Respiration control of multicellularity in Bacillus subtilis by a complex of the cytochrome chain with a membrane-embedded histidine kinase

Genes Dev. 2013 Apr 15;27(8):887-99. doi: 10.1101/gad.215244.113. Epub 2013 Apr 18.

Abstract

Bacillus subtilis forms organized multicellular communities known as biofilms wherein the individual cells are held together by a self-produced extracellular matrix. The environmental signals that promote matrix synthesis remain largely unknown. We discovered that one such signal is impaired respiration. Specifically, high oxygen levels suppressed synthesis of the extracellular matrix. In contrast, low oxygen levels, in the absence of an alternative electron acceptor, led to increased matrix production. The response to impaired respiration was blocked in a mutant lacking cytochromes caa3 and bc and markedly reduced in a mutant lacking kinase KinB. Mass spectrometry of proteins associated with KinB showed that the kinase was in a complex with multiple components of the aerobic respiratory chain. We propose that KinB is activated via a redox switch involving interaction of its second transmembrane segment with one or more cytochromes under conditions of reduced electron transport. In addition, a second kinase (KinA) contributes to the response to impaired respiration. Evidence suggests that KinA is activated by a decrease in the nicotinamide adenine dinucleotide (NAD(+))/NADH ratio via binding of NAD(+) to the kinase in a PAS domain A-dependent manner. Thus, B. subtilis switches from a unicellular to a multicellular state by two pathways that independently respond to conditions of impaired respiration.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Bacillus subtilis / drug effects
  • Bacillus subtilis / enzymology
  • Bacillus subtilis / genetics
  • Bacillus subtilis / physiology*
  • Bacterial Proteins / metabolism*
  • Biofilms*
  • Cytochromes / metabolism*
  • Extracellular Matrix / drug effects
  • Extracellular Matrix / metabolism
  • Gene Expression Regulation, Bacterial
  • Histidine Kinase
  • Iron / pharmacology
  • Mutation
  • NAD / metabolism
  • Oxygen / metabolism
  • Protein Binding
  • Protein Kinases / metabolism*
  • Trace Elements / pharmacology

Substances

  • Bacterial Proteins
  • Cytochromes
  • Trace Elements
  • NAD
  • Iron
  • Protein Kinases
  • Histidine Kinase
  • Oxygen