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Review
. 2016 Feb 10:7:131.
doi: 10.3389/fmicb.2016.00131. eCollection 2016.

Quorum Sensing: An Under-Explored Phenomenon in the Phylum Actinobacteria

Ashish V Polkade  1 , Shailesh S Mantri  1 , Umera J Patwekar  1 , Kamlesh Jangid  1
Affiliations
Review

Quorum Sensing: An Under-Explored Phenomenon in the Phylum Actinobacteria

Ashish V Polkade et al. Front Microbiol. .

Abstract

Quorum sensing is known to play a major role in the regulation of secondary metabolite production, especially, antibiotics, and morphogenesis in the phylum Actinobacteria. Although it is one of the largest bacterial phylum, only 25 of the 342 genera have been reported to use quorum sensing. Of these, only nine have accompanying experimental evidence; the rest are only known through bioinformatic analysis of gene/genome sequences. It is evident that this important communication mechanism is not extensively explored in Actinobacteria. In this review, we summarize the different quorum sensing systems while identifying the limitations of the existing screening strategies and addressing the improvements that have taken place in this field in recent years. The γ-butyrolactone system turned out to be almost exclusively limited to this phylum. In addition, methylenomycin furans, AI-2 and other putative AHL-like signaling molecules are also reported in Actinobacteria. The lack of existing screening systems in detecting minute quantities and of a wider range of signaling molecules was a major reason behind the limited information available on quorum sensing in this phylum. However, recent improvements in screening strategies hold a promising future and are likely to increase the discovery of new signaling molecules. Further, the quorum quenching ability in many Actinobacteria has a great potential in controlling the spread of plant and animal pathogens. A systematic and coordinated effort is required to screen and exploit the enormous potential that quorum sensing in the phylum Actinobacteria has to offer for human benefit.

Keywords: Actinobacteria; GBL; MMFs; Mycobacterium; Streptomyces; c-di-GMP; quorum quenching; quorum sensing.

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Figures

FIGURE 1
FIGURE 1
Schematics of quorum sensing systems in bacteria. (A) Gram-negative bacteria: at threshold concentrations the diffusible autoinducer signaling molecule, typically a homoserine lactone, binds to its cognate receptor inside the cell forming the autoinducer-receptor complex which then regulates the expression of target genes through its binding to the target promoter; and (B) Gram-positive bacteria: at threshold concentrations the autoinducer peptide molecule which is actively transported activates the sensor kinase protein inside the cell which phosphorylates the response regulator protein, which then regulates the expression of target genes through its binding to the target promoter. Adapted from Koh et al. (2013).
FIGURE 2
FIGURE 2
16S rRNA gene sequence based family tree of the phylum Actinobacteria depicting the genera with known quorum sensing systems. The evolutionary history was inferred using the Neighbor–Joining method (Saitou and Nei, 1987) using the bootstrap test of phylogeny (1000 replicates) (Felsenstein, 1985). The evolutionary distances were computed using the Kimura 2-parameter method (Kimura, 1980) Evolutionary analyses were conducted in MEGA6 (Tamura et al., 2013). A total of 54 sequences were used for constructing the tree and belonged to the type species of the type genera of each family as described in Ludwig et al. (2012) and are submitted as Supplementary Data in fasta format. Black color branch denotes family with no evidence of quorum sensing; red color denotes family with experimental evidence of quorum sensing; green color denotes family for which only gene homologs are known; ‘∗’ indicates genus for which only gene homologs are known; and ‘∗∗’ denotes genus for which putative AHL-like signal molecules are involved in quorum sensing.
FIGURE 3
FIGURE 3
Structures of representative signaling molecules in Actinobacteria. The A-factor of Streptomyces griseus, the GBLs of S. coelicolor (SCB1, SCB2, and SCB3), MMFs of S. coelicolor which are structurally distinct sharing a common 2-alkyl-4-hydroxymethylfuran-3-carboxylic acid core structure but differ in the identity of the C2 alkyl group. The C4-homoserine lactone of Pseudomonas aeruginosa is shown for comparison. Adapted from Willey and Gaskell (2011).
FIGURE 4
FIGURE 4
The S. griseus A-factor regulon. Similar to Gram-negative bacteria, at threshold concentrations the diffusible A-factor (a γ-butyrolactone) binds the intracellular receptor ArpA and activates expression of the transcriptional activator AdpA which in-turn regulates multiple phenotypes either indirectly via a multi-step cascade, such as the development of aerial hyphae and sporulation, or directly, such as the production of secondary metabolites like streptomycin.
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