Lack of genomic evidence of AI-2 receptors suggests a non-quorum sensing role for luxS in most bacteria

BMC Microbiol. 2008 Sep 20;8:154. doi: 10.1186/1471-2180-8-154.

Abstract

Background: Great excitement accompanied discoveries over the last decade in several Gram-negative and Gram-positive bacteria of the LuxS protein, which catalyzes production of the AI-2 autoinducer molecule for a second quorum sensing system (QS-2). Since the luxS gene was found to be widespread among the most diverse bacterial taxa, it was hypothesized that AI-2 may constitute the basis of a universal microbial language, a kind of bacterial Esperanto. Many of the studies published in this field have drawn a direct correlation between the occurrence of the luxS gene in a given organism and the presence and functionality of a QS-2 therein. However, rarely hathe existence of potential AI-2 receptors been examined. This is important, since it is now well recognized that LuxS also holds a central role as a metabolic enzyme in the activated methyl cycle which is responsible for the generation of S-adenosyl-L-methionine, the major methyl donor in the cell.

Results: In order to assess whether the role of LuxS in these bacteria is indeed related to AI-2 mediated quorum sensing we analyzed genomic databases searching for established AI-2 receptors (i.e., LuxPQ-receptor of Vibrio harveyi and Lsr ABC-transporter of Salmonella typhimurium) and other presumed QS-related proteins and compared the outcome with published results about the role of QS-2 in these organisms. An unequivocal AI-2 related behavior was restricted primarily to organisms bearing known AI-2 receptor genes, while phenotypes of luxS mutant bacteria lacking these genes could often be explained simply by assuming deficiencies in sulfur metabolism.

Conclusion: Genomic analysis shows that while LuxPQ is restricted to Vibrionales, the Lsr-receptor complex is mainly present in pathogenic bacteria associated with endotherms. This suggests that QS-2 may play an important role in interactions with animal hosts. In most other species, however, the role of LuxS appears to be limited to metabolism, although in a few cases the presence of yet unknown receptors or the adaptation of pre-existent effectors to QS-2 must be postulated.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Bacteria / classification
  • Bacteria / genetics*
  • Bacteria / metabolism
  • Bacterial Proteins / genetics*
  • Bacterial Proteins / metabolism
  • Carbon-Sulfur Lyases / genetics
  • Carbon-Sulfur Lyases / metabolism*
  • Genome, Bacterial*
  • Homoserine / analogs & derivatives*
  • Homoserine / metabolism
  • Lactones / metabolism*
  • Molecular Sequence Data
  • Phylogeny
  • Quorum Sensing*

Substances

  • Bacterial Proteins
  • Lactones
  • N-octanoylhomoserine lactone
  • Homoserine
  • Carbon-Sulfur Lyases
  • LuxS protein, Bacteria