Potential for luxS related signaling in marine bacteria and production of autoinducer-2 in the genus Shewanella

Helmholtz-Center for Infection Research, Group Microbial Communication, Division of Cell Biology, Inhoffenstr, 7, 38124 Braunschweig, Germany.
BMC Microbiology (Impact Factor: 2.73). 02/2008; 8(1):13. DOI: 10.1186/1471-2180-8-13
Source: PubMed


The autoinducer-2 (AI-2) group of signalling molecules are produced by both Gram positive and Gram negative bacteria as the by-product of a metabolic transformation carried out by the LuxS enzyme. They are the only non species-specific quorum sensing compounds presently known in bacteria. The luxS gene coding for the AI-2 synthase enzyme was found in many important pathogens. Here, we surveyed its occurrence in a collection of 165 marine isolates belonging to abundant marine phyla using conserved degenerated PCR primers and sequencing of selected positive bands to determine if the presence of the luxS gene is phylogenetically conserved or dependent on the habitat.
The luxS gene was not present in any of the Alphaproteobacteria (n = 71) and Bacteroidetes strains (n = 29) tested; by contrast, these bacteria harboured the sahH gene, coding for an alternative enzyme for the detoxification of S-adenosylhomocysteine (SAH) in the activated methyl cycle. Within the Gammaproteobacteria (n = 76), luxS was found in all Shewanella, Vibrio and Alteromonas isolates and some Pseudoalteromonas and Halomonas species, while sahH was detected in Psychrobacter strains. A number of Gammaproteobacteria (n = 27) appeared to have neither the luxS nor the sahH gene. We then studied the production of AI-2 in the genus Shewanella using the Vibrio harveyi bioassay. All ten species of Shewanella tested produced a pronounced peak of AI-2 towards the end of the exponential growth phase in several media investigated. The maximum of AI-2 activity was different in each Shewanella species, ranging from 4% to 46% of the positive control.
The data are consistent with those of fully sequenced bacterial genomes and show that the potential for luxS related signalling is dependent on phylogenetic affiliation rather than ecological niche and is largest in certain groups of Gammaproteobacteria in the marine environment. This is the first report on AI-2 production in Shewanella species; its signalling role in these organisms remains to be elucidated.

