Cooperative microbial interactions drive spatial segregation in porous environments

Yichao Wu, Chengxia Fu, Caroline L. Peacock, Søren J. Sørensen, Marc A. Redmile-Gordon, Ke-Qing Xiao, Chunhui Gao, Jun Liu, Qiaoyun Huang, Zixue Li, Peiyi Song, Yongguan Zhu, Jizhong Zhou and Peng Cai ()
Additional contact information
Yichao Wu: Huazhong Agricultural University
Chengxia Fu: Huazhong Agricultural University
Caroline L. Peacock: University of Leeds
Søren J. Sørensen: University of Copenhagen
Marc A. Redmile-Gordon: Royal Horticultural Society
Ke-Qing Xiao: University of Leeds
Chunhui Gao: Huazhong Agricultural University
Jun Liu: Huazhong Agricultural University
Qiaoyun Huang: Huazhong Agricultural University
Zixue Li: Huazhong University of Science and Technology
Peiyi Song: Huazhong University of Science and Technology
Yongguan Zhu: Chinese Academy of Sciences
Jizhong Zhou: University of Oklahoma
Peng Cai: Huazhong Agricultural University

Nature Communications, 2023, vol. 14, issue 1, 1-14

Abstract: Abstract 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.

Date: 2023
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DOI: 10.1038/s41467-023-39991-4

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