A complex LuxR–LuxI type quorum sensing network in a roseobacterial marine sponge symbiont activates flagellar motility and inhibits biofilm formation

Zan, Jindong; Cicirelli, Elisha M.; Mohamed, Naglaa M.; Sibhatu, Hiruy M.; Kroll, Stephanie; Choi, Okhee; Uhlson, Charis L.; Wysoczynski, Christina L.; Murphy, Robert C.; Churchill, Mair E. A.; Hill, Russell T.; Fuqua, Clay

doi:10.1111/j.1365-2958.2012.08149.x

Cited by 71 publications

(93 citation statements)

References 72 publications

(130 reference statements)

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“…While roseobacters are known to produce long-chain AHLs with various degrees of oxidation and side-chain saturation (11,30,34,35,46), the full complement of AHLs synthesized by lineage members and the contribution of these chemical signals to roseobacter ecology are not yet known. Here we identified a novel AHL, 3OHC 12:1 -HSL, in Phaeobacter sp.…”

Section: Discussionmentioning

confidence: 99%

“…Similar phenotypes have been reported in another roseobacter, Ruegeria sp. strain KLH11; it has been suggested that quorum sensing may control the lifestyle switch between the sessile (biofilm) and planktonic forms of that strain (35,60). An analogous cell-to-cell communication may be used to induce dispersion of Phaeobacter sp.…”

Section: Discussionmentioning

confidence: 99%

“…Examples of physiolo-aquatic bacteria (28,29). Representative members of the Roseobacter clade have been shown to produce multiple AHLs, and these compounds have been linked to biofilm formation, motility, and antimicrobial production in a limited number of strains (30)(31)(32)(33)(34)(35)(36). Relatively few Roseobacter AHLs have been linked to the LuxI homologs that mediate their syntheses, and many roseobacters possess multiple luxRI systems, suggesting the presence of complex AHL-mediated regulatory schemes in these strains that have not been explored (36).…”

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confidence: 99%

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Phaeobacter sp. Strain Y4I Utilizes Two Separate Cell-to-Cell Communication Systems To Regulate Production of the Antimicrobial Indigoidine

Cude

Prevatte

Hadden

et al. 2015

Appl Environ Microbiol

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The marine roseobacter Phaeobacter sp. strain Y4I synthesizes the blue antimicrobial secondary metabolite indigoidine when grown in a biofilm or on agar plates. Prior studies suggested that indigoidine production may be, in part, regulated by cell-to-cell communication systems. Phaeobacter sp. strain Y4I possesses two luxR and luxI homologous N-acyl-L-homoserine lactone (AHL)-mediated cell-to-cell communication systems, designated pgaRI and phaRI. We show here that Y4I produces two dominant AHLs, the novel monounsaturated N-(3-hydroxydodecenoyl)-L-homoserine lactone (3OHC 12:1 -HSL) and the relatively common N-octanoyl-L-homoserine lactone (C 8 -HSL), and provide evidence that they are synthesized by PhaI and PgaI, respectively. A Tn5 insertional mutation in either genetic locus results in the abolishment (pgaR::Tn5) or reduction (phaR::Tn5) of pigment production. Motility defects and denser biofilms were also observed in these mutant backgrounds, suggesting an overlap in the functional roles of these systems. Production of the AHLs occurs at distinct points during growth on an agar surface and was determined by isotope dilution high-performance liquid chromatography-tandem mass spectrometry (ID-HPLC-MS/MS) analysis. Within 2 h of surface inoculation, only 3OHC 12:1 -HSL was detected in agar extracts. As surface-attached cells became established (at ϳ10 h), the concentration of 3OHC 12:1 -HSL decreased, and the concentration of C 8 -HSL increased rapidly over 14 h. After longer (>24-h) establishment periods, the concentrations of the two AHLs increased to and stabilized at ϳ15 nM and ϳ600 nM for 3OHC 12:1 -HSL and C 8 -HSL, respectively. In contrast, the total amount of indigoidine increased steadily from undetectable to 642 M by 48 h. Gene expression profiles of the AHL and indigoidine synthases (pgaI, phaI, and igiD) were consistent with their metabolite profiles. These data provide evidence that pgaRI and phaRI play overlapping roles in the regulation of indigoidine biosynthesis, and it is postulated that this allows Phaeobacter sp. strain Y4I to coordinate production of indigoidine with different growth-phase-dependent physiologies. Bacteria are in constant competition for niches in the environment, and the ability to coordinate gene expression may provide a competitive advantage (1). Some bacteria are able to synchronize gene expression in a cell-density-dependent manner by sensing and responding to small diffusible molecules synthesized by individuals; in proteobacteria, members of the broadly distributed and chemically diverse class of N-acyl-L-homoserine lactones (AHLs) are among the best-characterized signaling molecules (2). Proteobacterial AHL synthases are fairly well conserved and form the LuxI protein family. Members of the LuxR protein family are cytoplasmic transcriptional regulators that can modulate gene expression, most typically when bound to the corresponding cognate AHL (3-7). It has been shown that luxI-luxR (luxIR) pairs are frequently colocalized within chromosomes and constitutively exp...

