Biosurfactant-Mediated Membrane Depolarization Maintains Viability during Oxygen Depletion in Bacillus subtilis
The presence or absence of oxygen in the environment is a strong effector of cellular metabolism and physiology. Like many eukaryotes and some bacteria, Bacillus subtilis primarily utilizes oxygen during respiration to generate ATP. Despite the importance of oxygen for B. subtilis survival, we know...
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Published in | Current biology Vol. 30; no. 6; pp. 1011 - 1022.e6 |
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Main Authors | , , , , , , , |
Format | Journal Article |
Language | English |
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Elsevier Inc
23.03.2020
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Abstract | The presence or absence of oxygen in the environment is a strong effector of cellular metabolism and physiology. Like many eukaryotes and some bacteria, Bacillus subtilis primarily utilizes oxygen during respiration to generate ATP. Despite the importance of oxygen for B. subtilis survival, we know little about how populations adapt to shifts in oxygen availability. Here, we find that when oxygen was depleted from stationary phase B. subtilis cultures, ∼90% of cells died while the remaining cells maintained colony-forming ability. We discover that production of the antimicrobial surfactin confers two oxygen-related fitness benefits: it increases aerobic growth yield by increasing oxygen diffusion, and it maintains viability during oxygen depletion by depolarizing the membrane. Strains unable to produce surfactin exhibited an ∼50-fold reduction in viability after oxygen depletion. Surfactin treatment of these cells led to membrane depolarization and reduced ATP production. Chemical and genetic perturbations that alter oxygen consumption or redox state support a model in which surfactin-mediated membrane depolarization maintains viability through slower oxygen consumption and/or a shift to a more reduced metabolic profile. These findings highlight the importance of membrane potential in regulating cell physiology and growth, and demonstrate that antimicrobials that depolarize cell membranes can benefit cells when the terminal electron acceptor in respiration is limiting. This foundational knowledge has deep implications for environmental microbiology, clinical anti-bacterial therapy, and industrial biotechnology.
[Display omitted]
•The majority of Bacillus subtilis cells die upon oxygen depletion•Surfactin production depolarizes cells to maintain viability upon oxygen depletion•Surfactin promotes growth in early stationary phase by enhancing oxygen diffusion•The autolytic enzyme LytC and surfactin mediate lysis upon oxygen depletion
Cells possess many mechanisms to cope with oxygen deprivation. Arjes et al. show that although oxygen depletion kills the majority of Bacillus subtilis bacteria, a fraction remains viable due to the surfactant surfactin, which mediates survival by depolarizing the membrane. Surfactin also increases oxygen diffusion to promote growth in low oxygen. |
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AbstractList | The presence or absence of oxygen in the environment is a strong effector of cellular metabolism and physiology. Like many eukaryotes and some bacteria,
Bacillus subtilis
primarily utilizes oxygen during respiration to generate ATP. Despite the importance of oxygen for
B. subtilis
survival, we know little about how populations adapt to shifts in oxygen availability. Here, we find that when oxygen was depleted from stationary phase
B. subtilis
cultures, ~90% of cells died while the remaining cells maintained colony-forming ability. We discover that production of the antimicrobial surfactin confers two oxygen-related fitness benefits: it increases aerobic growth yield due to increased oxygen diffusion, and it maintains viability during oxygen depletion by depolarizing the membrane. Strains unable to produce surfactin exhibited a ~50-fold reduction in viability after oxygen depletion. Surfactin treatment of these cells led to membrane depolarization and reduced ATP production. Chemical and genetic perturbations that alter oxygen consumption or redox state support a model in which surfactin-mediated membrane depolarization maintains viability through slower oxygen consumption and/or a shift to a more reduced metabolic profile. These findings highlight the importance of membrane potential in regulating cell physiology and growth, and demonstrate that antimicrobials that depolarize cell membranes can benefit cells when the terminal electron acceptor in respiration is limiting. This foundational knowledge has deep implications for environmental microbiology, clinical anti-bacterial therapy, and industrial biotechnology.
