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Review
. 2008 Feb;6(2):111-20.
doi: 10.1038/nrmicro1836.

Inter-kingdom signalling: communication between bacteria and their hosts

David T Hughes  1 , Vanessa Sperandio
Affiliations
Review

Inter-kingdom signalling: communication between bacteria and their hosts

David T Hughes et al. Nat Rev Microbiol. 2008 Feb.

Abstract

Microorganisms and their hosts communicate with each other through an array of hormonal signals. This cross-kingdom cell-to-cell signalling involves small molecules, such as hormones that are produced by eukaryotes and hormone-like chemicals that are produced by bacteria. Cell-to-cell signalling between bacteria, usually referred to as quorum sensing, was initially described as a means by which bacteria achieve signalling in microbial communities to coordinate gene expression within a population. Recent evidence shows, however, that quorum-sensing signalling is not restricted to bacterial cell-to-cell communication, but also allows communication between microorganisms and their hosts.

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Figures

Figure 1
Figure 1. Chemical structures of bacterial and host signals
The bacterial signal autoinducer (AI)-3 is an aromatic aminated signal; its final structure is still unknown. Because AI-3 is, to a certain degree, hydrophobic, it is not thought to be able to cross the cell membrane. The bacterial signal acyl homoserine lactone (AHL) is composed of a conserved homoserine ring and a variable acyl chain, and usually can cross the cell membrane. The host hormones adrenaline and noradrenaline are cathecolamines that are synthesized from tyrosine and usually do not cross the cell membrane. The host signals progesterone and cholesterol are two examples of lipid host hormones that can cross the cell membrane and bind intracellular receptors.
Figure 2
Figure 2. Mammalian signalling through membrane Receptors
a | Membrane receptor kinases dimerize and autophosphorylate a tyrosine or threonine residue upon binding to a hormone. They then initiate a phosphorelay signalling cascade in the cell. These cascades can include the mitogen-activated protein kinase (MAPK), Akt and Jun amino-terminal-kinase (JNK) pathways, and often lead to DNA synthesis and cell proliferation. b | G-protein-coupled receptors (GPCRs) are receptors that are coupled to guanine-binding proteins (G proteins) when they are inactive. G proteins consist of an α-, a β- and a γ-subunit. If a GPCR binds its signal (such as adrenaline or noradrenaline (NA)), the α-subunit of the G protein is uncoupled and exerts its effect. Different families of the α-subunit associate with different effectors and exert different effects. The αi inhibits adenylate cyclase and diminishes the levels of intracellular cyclic AMP (cAMP), the αs activates adenylate cyclase to increase the levels of cAMP and the αqactivates phospholipase C (PLC).
Figure 3
Figure 3. Adrenergic sensing in enterohaemorrhagic Escherichia coli
Autoinducer (AI)-3, adrenaline and noradrenaline (NA) bind the bacterial membrane receptor QseC, which results in its autophosphorylation. QseC then phosphorylates its response regulator QseB and initiates a complex phosphorelay signalling cascade that activates the expression of a second two-component system (QseEF), the locus of enterocyte effacement (LEE) genes (which encode various proteins, including the components of a type III section system that are involved in attaching and effacing (AE) lesion formation), the motility genes (flhDC) and Shiga toxin (stxAB). The QseEF two-component system is also involved in the expression of the LEE genes, and although its activators have not yet been elucidated, it is possible that it senses adrenaline and/or NA.
Figure 4
Figure 4. AHL inter-kingdom signaling
In bacteria, acyl homoserine lactones (AHLs) cross the cell membrane and interact with cytoplasmic receptors of the LuxR family. Binding the AHL to the LuxR-type receptor allows proper folding of this protein, which allows the receptor to dimerize and bind to its target sequence on DNA to regulate gene expression. In the absence of signal, LuxR-type proteins misfold and are targeted for degradation. In mammalian cells, AHLs also gain access to the cytoplasm by crossing the plasma membrane. The identity of the mammalian receptor (or receptors) for AHLs in mammalian cells is unknown. However, if there are intracellular receptors, it is proposed that the interaction with the AHL ligand activates these receptors and thereby allows their transportation into the nucleus, where they could control gene expression.
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