Cheaters shape the evolution of phenotypic heterogeneity in <i>Bacillus subtilis</i> biofilms

Martin, Marivic; Dragoš, Anna; Otto, Simon B.; Schafer, Daniel W.; Brix, Susanne; Maróti, Gergely; Kovács, Ákos T.

doi:10.1038/s41396-020-0685-4

Cited by 28 publications

(30 citation statements)

References 53 publications

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“…Here, we showed that in the initial stage of biofilm formation, the majority of the population was in an ON state, followed by heterogeneity in older biofilms. We show that in the timeframe between [16][17][18][19][20] hours, where an increase of robust pellicle biomass is the most pronounced (Fig 1D), there is a significant shift eps-expression intensity and switching ON of tasA expression in nearly all biofilm cells. Therefore, our results link temporal dynamics in matrix genes expression with temporal changes of robust biofilm biomass.…”

Section: Discussionmentioning

confidence: 80%

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Privatization of biofilm matrix in structurally heterogeneous biofilms

Otto¹,

Martin

Schafer

et al. 2019

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ABSTRACTThe self-produced biofilm provides beneficial protection for the enclosed cells, but the costly production of matrix components makes producer cells susceptible to cheating by non-producing individuals. Despite detrimental effects of non-producers, biofilms can be heterogeneous, with isogenic non-producers being a natural consequence of phenotypic differentiation processes. For instance, in Bacillus subtilis biofilm cells differ in the two major matrix components production, the amyloid fiber protein TasA and exopolysaccharides (EPS), demonstrating different expression levels of corresponding matrix genes. This raises questions regarding matrix gene expression dynamics during biofilm development and the impact of phenotypic non-producers on biofilm robustness. Here, we show that biofilms are structurally heterogeneous and can be separated into strongly and weakly associated clusters. We reveal that spatiotemporal changes in structural heterogeneity correlate with matrix gene expression, with TasA playing a key role in biofilm integrity and timing of development. We show that the matrix remains partially privatized by the producer subpopulation, where cells tightly stick together even when exposed to shear stress. Our results support previous findings on the existence of ‘weak points’ in seemingly robust biofilms as well as on the key role of linkage proteins in biofilm formation. Furthermore, we provide a starting point for investigating the privatization of common goods within isogenic populations.IMPORTANCEBiofilms are communities of bacteria protected by a self-produced extracellular matrix. The detrimental effects of non-producing individuals on biofilm development raises questions about the dynamics between community members, especially when isogenic non-producers exist within wild-type populations. We asked ourselves whether phenotypic non-producers impact biofilm robustness, and where and when this heterogeneity of matrix gene expression occurs. Based on our results we propose that the matrix remains partly privatized by the producing subpopulation, since producing cells stick together when exposed to shear stress. The important role of linkage proteins in robustness and development of the structurally heterogeneous biofilm provides an entry into studying the privatization of common goods within isogenic populations.

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Section: Discussionmentioning

confidence: 80%

“…We began from a simple question: does phenotypic heterogeneity of matrix gene expression in B. subtilis (16,19,37) translate into non-uniform robustness within the biofilm? We will refer to such non-uniform biofilm robustness as "structural heterogeneity".…”

Section: Structural Heterogeneity Develops In Late Stages Of Pelliclementioning

confidence: 99%

Privatization of biofilm matrix in structurally heterogeneous biofilms

Otto¹,

Martin

Schafer

et al. 2019

Preprint

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“…Structural heterogeneity develops in late stages of pellicle growth. We began from a simple question: does phenotypic heterogeneity of matrix gene expression in B. subtilis (16,19,37) translate into nonuniform robustness within the biofilm? We will refer to such nonuniform biofilm robustness as "structural heterogeneity."…”

Section: Resultsmentioning

confidence: 99%

“…We began from a simple question: does phenotypic heterogeneity of matrix gene expression in B. subtilis ( 16 , 19 , 37 ) translate into nonuniform robustness within the biofilm? We will refer to such nonuniform biofilm robustness as “structural heterogeneity.” Biofilms were mechanically disrupted by vortexing with sterile glass sand ( Fig.…”

Section: Resultsmentioning

confidence: 99%

“…Alternatively, production of the matrix components may not be easily exploitable if there is limited sharing, low cost of production, or spatial assortment of cells within the biofilm (14,15). Finally, long-term cheating on matrix production may have evolutionary consequences for the producers, changing the phenotypic heterogeneity pattern of matrix expression within the population (16).…”

mentioning

confidence: 99%

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Privatization of Biofilm Matrix in Structurally Heterogeneous Biofilms

et al. 2020

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The self-produced biofilm provides beneficial protection for the enclosed cells, but the costly production of matrix components makes producer cells susceptible to cheating by nonproducing individuals. Despite detrimental effects of nonproducers, biofilms can be heterogeneous, with isogenic nonproducers being a natural consequence of phenotypic differentiation processes. For instance, in Bacillus subtilis biofilm cells differ in production of the two major matrix components, the amyloid fiber protein TasA and exopolysaccharides (EPS), demonstrating different expression levels of corresponding matrix genes. This raises questions regarding matrix gene expression dynamics during biofilm development and the impact of phenotypic nonproducers on biofilm robustness. Here, we show that biofilms are structurally heterogeneous and can be separated into strongly and weakly associated clusters. We reveal that spatiotemporal changes in structural heterogeneity correlate with matrix gene expression, with TasA playing a key role in biofilm integrity and timing of development. We show that the matrix remains partially privatized by the producer subpopulation, where cells tightly stick together even when exposed to shear stress. Our results support previous findings on the existence of “weak points” in seemingly robust biofilms as well as on the key role of linkage proteins in biofilm formation. Furthermore, we provide a starting point for investigating the privatization of common goods within isogenic populations. IMPORTANCE Biofilms are communities of bacteria protected by a self-produced extracellular matrix. The detrimental effects of nonproducing individuals on biofilm development raise questions about the dynamics between community members, especially when isogenic nonproducers exist within wild-type populations. We asked ourselves whether phenotypic nonproducers impact biofilm robustness, and where and when this heterogeneity of matrix gene expression occurs. Based on our results, we propose that the matrix remains partly privatized by the producing subpopulation, since producing cells stick together when exposed to shear stress. The important role of linkage proteins in robustness and development of the structurally heterogeneous biofilm provides an entry into studying the privatization of common goods within isogenic populations.

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