Cells possess many mechanisms to cope with oxygen deprivation. Arjes
et al.
show that although oxygen depletion kills the majority of
Bacillus subtilis
bacteria, a fraction remains viable due to the surfactant surfactin, which mediates survival by depolarizing the membrane. Surfactin also increases oxygen diffusion to promote growth in low oxygen. The presence or absence of oxygen in the environment is a strong effector of cellular metabolism and physiology. Like many eukaryotes and some bacteria, Bacillus subtilis primarily utilizes oxygen during respiration to generate ATP. Despite the importance of oxygen for B. subtilis survival, we know little about how populations adapt to shifts in oxygen availability. Here, we find that when oxygen was depleted from stationary phase B. subtilis cultures, ∼90% of cells died while the remaining cells maintained colony-forming ability. We discover that production of the antimicrobial surfactin confers two oxygen-related fitness benefits: it increases aerobic growth yield by increasing oxygen diffusion, and it maintains viability during oxygen depletion by depolarizing the membrane. Strains unable to produce surfactin exhibited an ∼50-fold reduction in viability after oxygen depletion. Surfactin treatment of these cells led to membrane depolarization and reduced ATP production. Chemical and genetic perturbations that alter oxygen consumption or redox state support a model in which surfactin-mediated membrane depolarization maintains viability through slower oxygen consumption and/or a shift to a more reduced metabolic profile. These findings highlight the importance of membrane potential in regulating cell physiology and growth, and demonstrate that antimicrobials that depolarize cell membranes can benefit cells when the terminal electron acceptor in respiration is limiting. This foundational knowledge has deep implications for environmental microbiology, clinical anti-bacterial therapy, and industrial biotechnology. The presence or absence of oxygen in the environment is a strong effector of cellular metabolism and physiology. Like many eukaryotes and some bacteria, Bacillus subtilis primarily utilizes oxygen during respiration to generate ATP. Despite the importance of oxygen for B. subtilis survival, we know little about how populations adapt to shifts in oxygen availability. Here, we find that when oxygen was depleted from stationary phase B. subtilis cultures, ∼90% of cells died while the remaining cells maintained colony-forming ability. We discover that production of the antimicrobial surfactin confers two oxygen-related fitness benefits: it increases aerobic growth yield by increasing oxygen diffusion, and it maintains viability during oxygen depletion by depolarizing the membrane. Strains unable to produce surfactin exhibited an ∼50-fold reduction in viability after oxygen depletion. Surfactin treatment of these cells led to membrane depolarization and reduced ATP production. Chemical and genetic perturbations that alter oxygen consumption or redox state support a model in which surfactin-mediated membrane depolarization maintains viability through slower oxygen consumption and/or a shift to a more reduced metabolic profile. These findings highlight the importance of membrane potential in regulating cell physiology and growth, and demonstrate that antimicrobials that depolarize cell membranes can benefit cells when the terminal electron acceptor in respiration is limiting. This foundational knowledge has deep implications for environmental microbiology, clinical anti-bacterial therapy, and industrial biotechnology. The presence or absence of oxygen in the environment is a strong effector of cellular metabolism and physiology. Like many eukaryotes and some bacteria, Bacillus subtilis primarily utilizes oxygen during respiration to generate ATP. Despite the importance of oxygen for B. subtilis survival, we know little about how populations adapt to shifts in oxygen availability. Here, we find that when oxygen was depleted from stationary phase B. subtilis cultures, ∼90% of cells died while the remaining cells maintained colony-forming ability. We discover that production of the antimicrobial surfactin confers two oxygen-related fitness benefits: it increases aerobic growth yield by increasing oxygen diffusion, and it maintains viability during oxygen depletion by depolarizing the membrane. Strains unable to produce surfactin exhibited an ∼50-fold reduction in viability after oxygen depletion. Surfactin treatment of these cells led to membrane depolarization and reduced ATP production. Chemical and genetic perturbations that alter oxygen consumption or redox state support a model in which surfactin-mediated membrane depolarization maintains viability through slower oxygen consumption and/or a shift to a more reduced metabolic profile. These findings highlight the importance of membrane potential in