Abstract
Biofilms provide individual bacteria with many advantages, yet dense cellular proliferation can also create intrinsic metabolic challenges including excessive acidification. Because such pH stress can be masked in buffered laboratory media—such as MSgg commonly used to study Bacillus subtilis biofilms—it is not always clear how such biofilms cope with minimally buffered natural environments. Here, we report how B. subtilis biofilms overcome this intrinsic metabolic challenge through an active pH regulation mechanism. Specifically, we find that these biofilms can modulate their extracellular pH to the preferred neutrophile range, even when starting from acidic and alkaline initial conditions, while planktonic cells cannot. We associate this behavior with dynamic interplay between acetate and acetoin biosynthesis and show that this mechanism is required to buffer against biofilm acidification. Furthermore, we find that buffering-deficient biofilms exhibit dysregulated biofilm development when grown in minimally buffered conditions. Our findings reveal an active pH regulation mechanism in B. subtilis biofilms that could lead to new targets to control unwanted biofilm growth.
Original language | English (US) |
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Journal | mBio |
Volume | 15 |
Issue number | 3 |
DOIs | |
State | Published - Mar 2024 |
Funding
We thank Dr. Sarah Jane Quillin and Dr. Angelia Wang for comments during the writing of this manuscript. This work was supported by the Northwestern University NUSeq Core Facility. Metabolomics services were provided by the Metabolomics Core Facility at Robert H. Lurie Comprehensive Cancer Center of Northwestern University. The authors apologize to our many colleagues whose work we could not include due to space constraints. We are grateful for the generous support from the Burroughs Wellcome Fund (1015883.01), the David and Lucile Packard Foundation (2018–68055), the Army Research Office (W911NF-19-1-0136), Pew Charitable Trusts (2019-A-06953), the National Science Foundation (NSF 2239567), and the Biotechnology Training Program at Northwestern University. Research reported in this publication was also supported by the National Institute of General Medical Sciences of the National Institutes of Health under Award Number F31GM143907. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. P.T. designed the studies, carried out the research, interpreted the results, and wrote the manuscript. S.L. designed the studies, carried out the research, analyzed the data, and reviewed the manuscript. A.P. designed the study, analyzed the data, reviewed and revised the manuscript, and is responsible for the integrity of this work. All authors approved the final version of the manuscript. We are grateful for the generous support from the Burroughs Wellcome Fund (1015883.01), the David and Lucile Packard Foundation (2018–68055), the Army Research (W911NF-19-1-0136), Pew Charitable Trusts (2019-A-06953), the National Science Foundation (NSF 2239567), and the Biotechnology Training Program at Northwestern University. Research reported in this publication was also supported by the National Institute of General Medical Sciences of the National Institutes of Health under Award Number F31GM143907. The content is solely the responsibility of the authors and does not necessarily represent the views of the National Institutes of Health.
Keywords
- biofilms
- buffer
- emergent behaviors
- microbial communities
- pH
ASJC Scopus subject areas
- Microbiology
- Virology