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

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Phaeobacter sp. Strain Y4I Utilizes Two Separate Cell-to-Cell Communication Systems To Regulate Production of the Antimicrobial Indigoidine

Cude

Prevatte

Hadden

et al. 2015

Appl Environ Microbiol

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“…are also known to possess multiple systems and signals ( Table 2). The QS signals modulating these QSS range from unsubstituted-to substituted-HSLs, as well as peptides (DKPs), quinolones, hormones [69,[94][95][96][97][98][99][100][101][102][103][104][105]. In Yersinia, luxI/R homologues are majorly regulated by substituted AHLs [106][107][108].…”

Section: Othersmentioning

confidence: 99%

Potential Emergence of Multi-quorum Sensing Inhibitor Resistant (MQSIR) Bacteria

et al. 2015

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Expression of certain bacterial genes only at a high bacterial cell density is termed as quorum-sensing (QS). Here bacteria use signaling molecules to communicate among themselves. QS mediated genes are generally involved in the expression of phenotypes such as bioluminescence, biofilm formation, competence, nodulation, and virulence. QS systems (QSS) vary from a single in Vibrio spp. to multiple in Pseudomonas and Sinorhizobium species. The complexity of QSS is further enhanced by the multiplicity of signals: (1) peptides, (2) acyl-homoserine lactones, (3) diketopiperazines. To counteract this pathogenic behaviour, a wide range of bioactive molecules acting as QS inhibitors (QSIs) have been elucidated. Unlike antibiotics, QSIs don't kill bacteria and act at much lower concentration than those of antibiotics. Bacterial ability to evolve resistance against multiple drugs has cautioned researchers to develop QSIs which may not generate undue pressure on bacteria to develop resistance against them. In this paper, we have discussed the implications of the diversity and multiplicity of QSS, in acting as an arsenal to withstand attack from QSIs and may use these as reservoirs to develop multi-QSI resistance.

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“…Not all AHL synthases belong to the LuxI family proteins; AHLs can also be synthesized by LuxM-and AinS-type proteins (11). QS systems can regulate a variety of cellular processes that are beneficial to a bacterial community, such as motility, sporulation, production of virulence factors and secondary metabolites, plasmid transfer, and biofilm formation (11), and they can facilitate the colonization of desirable niches (13).Bacteria with AHL-QS systems have been isolated from marine sponges (for examples, see references 7 and 14), and signaling molecules able to activate AHL biosensors have been reported in sponge extracts (7,14,15); the chemical nature of most of these signaling compounds is currently unknown. Gardères et al (16) identified AHLs produced in vivo by symbionts of the Celtic Sea sponge Suberites domuncula; more recently, it was determined that the signal molecule produced, N-3-oxododecanoyl-L-homoserine lactone, affects the expression of immune and apoptotic genes of the host sponge S. domuncula, possibly enabling the …”

