab for solid organic waste utilization, Nanjing Agricultural University, Nanjing, Jiangsu, ChinaKey lab of organic-based fertilizers of China and Jiangsu provincial key lab for solid organic waste utilization, Nanjing Agricultural University, Nanjing, Jiangsu, ChinaKey lab of organic-based fertilizers of China and Jiangsu provincial key lab for solid organic waste utilization, Nanjing Agricultural University, Nanjing, Jiangsu, ChinaKey lab of organic-based fertilizers of China and Jiangsu provincial key lab for solid organic waste utilization, Nanjing Agricultural University, Nanjing, Jiangsu, ChinaKey lab of organic-based fertilizers of China and Jiangsu provincial key lab for solid organic waste utilization, Nanjing Agricultural University, Nanjing, Jiangsu, ChinaKey lab of organic-based fertilizers of China and Jiangsu provincial key lab for solid organic waste utilization, Nanjing Agricultural University, Nanjing, Jiangsu, ChinaKey lab of organic-based fertilizers of China and Jiangsu provincial key lab for solid organic waste utilization, Nanjing Agricultural University, Nanjing, Jiangsu, ChinaBacterial Interactions and Evolution Group, DTU Bioengineering, Technical University of Denmark, Kongens Lyngby, DenmarkKey lab of organic-based fertilizers of China and Jiangsu provincial key lab for solid organic waste utilization, Nanjing Agricultural University, Nanjing, Jiangsu, ChinaKey lab of organic-based fertilizers of China and Jiangsu provincial key lab for solid organic waste utilization, Nanjing Agricultural University, Nanjing, Jiangsu, ChinaABSTRACTMicrobes typically reside in communities containing multiple species, whose interactions have considerable impacts on the robustness and functionality of such communities. To manage microbial communities, it is essential to understand the factors driving their assemblage and maintenance. Even though the community composition could be easily assessed, interspecies interactions during community establishment remain poorly understood. Here, we combined co-occurrence network analysis with quantitative PCR to examine the importance of each species within synthetic communities (SynComs) of pellicle biofilms. Genome-scale metabolic models and in vitro experiments indicated that the biomass of SynComs was primarily affected by keystone species that are acting either as metabolic facilitators or as competitors. Our study sets an example of how to construct a SynCom and investigate interspecies interactions.IMPORTANCECo-occurrence network analysis is an effective tool for predicting complex networks of microbial interactions in the natural environment. Using isolates from a rhizosphere, we constructed multi-species biofilm communities and investigated co-occurrence patterns between microbial species in genome-scale metabolic models and in vitro experiments. According to our results, metabolic exchanges and resource competition may partially explain the co-occurrence network analysis results found in synthetic bacterial biofilm communities.https://journals.asm.org/doi/10.1128/msystems.01045-23soil microbiologySynComsbiofilmsnetwork analysismetabolic modeling
spellingShingle Xinli Sun
Jiyu Xie
Daoyue Zheng
Riyan Xia
Wei Wang
Weibing Xun
Qiwei Huang
Ruifu Zhang
Ákos T. Kovács
Zhihui Xu
Qirong Shen
Metabolic interactions affect the biomass of synthetic bacterial biofilm communities
mSystems
soil microbiology
SynComs
biofilms
network analysis
metabolic modeling
title Metabolic interactions affect the biomass of synthetic bacterial biofilm communities
title_full Metabolic interactions affect the biomass of synthetic bacterial biofilm communities
title_fullStr Metabolic interactions affect the biomass of synthetic bacterial biofilm communities
title_full_unstemmed Metabolic interactions affect the biomass of synthetic bacterial biofilm communities
title_short Metabolic interactions affect the biomass of synthetic bacterial biofilm communities
title_sort metabolic interactions affect the biomass of synthetic bacterial biofilm communities
topic soil microbiology
SynComs
biofilms
network analysis
metabolic modeling
url https://journals.asm.org/doi/10.1128/msystems.01045-23
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AT riyanxia metabolicinteractionsaffectthebiomassofsyntheticbacterialbiofilmcommunities
AT weiwang metabolicinteractionsaffectthebiomassofsyntheticbacterialbiofilmcommunities
AT weibingxun metabolicinteractionsaffectthebiomassofsyntheticbacterialbiofilmcommunities
AT qiweihuang metabolicinteractionsaffectthebiomassofsyntheticbacterialbiofilmcommunities
AT ruifuzhang metabolicinteractionsaffectthebiomassofsyntheticbacterialbiofilmcommunities
AT akostkovacs metabolicinteractionsaffectthebiomassofsyntheticbacterialbiofilmcommunities
AT zhihuixu metabolicinteractionsaffectthebiomassofsyntheticbacterialbiofilmcommunities
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