<i>Methylobacterium extorquens</i> AM1 produces a novel type of acyl‐homoserine lactone with a double unsaturated side chain under methylotrophic growth conditions

Nieto-Peñalver, Carlos Gabriel; Morin, Danièle; Cantet, Franck; Saurel, Olivier; Milon, Alain; Vorholt, Julia A.

doi:10.1016/j.febslet.2005.12.062

Cited by 38 publications

(50 citation statements)

References 29 publications

(55 reference statements)

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“…common tool in the analysis of AHLs from biological samples (Morin et al, 2003;Nieto Penalver et al, 2006); however, our results suggest that this type of instrument may not be the most appropriate tool for the comprehensive analysis of AHLs from extremely complex matrices.…”

Section: Discussioncontrasting

confidence: 40%

Microbial interactions associated with biofilms attached to Trichodesmium spp. and detrital particles in the ocean

Hmelo¹

2010

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Quorum sensing (QS) via acylated homoserine lactones (AHLs) was discovered in the ocean, yet little is known about its role in the ocean beyond its involvement in certain symbiotic interactions. The objectives of this thesis were to constrain the chemical stability of AHLs in seawater, explore the production of AHLs in marine particulate environments, and probe selected behaviors which might be controlled by AHL-QS. I established that AHLs are more stable in seawater than previously expected and are likely to accumulate within biofilms. Based on this result, I chose to study AHL-QS in the bacterial communities inhabiting biofilms attached to Trichodesmium spp. and detrital (photosynthetically-derived sinking particulate organic carbon, POC) particles. These hot spots of microbial activity are primary sites of interaction between marine primary producers and heterotrophs and crucial components of the biological pump.Biofilm communities associated with Trichodesmium thiebautii colonies in the Sargasso Sea differed considerably from seawater microbial communities. In addition, there was no overlap between the communities associated with tuft and puff colonies. These results suggest that bacterial communities associated with Trichodesmium are not random; rather, Trichodesmium selects for specific microbial flora. Novel 16S rRNA gene sequences are present both in clone libraries constructed from DNA extracted from colonies of Trichodesmium spp. and in culture collections derived from wild and laboratory cultivated Trichodesmium spp., supporting the idea that the phycosphere of Trichodesmium is a unique microenvironment.Using high performance liquid chromatography-mass spectrometry, I demonstrated that bacteria isolated from Trichodesmium synthesize AHLs. In addition, I detected AHLs in sinking particles collected from a site off of Vancouver Island, Canada. AHLs were subsequently added to laboratory cultures of non-axenic Trichodesmium colonies and sinking POC samples. This is the first time AHLs have been detected in POC and indicates that AHL-QS was occurring in POC. Further, I showed that AHLs enhanced certain organic-matter degrading hydrolytic enzyme activities. My results suggest that AHL-QS is a factor regulating biogeochemically relevant enzyme activities on sinking POC and within the biofilms attached to Trichodesmium colonies and thereby may impact the timing and magnitude of biogeochemical fluxes in the ocean.

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Section: Discussioncontrasting

confidence: 40%

Microbial interactions associated with biofilms attached to Trichodesmium spp. and detrital particles in the ocean

Hmelo¹

2010

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“…1A). Clade 1 includes NwiI as well as two putative autoinducer synthases from the closely related N. hamburgensis, several uncharacterized autoinducer synthase genes from different R. palustris strains (only strain HaA2 shown), and a synthase from Methylobacterium extorquens (41)(42)(43)(44). Clade 1 has few other distinguishing features besides that M. extorquens produces unsaturated acyl-HSLs (41).…”

Section: Characterization Of Autoinducer Synthase and Receptor Homolomentioning

confidence: 99%

Nitrite-Oxidizing Bacterium Nitrobacter winogradskyi Produces N -Acyl-Homoserine Lactone Autoinducers

Mellbye

Bottomley

Sayavedra-Soto

2015

Appl Environ Microbiol

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bNitrobacter winogradskyi is a chemolithotrophic bacterium that plays a role in the nitrogen cycle by oxidizing nitrite to nitrate. Here, we demonstrate a functional N-acyl-homoserine lactone (acyl-HSL) synthase in this bacterium. The N. winogradskyi genome contains genes encoding a putative acyl-HSL autoinducer synthase (nwi0626, nwiI) and a putative acyl-HSL autoinducer receptor (nwi0627, nwiR) with amino acid sequences 38 to 78% identical to those in Rhodopseudomonas palustris and other Rhizobiales. Expression of nwiI and nwiR correlated with acyl-HSL production during culture. N. winogradskyi produces two distinct acyl-HSLs, N-decanoyl-L-homoserine lactone (C 10 -HSL) and a monounsaturated acyl-HSL (C 10:1 -HSL), in a cell-densityand growth phase-dependent manner, during batch and chemostat culture. The acyl-HSLs were detected by bioassay and identified by ultraperformance liquid chromatography with information-dependent acquisition mass spectrometry (UPLC-IDA-MS). The C‫؍‬C bond in C 10:1 -HSL was confirmed by conversion into bromohydrin and detection by UPLC-IDA-MS.