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confidence: 99%

A NewN-Acyl Homoserine Lactone Synthase in an Uncultured Symbiont of the Red Sea Sponge Theonella swinhoei

Britstein

Devescovi

Handley

et al. 2016

Appl Environ Microbiol

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i Sponges harbor a remarkable diversity of microbial symbionts in which signal molecules can accumulate and enable cell-cell communication, such as quorum sensing (QS). Bacteria capable of QS were isolated from marine sponges; however, an extremely small fraction of the sponge microbiome is amenable to cultivation. We took advantage of community genome assembly and binning to investigate the uncultured majority of sponge symbionts. We identified a complete N-acyl-homoserine lactone (AHL)-QS system (designated TswIR) and seven partial luxI homologues in the microbiome of Theonella swinhoei. The TswIR system was novel and shown to be associated with an alphaproteobacterium of the order Rhodobacterales, here termed Rhodobacterales bacterium TS309. The tswI gene, when expressed in Escherichia coli, produced three AHLs, two of which were also identified in a T. swinhoei sponge extract. The taxonomic affiliation of the 16S rRNA of Rhodobacterales bacterium TS309 to a sponge-coral specific clade, its enrichment in sponge versus seawater and marine sediment samples, and the presence of spongespecific features, such as ankyrin-like domains and tetratricopeptide repeats, indicate a likely symbiotic nature of this bacterium. Symbiosis between metazoans and microbes exists in virtually every environment, including in marine sponges (phylum Porifera) (1). Marine sponges are important members of shallow and deep reef communities and are a rich source of secondary metabolites with pharmaceutical potential, and these metabolites are often produced by the sponges' microbial symbionts (2, 3). These host-associated bacteria are sponge specific and can comprise up to 35% of the sponge volume (4), spanning at least 47 bacterial phyla (5).In recent years, symbioses between microorganisms and eukaryotic hosts have received growing attention. The host, together with all its symbionts, is now seen as a single entity designated the holobiont, defined as the sum of the genetic information of the host and its microbiota (6). Sponge holobionts provide an enclosed niche in which extensive interactions among dense and diverse microbial populations are accomplished (7). The mechanisms underlying cell-cell interactions among bacteria within the sponge and the genetic regulation systems controlling gene expression in sponge symbionts are largely unknown. One of the best understood microbial quorum-sensing (QS) systems is the one that uses N-acyl-homoserine lactones (AHLs) as signals (e.g., 8-10). QS enables bacteria to regulate their gene expression in a population density-dependent manner. At a low cell density, low levels of AHLs, which diffuse in and out of the bacterial cell, are present. As the bacterial density increases, especially for bacteria enclosed in niches, AHLs accumulate, and once they reach a critical level (quorum), they interact with LuxR cognate receptor proteins, which then affect target gene expression (11). A canonical AHL-QS system produces AHLs via the LuxI family AHL synthase protein and responds to them via the LuxR co...

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A complex LuxR–LuxI type quorum sensing network in a roseobacterial marine sponge symbiont activates flagellar motility and inhibits biofilm formation

Cited by 71 publications

References 72 publications

Phaeobacter sp. Strain Y4I Utilizes Two Separate Cell-to-Cell Communication Systems To Regulate Production of the Antimicrobial Indigoidine

Phaeobacter sp. Strain Y4I Utilizes Two Separate Cell-to-Cell Communication Systems To Regulate Production of the Antimicrobial Indigoidine

Potential Emergence of Multi-quorum Sensing Inhibitor Resistant (MQSIR) Bacteria

A NewN-Acyl Homoserine Lactone Synthase in an Uncultured Symbiont of the Red Sea Sponge Theonella swinhoei

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