Social evolution of shared biofilm matrix components.
Social evolution of shared biofilm matrix components.
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DOI:
10.1073/pnas.2123469119
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发表时间:
2022-07-05
影响因子:
11.1
通讯作者:
Yan, Jing
中科院分区:
文献类型:
--
作者:
Tai, Jung-Shen B.;Mukherjee, Saikat;Nero, Thomas;Olson, Rich;Tithof, Jeffrey;Nadell, Carey D.;Yan, Jing
Biofilms are an important mode of bacterial growth where surface-attached cells enjoy survival advantages provided by the extracellular matrix composed of secreted, diffusible biopolymers. An important question is how diffusible matrix production can be stable under the evolutionary pressure of exploitation. Here, we show that some matrix proteins in Vibrio cholerae biofilms can indeed be exploited by nonproducers, but the exploitation happens within a quantifiable spatial range around the producer cell clusters. An ecological model considering the length scales of exploitation and cell group structure reveals the stable conditions for diffusible matrix production that are consistent with those in natural environments. Our study provides concepts and tools for studying public goods sharing in spatially structured bacterial biofilms. Biofilm formation is an important and ubiquitous mode of growth among bacteria. Central to the evolutionary advantage of biofilm formation is cell–cell and cell–surface adhesion achieved by a variety of factors, some of which are diffusible compounds that may operate as classical public goods—factors that are costly to produce but may benefit other cells. An outstanding question is how diffusible matrix production, in general, can be stable over evolutionary timescales. In this work, using Vibrio cholerae as a model, we show that shared diffusible biofilm matrix proteins are indeed susceptible to cheater exploitation and that the evolutionary stability of producing these matrix components fundamentally depends on biofilm spatial structure, intrinsic sharing mechanisms of these components, and flow conditions in the environment. We further show that exploitation of diffusible adhesion proteins is localized within a well-defined spatial range around cell clusters that produce them. Based on this exploitation range and the spatial distribution of cell clusters, we constructed a model of costly diffusible matrix production and related these length scales to the relatedness coefficient in social evolution theory. Our results show that production of diffusible biofilm matrix components is evolutionarily stable under conditions consistent with natural biofilm habitats and host environments. We expect the mechanisms revealed in this study to be relevant to other secreted factors that operate as cooperative public goods in bacterial communities and the concept of exploitation range and the associated analysis tools to be generally applicable.
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DOI:
10.1126/science.1222981
发表时间:
2012-07-13
期刊:
Science (New York, N.Y.)
影响因子:
--
作者:
Berk V;Fong JC;Dempsey GT;Develioglu ON;Zhuang X;Liphardt J;Yildiz FH;Chu S
通讯作者:
Chu S
影响因子:
18.3
作者:
Alcolombri, Uria;Peaudecerf, Francois J.;Stocker, Roman
通讯作者:
Stocker, Roman
DOI:
10.1016/s0967-0637(96)00104-5
发表时间:
1997-03-01
影响因子:
2.4
作者:
Diercks, AR;Asper, VL
通讯作者:
Asper, VL
影响因子:
4.1
作者:
Fischer, PF
通讯作者:
Fischer, PF
影响因子:
7.7
作者:
Fong, Jiunn C. N.;Rogers, Andrew;Yildiz, Fitnat H.
通讯作者:
Yildiz, Fitnat H.