Interspecies Chemical Signaling in a Methane-Oxidizing Bacterial Community

Appl Environ Microbiol. 2019 Mar 22;85(7):e02702-18. doi: 10.1128/AEM.02702-18. Print 2019 Apr 1.

Abstract

Multiple species of bacteria oxidize methane in the environment after it is produced by anaerobic ecosystems. These organisms provide reduced carbon substrates for species that cannot oxidize methane themselves, thereby serving a key role in these niches while also sequestering this potent greenhouse gas before it enters the atmosphere. Deciphering the molecular details of how methane-oxidizing bacteria interact in the environment enables us to understand an important aspect that shapes the structures and functions of these communities. Here we show that many members of the Methylomonas genus possess a LuxR-type acyl-homoserine lactone (acyl-HSL) receptor/transcription factor that is highly homologous to MbaR from the quorum-sensing (QS) system of Methylobacter tundripaludum, another methane oxidizer that has been isolated from the same environment. We reconstitute this detection system in Escherichia coli and use mutant and transcriptomic analysis to show that the receptor/transcription factor from Methylomonas sp. strain LW13 is active and alters LW13 gene expression in response to the acyl-HSL produced by M. tundripaludum These findings provide a molecular mechanism for how two species of bacteria that may compete for resources in the environment can interact in a specific manner through a chemical signal.IMPORTANCE Methanotrophs are bacteria that sequester methane, a significant greenhouse gas, and thereby perform an important ecosystem function. Understanding the mechanisms by which these organisms interact in the environment may ultimately allow us to manipulate and to optimize this activity. Here we show that members of a genus of methane-oxidizing bacteria can be influenced by a chemical signal produced by a possibly competing species. This provides insight into how gene expression can be controlled in these bacterial communities via an exogenous chemical signal.

Keywords: LuxR solo; acyl-homoserine lactone; methane; methanotroph; orphan LuxR; quorum sensing; sociomicrobiology.

Publication types

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

MeSH terms

  • 4-Butyrolactone / analogs & derivatives
  • 4-Butyrolactone / metabolism
  • Bacterial Proteins / genetics
  • Binding Sites
  • Ecosystem
  • Escherichia coli / metabolism
  • Gene Expression Regulation, Bacterial
  • Genome, Bacterial
  • Methane / metabolism*
  • Methylococcaceae / genetics
  • Methylococcaceae / metabolism*
  • Methylomonas / genetics
  • Methylomonas / metabolism
  • Microbiota / genetics
  • Microbiota / physiology*
  • Oxidation-Reduction
  • Quorum Sensing / physiology
  • Repressor Proteins
  • Signal Transduction* / genetics
  • Trans-Activators
  • Transcription Factors / genetics
  • Transcriptome

Substances

  • Bacterial Proteins
  • Repressor Proteins
  • Trans-Activators
  • Transcription Factors
  • LuxR autoinducer binding proteins
  • homoserine lactone
  • 4-Butyrolactone
  • Methane