Surfactin Activating KinB to Sense and Utilize Carbon Sources Against Cannibalism in Bacillus amyloliquefaciens.

Abstract

Bacillus species are ubiquitous microorganisms with broad applications. The lipopeptide surfactin serves as a signaling molecule to activate histidine kinases, subsequently activating the global regulatory protein Spo0A to modulate quorum sensing like cannibalism in response to specific environmental conditions such as carbon source limitation. Our previous studies revealed that deletion of the surfactin synthesis gene in Bacillus amyloliquefaciens resulted in rapid cell death during the logarithmic growth phase. In this study, by employing gene knockout strains involved in the surfactin signaling pathway, we found that B. amyloliquefaciens primarily employs histidine kinase KinB to perceive surfactin signals, enabling the utilization of environmental carbon sources. Surfactin signal transduction is not exclusively dependent on histidine kinases; cells utilize alternative pathways (e.g., cation-induced Spo0A activation) to regulate carbon source utilization. Adding glucose, NADH, and ATP all alleviated cell death in ΔsrfA cultures. Both the wild-type and ΔsrfA mutant produce polypeptide/protein-like autotoxins during growth, but ΔsrfA produced more toxins earlier. Carbon sources such as glucose inhibit autotoxin production, while surfactin initiates detoxifying against these toxins. The absence of Spo0A results in both the loss of autotoxin production and antitoxin capabilities, indicating that Spo0A regulates both toxin production and detoxification mechanisms. Collectively, we firstly reported that in B. amyloliquefaciens, cells utilize surfactin as a signaling molecule to activate KinB, which senses environmental carbon sources and thereby inhibits rather than promotes the production of autotoxins as seen in Bacillus subtilis. However, similar to B. subtilis, KinB activates Spo0A to combat autotoxins.