regulating cell physiology and growth, and demonstrate that antimicrobials that depolarize cell membranes can benefit cells when the terminal electron acceptor in respiration is limiting. This foundational knowledge has deep implications for environmental microbiology, clinical anti-bacterial therapy, and industrial biotechnology. [Display omitted] •The majority of Bacillus subtilis cells die upon oxygen depletion•Surfactin production depolarizes cells to maintain viability upon oxygen depletion•Surfactin promotes growth in early stationary phase by enhancing oxygen diffusion•The autolytic enzyme LytC and surfactin mediate lysis upon oxygen depletion Cells possess many mechanisms to cope with oxygen deprivation. Arjes et al. show that although oxygen depletion kills the majority of Bacillus subtilis bacteria, a fraction remains viable due to the surfactant surfactin, which mediates survival by depolarizing the membrane. Surfactin also increases oxygen diffusion to promote growth in low oxygen. |
Author | Willis, Lisa Kearns, Daniel B. Dunn, Caroline M. DeRosa, Christopher A. Arjes, Heidi A. Vo, Lam Fraser, Cassandra L. Huang, Kerwyn Casey |
AuthorAffiliation | 3 Department of Chemistry, McCormick Road, University of Virginia, Charlottesville, VA 22904, USA 2 Department of Biology, 1001 E 3rd St, Indiana University, Bloomington, IN 47405, USA 4 Department of Microbiology & Immunology, Stanford University School of Medicine, 300 Pasteur Dr, Stanford, CA 94305, USA 5 Chan Zuckerberg Biohub, 499 Illinois St, San Francisco, CA 94158, USA 1 Department of Bioengineering, Stanford University School of Medicine, 443 via Ortega, Stanford, CA 94305, USA |
AuthorAffiliation_xml | – name: 2 Department of Biology, 1001 E 3rd St, Indiana University, Bloomington, IN 47405, USA – name: 3 Department of Chemistry, McCormick Road, University of Virginia, Charlottesville, VA 22904, USA – name: 4 Department of Microbiology & Immunology, Stanford University School of Medicine, 300 Pasteur Dr, Stanford, CA 94305, USA – name: 1 Department of Bioengineering, Stanford University School of Medicine, 443 via Ortega, Stanford, CA 94305, USA – name: 5 Chan Zuckerberg Biohub, 499 Illinois St, San Francisco, CA 94158, USA |
Author_xml | – sequence: 1 givenname: Heidi A. surname: Arjes fullname: Arjes, Heidi A. organization: Department of Bioengineering, Stanford University School of Medicine, 443 via Ortega, Stanford, CA 94305, USA – sequence: 2 givenname: Lam surname: Vo fullname: Vo, Lam organization: Department of Bioengineering, Stanford University School of Medicine, 443 via Ortega, Stanford, CA 94305, USA – sequence: 3 givenname: Caroline M. surname: Dunn fullname: Dunn, Caroline M. organization: Department of Biology, 1001 E 3rd Street, Indiana University, Bloomington, IN 47405, USA – sequence: 4 givenname: Lisa surname: Willis fullname: Willis, Lisa organization: Department of Bioengineering, Stanford University School of Medicine, 443 via Ortega, Stanford, CA 94305, USA – sequence: 5 givenname: Christopher A. surname: DeRosa fullname: DeRosa, Christopher A. organization: Department of Chemistry, McCormick Road, University of Virginia, Charlottesville, VA 22904, USA – sequence: 6 givenname: Cassandra L. surname: Fraser fullname: Fraser, Cassandra L. organization: Department of Chemistry, McCormick Road, University of Virginia, Charlottesville, VA 22904, USA – sequence: 7 givenname: Daniel B. surname: Kearns fullname: Kearns, Daniel B. email: dbkearns@indiana.edu organization: Department of Biology, 1001 E 3rd Street, Indiana University, Bloomington, IN 47405, USA – sequence: 8 givenname: Kerwyn Casey surname: Huang fullname: Huang, Kerwyn Casey email: kchuang@stanford.edu organization: Department of Bioengineering, Stanford University School of Medicine, 443 via Ortega, Stanford, CA 94305, USA |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/32059765$$D View this record in MEDLINE/PubMed |
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Keywords | surfactin oxygen diffusion hypoxia biosurfactant oxygen depletion membrane depolarization membrane potential aerobic respiration cell lysis |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 H.A., D.B.K., and K.C.H. designed the research. H.A., L.V., L.W., C.M.D., performed the research. C.A.D and C.L.F provided reagents. H.A., L.V., L.W., C.M.D, D.B.K., and K.C.H. analyzed data and wrote the paper. Author Contributions |
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SubjectTerms | aerobic respiration Bacillus subtilis - physiology Bacterial Proteins - metabolism biosurfactant cell lysis Cell Membrane - physiology hypoxia membrane depolarization membrane potential Oxygen - metabolism oxygen depletion oxygen diffusion surfactin |
Title | Biosurfactant-Mediated Membrane Depolarization Maintains Viability during Oxygen Depletion in Bacillus subtilis |
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