Extracellular proteases are an essential public good supporting<i>Bacillus subtilis</i>growth through exogenous protein degradation

Rosazza, Thibault; Eigentler, Lukas; Earl, Chris; Davidson, Fordyce A.; Stanley‐Wall, Nicola R.

doi:10.1101/2023.02.08.527645

Cited by 7 publications

(7 citation statements)

References 69 publications

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“…The datasets and code generated are available in a Zenodo repository (Rosazza et al, 2024). Data was plotted using Graphpad Prism version 9.4.1 and analysed using the built-in methods as specified.…”

Section: Data Analysis and Visualisationmentioning

confidence: 99%

Reciprocal sharing of extracellular proteases and extracellular matrix molecules facilitates Bacillus subtilis biofilm formation

Rosazza,

Earl,

Eigentler

et al. 2024

Molecular Microbiology

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Extracellular proteases are a class of public good that support growth of Bacillus subtilis when nutrients are in a polymeric form. Bacillus subtilis biofilm matrix molecules are another class of public good that are needed for biofilm formation and are prone to exploitation. In this study, we investigated the role of extracellular proteases in B. subtilis biofilm formation and explored interactions between different public good producer strains across various conditions. We confirmed that extracellular proteases support biofilm formation even when glutamic acid provides a freely available nitrogen source. Removal of AprE from the NCIB 3610 secretome adversely affects colony biofilm architecture, while sole induction of WprA activity into an otherwise extracellular protease‐free strain is sufficient to promote wrinkle development within the colony biofilm. We found that changing the nutrient source used to support growth affected B. subtilis biofilm structure, hydrophobicity and architecture. We propose that the different phenotypes observed may be due to increased protease dependency for growth when a polymorphic protein presents the sole nitrogen source. We however cannot exclude that the phenotypic changes are due to alternative matrix molecules being made. Co‐culture of biofilm matrix and extracellular protease mutants can rescue biofilm structure, yet reliance on extracellular proteases for growth influences population coexistence dynamics. Our findings highlight the intricate interplay between these two classes of public goods, providing insights into microbial social dynamics during biofilm formation across different ecological niches.

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Section: Data Analysis and Visualisationmentioning

confidence: 99%

Reciprocal sharing of extracellular proteases and extracellular matrix molecules facilitates Bacillus subtilis biofilm formation

Rosazza,

Earl,

Eigentler

et al. 2024

Molecular Microbiology

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“…Computational code and experimental data sets have been deposited in the nrstanleywall GitHub repository (https://github.com/ NSWla bDund ee/) and archived by BioStudies (Rosazza et al, 2023a) and Zenodo (Rosazza et al, 2023b). Sequencing data sets have been deposited in the ENA portal (PRJEB59494).…”

Section: Statistical and Data Analysismentioning

confidence: 99%

Bacillus subtilis extracellular protease production incurs a context‐dependent cost

Rosazza

Eigentler

Earl

et al. 2023

Molecular Microbiology

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Microbes encounter a wide range of polymeric nutrient sources in various environmental settings, which require processing to facilitate growth. Bacillus subtilis, a bacterium found in the rhizosphere and broader soil environment, is highly adaptable and resilient due to its ability to utilise diverse sources of carbon and nitrogen. Here, we explore the role of extracellular proteases in supporting growth and assess the cost associated with their production. We provide evidence of the essentiality of extracellular proteases when B. subtilis is provided with an abundant, but polymeric nutrient source and demonstrate the extracellular proteases as a shared public good that can operate over a distance. We show that B. subtilis is subjected to a public good dilemma, specifically in the context of growth sustained by the digestion of a polymeric food source. Furthermore, using mathematical simulations, we uncover that this selectively enforced dilemma is driven by the relative cost of producing the public good. Collectively, our findings reveal how bacteria can survive in environments that vary in terms of immediate nutrient accessibility and the consequent impact on the population composition. These findings enhance our fundamental understanding of how bacteria respond to diverse environments, which has importance to contexts ranging from survival in the soil to infection and pathogenesis scenarios.

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“…P-values from comparison between NCIB 3610 and other relevant strains at different timepoints were included in the figures (*** = p-value<0.001, ** = p-value<0.01, *= p-value<0.05). The datasets and code generated are available in a Zenodo repository (Rosazza et al, 2023a).…”

Section: Data Analysis and Visualisationmentioning

confidence: 99%

“…Analysis code and experimental datasets have been deposited in the nrstanleywall GitHub repository (https://github.com/NSWlabDundee/) and archived by Zenodo (Rosazza et al, 2023a). The scale bar represents 5 mm.…”

Section: Competing Interestsmentioning

confidence: 99%

Reciprocal sharing of extracellular proteases and extracellular matrix molecules facilitatesBacillus subtilisbiofilm formation

Rosazza,

Earl,

Eigentler

et al. 2023

Preprint

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Public goods support the development of microbial communities but are prone to exploitation. The extracellular matrix molecules of Bacillus subtilis are examples of public goods that are produced through the division of labour and support biofilm formation. Another class of public good that supports B. subtilis growth when nutrients are in a polymeric form are extracellular proteases. In this study, we investigated the role of extracellular proteases during B. subtilis biofilm formation. We established that the extracellular proteases support biofilm growth even when the nitrogen source is available as glutamic acid. Reviewing the contribution played by each protease identified that selected individual extracellular proteases have distinct functions, with AprE found to be crucial for development and WprA sufficient for biofilm formation. We found that changing the nutrient source affected biofilm structure, hydrophobicity, and architecture, likely due to the increased cost of protease dependency for growth. Co-culture of biofilm matrix and extracellular protease mutants rescued biofilm structure through public goods sharing, but the dependence on extracellular protease for growth influenced community coexistence. The intricate sharing among these two classes of public goods sheds light on microbial social dynamics during biofilm formation in different ecological contexts.

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Extracellular proteases are an essential public good supportingBacillus subtilisgrowth through exogenous protein degradation

Cited by 7 publications

References 69 publications

Reciprocal sharing of extracellular proteases and extracellular matrix molecules facilitates Bacillus subtilis biofilm formation

Reciprocal sharing of extracellular proteases and extracellular matrix molecules facilitates Bacillus subtilis biofilm formation

Bacillus subtilis extracellular protease production incurs a context‐dependent cost

Reciprocal sharing of extracellular proteases and extracellular matrix molecules facilitatesBacillus subtilisbiofilm formation

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