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    • "One hypothesis to explain this observation is that cells might form aggregates at high cell concentration that are more resistant to pressure than cells alone (Furukawa et al., 2002). The presence of quorum sensing in Shewanella has been suggested by the presence of signaling molecules in several Shewanella species, including marine species and strain MR-1 (Bodor et al., 2008). In Sp LT13a, high CFU concentrations could induce changes in the metabolic state of cells, for example by channeling most energy produced via Fe(III) reduction to cell-maintenancerelated processes, as opposed to growth. "
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    ABSTRACT: Microorganisms influence biogeochemical cycles from the surface down to the depths of the continental rocks and oceanic basaltic crust. Due to the poor recovery of microbial isolates from the deep subsurface, the influence of physical environmental parameters, such as pressure and temperature, on the physiology and metabolic potential of subsurface inhabitants is not well constrained. We evaluated Fe(III) reduction rates (FeRRs) and viability, measured as colony-forming ability, of the deep-sea piezophilic bacterium Shewanella profunda LT13a over a range of pressures (0–125 MPa) and temperatures (4–37∘C) that included the in situ habitat of the bacterium isolated from deep-sea sediments at 4500 m depth below sea level. S. profunda LT13a was active at all temperatures investigated and at pressures up to 120 MPa at 30∘C, suggesting that it is well adapted to deep-sea and deep sedimentary environments. Average initial cellular FeRRs only slightly decreased with increasing pressure until activity stopped, suggesting that the respiratory chain was not immediately affected upon the application of pressure. We hypothesize that, as pressure increases, the increased energy demand for cell maintenance is not fulfilled, thus leading to a decrease in viability. This study opens up perspectives about energy requirements of cells in the deep subsurface.
    Full-text · Article · Jan 2015 · Frontiers in Microbiology
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    • "These results indicate that the SSO are able to produce AI-2. The production of AI-2 in Shewanella has been previously reported by Bodor et al. (2008). When the ethyl acetate extract from SA02 was analyzed by GC–MS, one peak was identified as cyclo-(L-Pro-L-Leu) (Fig. 3c and d), while no DKPs were identified in the ethyl acetate extracts from SS01 and the negative control (data not shown). "
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    ABSTRACT: Quorum-sensing signals in refrigerated shrimp (Litopenaeus vannamei) undergoing spoilage were examined using bioreporter assays, thin-layer chromatography and gas chromatography–mass spectrometry, and the results revealed the presence of three types of autoinducers including acetylated homoserine lactones (AHLs) (i.e., N-hexanoyl-homoserine lactone, N-oxohexanoyl-homoserine lactone and N-octanoyl-homoserine lactone), autoinducer-2, and cyclic dipeptides (i.e., cyclo-(l-Pro-l-Leu), cyclo-(l-Leu-l-Leu) and cyclo-(l-Pro-l-Phe)). Autoinducer-2, rather than any AHL, was detected in extracts from pure cultures of the specific spoilage organisms (SSO), i.e., Shewanella putrefaciens (SS01) and Shewanella baltica (SA02). As for the cyclic peptides, only SA02 was determined to produce cyclo-(l-Pro-l-Leu). According to the transcription levels of LuxR (the master quorum-sensing regulator) in the SSO in response to exogenous autoinducers, the SSO could sense AHLs and cyclo-(l-Leu-l-Leu), rather than autoinducer-2, cyclo-(l-Leu-l-Leu) and cyclo-(l-Pro-l-Phe). In accordance with the results of LuxR expression, the production of biofilm matrixes and extracellular proteases in the SSO was regulated by exogenous AHLs and cyclo-(l-Pro-l-Leu), rather than 4,5-dihydroxy-2,3-pentanedione (the autoinducer-2 precursor), cyclo-(l-Leu-l-Leu) and cyclo-(l-Pro-l-Phe). Exogenous N-hexanoyl-homoserine lactone and cyclo-(l-Pro-l-Leu) increased the growth rates and population percentages of the SSO in shrimp samples under refrigerated storage, and interestingly, exogenous 4,5-dihydroxy-2,3-pentanedione also increased the population percentages of the SSO in vivo by inhibiting the growth of the competing bacteria. However, according to the levels of TVB-N and the volatile organic components in the shrimp samples, exogenous 4,5-dihydroxy-2,3-pentanedione did not accelerate the shrimp spoilage process as N-hexanoyl-homoserine lactone and cyclo-(l-Pro-l-Leu) did. In summary, our results suggest that quorum sensing involves the spoilage of refrigerated Litopenaeus vannamei.
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    • "The most investigated characteristic of S. oneidensis is its ability to use a broad spectrum of electron acceptors [3]. In our previous study, Shewanella species were shown to produce autoinducer-2, proposed to be a universal signal molecule in bacteria [4], and to contain its synthesis gene, luxS [5]. As S. oneidensis readily forms biofilms and lives in bacterial communities and since AI-2 is the product of the widely distributed luxS enzyme, AI-2 signalling would represent a possibility for this species to react to the bacterial density in its environment. "
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    ABSTRACT: The luxS gene in Shewanella oneidensis was shown to encode an autoinducer-2 (AI-2)-like molecule, the postulated universal bacterial signal, but the impaired biofilm growth of a luxS deficient mutant could not be restored by AI-2, indicating it might not have a signalling role in this organism. Here, we provide further evidence regarding the metabolic role of a luxS mutation in S. oneidensis. We constructed a luxS mutant and compared its phenotype to a wild type control with respect to its ability to remove AI-2 from the medium, expression of secreted proteins and biofilm formation. We show that S. oneidensis has a cell-dependent mechanism by which AI-2 is depleted from the medium by uptake or degradation at the end of the exponential growth phase. As AI-2 depletion is equally active in the luxS mutant and thus does not require AI-2 as an inducer, it appears to be an unspecific mechanism suggesting that AI-2 for S. oneidensis is a metabolite which is imported under nutrient limitation. Secreted proteins were studied by iTraq labelling and liquid chromatography mass spectrometry (LC-MS) detection. Differences between wild type and mutant were small. Proteins related to flagellar and twitching motility were slightly up-regulated in the luxS mutant, in accordance with its loose biofilm structure. An enzyme related to cysteine metabolism was also up-regulated, probably compensating for the lack of the LuxS enzyme. The luxS mutant developed an undifferentiated, loosely-connected biofilm which covered the glass surface more homogenously than the wild type control, which formed compact aggregates with large voids in between. The data confirm the role of the LuxS enzyme for biofilm growth in S. oneidensis and make it unlikely that AI-2 has a signalling role in this organism.
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