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Quorum sensing: How Bacteria Talk to Each Other

Vikash Kumar*1, Suvra Roy1, Debtanu Barman2

1Central Institute of Fisheries Education, Mumbai, India, 400061. 2College of Fisheries, Central Agricultural University, Lembucherra, Tripura-799210, India.

*Corresponding author: kumar.vika.vikash2@gmail.com


Introduction

Quorum sensing (QS) is a cell-to-cell signaling mechanism that refers to the ability of bacteria to respond to chemical hormone-like molecules called autoinducers. When an autoinducer reaches a critical threshold, the bacteria detect and respond to this signal by altering their gene expression. Quorum sensing thus enables bacteria to co-ordinate and respond quickly to environmental changes, such as the availability of nutrients, other microbes or toxins in their environment.QS was first described in the regulation of bioluminescence in Vibrio fischeriand Vibrio harveyiand since then shown to be a widespread mechanism of gene regulation in bacteria. In this review, we will explore several QS systems used by bacteria; the LuxR/I-type systems, primarily used by Gram-negative bacteria, in which the signaling molecule is an acyl-homoserine lactone (AHL), the peptide signaling systems used primarily by Gram-positive bacteria, the luxS/AI-2 signaling used for interspecies communication, and the AI-3/epinephrine/ norepinephrine interkingdom signaling system.

Signal Molecules Involved in Quorum Sensing

Most quorum sensing signals are small organic molecules or peptides (Box 1). For example, gram-negative bacteria employ N-acyl homoserine lactones (AHLs), alkyl quinolones (AQs) and fatty acidmethyl esters. Gram-positive bacteria use peptides like the autoinducing peptides (AIPs). The streptomycetes synthesize butyrolactones such as A-factor. AHL-mediated quorum sensing is one of the best characterized cell-to-cell communication mechanisms. More than 70 bacterial species are known to produce AHL-type quorum-sensing signals, with many producing multiple AHLs.

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The LuxR/I signalingsystem

The LuxR/I system was the first one to be described in V. fischeri. The luciferase operon in V. fischeriis regulated by two proteins, LuxI, which is responsible for the production of the AHL autoinducer, and LuxR, which is activated by this autoinducer to increase transcription of the luciferase operon. Since this initial description, homologs of LuxR-LuxI have been identified in other bacteria, and in all of these LuxR-LuxI systems, the bacteria produce an AHL autoinducer, which binds to the LuxR protein and regulates the transcription of several genes involved in a variety of phenotypes. These include the production of antibiotics in Erwinia, motility in Yersinia pseudotuberculosis, and pathogenesis and biofilm formation in Pseudomonas aeruginosa, among others.


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Fig. 1.Model of bioluminescence activation in Vibrio fischeri by the LuxR/I quorum-sensing system. In high cell density, the acyl-homoserine lactone (AHL) autoinducer binds to LuxR. LuxR complexed with AHL then activates transcription of itself and the luciferase operon.


The LuxS/AI-2 signaling system

Vibrio harveyiis a marine bacterium that controls bioluminescence through QS. Vibrio harveyi QS system constitutes a mix between components of Gram-positive and Gram negative systems. It has two QS systems: system 1 in which the autoinducer (AI-1) is an AHL, and is primarily involved in intraspecies signaling; system 2, in which the autoinducer is a furanosyl borate diester involved in interspecies signaling. Vibrio harveyihas two hybrid sensor kinases, LuxN and LuxQ, which sense AI-1 and AI-2, respectively. In the absence of signal, these proteins are intrinsic kinases and phosphorylate a complex phosphorelay system, with LuxU and LuxO (an enhancer-binding protein) as intermediaries. Phospho-LuxO in conjunction with s54 then activates transcription of small regulatory RNAs, which destabilize the message of the LuxR protein, which in turn no longer can activate transcription of the luciferase operon. Upon interaction with their cognate autoinducers, these sensors behave as phosphatases and the system is dephosphorylated, allowing LuxR to activate bioluminescence.


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Fig. 2.The LuxS/AI-2 quorum-sensing system. (a) Vibrio harveyiuses two sensor kinases, LuxN and LuxQ, to recognize AI-1 and AI-2, respectively. (b) In Salmonella and Escherichia colithe AI-2 receptor is the LsrB periplasmic protein.


