Biosurfactant-Mediated Membrane Depolarization Maintains Viability during Oxygen Depletion in Bacillus subtilis

• Published in: Current biology Vol. 30; no. 6; pp. 1011 - 1022.e6
• Main Authors: Arjes, Heidi A., Vo, Lam, Dunn, Caroline M., Willis, Lisa, DeRosa, Christopher A., Fraser, Cassandra L., Kearns, Daniel B., Huang, Kerwyn Casey
• Format: Journal Article
• Language: English
• Published: England Elsevier Inc 23.03.2020
• Subjects: 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; surfactin; oxygen diffusion; hypoxia; biosurfactant; oxygen depletion; membrane depolarization; membrane potential; aerobic respiration; cell lysis
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2020.01.073

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.