Negative Interplay between Biofilm Formation and Competence in the Environmental Strains of <italic toggle="yes">Bacillus subtilis</italic>

ABSTRACT Environmental strains of the soil bacterium Bacillus subtilis have valuable applications in agriculture, industry, and biotechnology; however, environmental strains are genetically less accessible. This reduced accessibility is in sharp contrast to laboratory strains, which are well known f...

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Autores principales:	Qianxuan She, Evan Hunter, Yuxuan Qin, Samantha Nicolau, Eliza A. Zalis, Hongkai Wang, Yun Chen, Yunrong Chai
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	biofilm competence Bacillus subtilis cell differentiation environmental strains Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/d3ab0ca95c48483c943ca03bb485989b
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spelling	oai:doaj.org-article:d3ab0ca95c48483c943ca03bb485989b2021-12-02T18:15:47ZNegative Interplay between Biofilm Formation and Competence in the Environmental Strains of <italic toggle="yes">Bacillus subtilis</italic>10.1128/mSystems.00539-202379-5077https://doaj.org/article/d3ab0ca95c48483c943ca03bb485989b2020-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00539-20https://doaj.org/toc/2379-5077ABSTRACT Environmental strains of the soil bacterium Bacillus subtilis have valuable applications in agriculture, industry, and biotechnology; however, environmental strains are genetically less accessible. This reduced accessibility is in sharp contrast to laboratory strains, which are well known for their natural competence, and a limitation in their applications. In this study, we observed that robust biofilm formation by environmental strains of B. subtilis greatly reduced the frequency of competent cells in the biofilm. By using model strain 3610, we revealed a cross-pathway regulation that allows biofilm matrix producers and competence-developing cells to undergo mutually exclusive cell differentiation. We further demonstrated that the competence activator ComK represses the key biofilm regulatory gene sinI by directly binding to the sinI promoter, thus blocking competent cells from simultaneously becoming matrix producers. In parallel, the biofilm activator SlrR represses competence through three distinct mechanisms involving both genetic regulation and cell morphological changes. Finally, we discuss the potential implications of limiting competence in a bacterial biofilm. IMPORTANCE The soil bacterium Bacillus subtilis can form robust biofilms, which are important for its survival in the environment. B. subtilis also exhibits natural competence. By investigating competence development in B. subtilis in situ during biofilm formation, we reveal that robust biofilm formation often greatly reduces the frequency of competent cells within the biofilm. We then characterize a cross-pathway regulation that allows cells in these two developmental events to undergo mutually exclusive cell differentiation during biofilm formation. Finally, we discuss potential biological implications of limiting competence in a bacterial biofilm.Qianxuan SheEvan HunterYuxuan QinSamantha NicolauEliza A. ZalisHongkai WangYun ChenYunrong ChaiAmerican Society for MicrobiologyarticlebiofilmcompetenceBacillus subtiliscell differentiationenvironmental strainsMicrobiologyQR1-502ENmSystems, Vol 5, Iss 5 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	biofilm competence Bacillus subtilis cell differentiation environmental strains Microbiology QR1-502
spellingShingle	biofilm competence Bacillus subtilis cell differentiation environmental strains Microbiology QR1-502 Qianxuan She Evan Hunter Yuxuan Qin Samantha Nicolau Eliza A. Zalis Hongkai Wang Yun Chen Yunrong Chai Negative Interplay between Biofilm Formation and Competence in the Environmental Strains of <italic toggle="yes">Bacillus subtilis</italic>
description	ABSTRACT Environmental strains of the soil bacterium Bacillus subtilis have valuable applications in agriculture, industry, and biotechnology; however, environmental strains are genetically less accessible. This reduced accessibility is in sharp contrast to laboratory strains, which are well known for their natural competence, and a limitation in their applications. In this study, we observed that robust biofilm formation by environmental strains of B. subtilis greatly reduced the frequency of competent cells in the biofilm. By using model strain 3610, we revealed a cross-pathway regulation that allows biofilm matrix producers and competence-developing cells to undergo mutually exclusive cell differentiation. We further demonstrated that the competence activator ComK represses the key biofilm regulatory gene sinI by directly binding to the sinI promoter, thus blocking competent cells from simultaneously becoming matrix producers. In parallel, the biofilm activator SlrR represses competence through three distinct mechanisms involving both genetic regulation and cell morphological changes. Finally, we discuss the potential implications of limiting competence in a bacterial biofilm. IMPORTANCE The soil bacterium Bacillus subtilis can form robust biofilms, which are important for its survival in the environment. B. subtilis also exhibits natural competence. By investigating competence development in B. subtilis in situ during biofilm formation, we reveal that robust biofilm formation often greatly reduces the frequency of competent cells within the biofilm. We then characterize a cross-pathway regulation that allows cells in these two developmental events to undergo mutually exclusive cell differentiation during biofilm formation. Finally, we discuss potential biological implications of limiting competence in a bacterial biofilm.
format	article
author	Qianxuan She Evan Hunter Yuxuan Qin Samantha Nicolau Eliza A. Zalis Hongkai Wang Yun Chen Yunrong Chai
author_facet	Qianxuan She Evan Hunter Yuxuan Qin Samantha Nicolau Eliza A. Zalis Hongkai Wang Yun Chen Yunrong Chai
author_sort	Qianxuan She
title	Negative Interplay between Biofilm Formation and Competence in the Environmental Strains of <italic toggle="yes">Bacillus subtilis</italic>
title_short	Negative Interplay between Biofilm Formation and Competence in the Environmental Strains of <italic toggle="yes">Bacillus subtilis</italic>
title_full	Negative Interplay between Biofilm Formation and Competence in the Environmental Strains of <italic toggle="yes">Bacillus subtilis</italic>
title_fullStr	Negative Interplay between Biofilm Formation and Competence in the Environmental Strains of <italic toggle="yes">Bacillus subtilis</italic>
title_full_unstemmed	Negative Interplay between Biofilm Formation and Competence in the Environmental Strains of <italic toggle="yes">Bacillus subtilis</italic>
title_sort	negative interplay between biofilm formation and competence in the environmental strains of <italic toggle="yes">bacillus subtilis</italic>
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/d3ab0ca95c48483c943ca03bb485989b
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Negative Interplay between Biofilm Formation and Competence in the Environmental Strains of <italic toggle="yes">Bacillus subtilis</italic>

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