TheAI-3/epinephrine/norepinephrine signaling system

This QS system was first discovered by serendipity as being associated with the LuxS system. LuxS is not devoted solely to AI-2 production; it is in fact an enzyme involved in the activated methyl pathway which is involved in the synthesis of methionine and SAM. Consequently, altered gene expression because of a luxS mutation will involve genes affected by QS per se and genes differentially expressed because of the interruption of this metabolic pathway. A luxS mutant will accumulate S-ribosyl-homocysteine within the cell because it is unable to catalyze its conversion to homocysteine. This would cause the levels of homocysteine to diminish within the cell. Inasmuch as homocysteine is used for the de novo synthesis of methionine, the cell will use a salvage pathway. It will use oxaloacetate to produce homocysteine to synthesize methionine. Given that oxaloacetate and L-glutamate are necessary to synthesize aspartate, using this salvage pathway for the de novo synthesis of methionine, other amino acid synthetic and catabolic pathways will be changed within the cell. Changes in other amino acid metabolic processes are responsible for the lack of AI-3 activity in a luxS mutant. Structural analysis of AI-3 suggests that this signal is an aromatic compound and does not contain a sugar skeleton like AI-2.


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Fig. 3.Model of quorum sensing signaling in enterohemorrhagic Escherichia coli. Both AI-3 and epinephrine/norepinephrine seem to be recognized by the same receptor, which is probably in the outer membrane of the bacteria.


Quorum-Quenching Mechanisms

Conventional antibiotics kill or stop bacterial growth by interfering with essential housekeeping functions (e.g. DNA, RNA and protein synthesis), hence inevitably imposing selection pressure that results in the emergence of antibiotic-resistant microbial pathogens. The concerns about resistance not only call for better use and administration of conventional antibiotics, but also prompt scientists to look for new disease control strategies. At least in theory, any strategy that can effectively stop pathogenic infection, but does not impose a 'life-or-death' selection pressure, would be a promising alternative to contain infectious diseases and may help to prevent antibiotic resistance in microbial communities. One such promising strategy is the recently demonstrated quorum-quenching approach, also known as antipathogenic or signal interference, which abolishes bacterial infection by interfering with microbial cell-to-cell communication-also known as quorum sensing.


Conclusion

"Quorum sensing" (QS) relies on the activation of a sensor kinase or response regulator protein by, in many cases, a diffusible, low molecular weight signal molecule (a "pheromone" or "autoinducer"). In QS, the concentration of the signal molecule reflects the number of bacterial cells in a particular niche and perception of a threshold concentration of that signal molecule indicates that the population is "quorated" i.e. ready to make a behavioural decision. Bacteria cell-to-cell communication is perhaps the most important tool in the battle for survival; they employ communication to trigger transcriptional regulation resulting in sexual exchange and niche protection in some cases, to battle host' defences and coordinate population migration.


Reference

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  • Bassler BL, Wright M, Showalter RE & Silverman MR (1993) Intercellular signalling in Vibrio harveyi: sequence and function of genes regulating expression of luminescence. Mol Microbiol 9: 773-786.

  • Nicola C. Reading & Vanessa Sperandio. 2006. Quorum sensing: the many languages of bacteria. FEMS Microbiol. Lett., 254, 1-11.

  • Dong YH, Wang LH, Xu JL, Zhang HB, Zhang XF & Zhang LH (2001) Quenching quorum-sensing-dependent bacterial infection by an N-acyl homoserine lactonase. Nature 411: 813-817.

  • Elliott SJ, Wainwright LA, McDaniel TK, Jarvis KG, Deng YK, Lai LC, McNamara BP, Donnenberg MS & Kaper JB (1998) The complete sequence of the locus of enterocyte effacement (LEE) from enteropathogenic Escherichia coli E2348/69. Mol Microbiol 28: 1-4.

  • Winzer K, Hardie KR &Williams P (2002) Bacterial cell-to-cell communication: sorry, can't talk now - gone to lunch! Curr Opin Microbiol 5: 216-222.

  • Xavier KB & Bassler BL (2003) LuxS quorum sensing: more than just a numbers game. Curr Opin Microbiol 6: 191-197.

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