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“…In line with the loss of the N-terminal region of the predicted product, there was no evidence that tslI encodes a bona fide acyl-HSL synthase. However, tslI is expressed and involved in acyl-HSL synthesis by MsaI and MlaI (15). We hypothesize that tslI encodes an enzyme that might be responsible for the biosynthesis of a regulatory molecule whose biosynthesis does not require S-adenosyl-L-methionine as substrate.…”

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confidence: 99%

“…CAD31444) (18). However, the predicted product of RMQ03963 shows 48% identity in local pair-wise alignments with Msi039 and 29% and 26% identity, respectively, with MlaI and MsaI (15). RMQ03963 is probably not part of an operon.…”

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confidence: 99%

“…To study the potential role of tslI in acyl-HSL production, we constructed a ⌬tslI mutant using pCM184 (9). Culture extracts of M. extorquens AM1 ⌬tslI::Km r were analyzed in bioassays using Chromobacterium violaceum CV026, Agrobacterium tumefaciens NTL4, and Pseudomonas putida F117 as biosensor strains (11,17,25) and using liquid chromatography-tandem mass spectrometry (LC-MS/MS) (12,15). Surprisingly, the acyl-HSL profile of the ⌬tslI mutant was indistinguishable from the ⌬msaI mutant (15), i.e., production of C 8 -and C 6 -HSL was abolished and C 14:1 -and C 14:2 -HSL synthesis was reduced ( Fig.…”

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confidence: 99%

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A Plasmid-Borne Truncated luxI Homolog Controls Quorum-Sensing Systems and Extracellular Carbohydrate Production in Methylobacterium extorquens AM1

et al. 2006

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A cryptic plasmid of Methylobacterium extorquens AM1 was found to encode tslI, a truncated luxI homolog. tslI was shown to be expressed and to control transcription of the acyl-homoserine lactone (HSL) synthase gene msaI and thus, indirectly, acyl-HSL production. In addition, tslI was found to positively regulate extracellular polysaccharide production.Many bacteria coordinate physiological processes, including biofilm differentiation, conjugation, and motility, by intercellular signaling. This type of regulation, termed quorum sensing (QS), allows the coordination of gene expression through the perception of signal molecules in a concentration-dependent manner. Produced by homoserine lactone synthases, many gram-negative bacteria secrete N-acyl-homoserine lactones (acyl-HSLs) as the QS signal molecules (6). Acyl-HSLs vary in the acyl group length, the substitution on the third carbon, and the degree of saturation of the acyl chain. These differences confer signal specificity through the affinity of receptor proteins of the LuxR family (6).Methylobacterium spp. are systematically found in association with plants and potentially dominate the epiphytic population (4, 8). These ␣-Proteobacteria are capable of utilizing substrates lacking carbon-carbon bonds (3, 21) and take advantage of methanol produced by plants (19). We have recently shown that the model methylotroph Methylobacterium extorquens AM1 possesses two functional LuxI homologs: MsaI, responsible for the synthesis of C 8 -HSL and C 6 -HSL, and MlaI, responsible for C 14:1 -HSL and C 14:2 -HSL (15), which are organized in hierarchical fashion, with MsaI activity required for full expression of mlaI.Identification of a truncated LuxI homolog. The genome of M. extorquens AM1 is composed of a single chromosome of 6.8 Mb and three plasmids of 44, 38, and 25 kb (M. E. Lidstrom et al., unpublished data). To date, these plasmids are cryptic and no functions could be attributed to them. A BLAST search in the genome sequence of M. extorquens AM1 (http://www .integratedgenomics.com/genomereleases.html#6) permitted us to identify an open reading frame (ORF) (RMQ03963) which is preceded by a ribosome binding site and which encodes a putative protein of 123 amino acids that is located on the 44-kb plasmid. The predicted product of RMQ03963 exhibits 24% sequence identity to Msi039, a predicted LuxI homolog in Mesorhizobium loti M7A (accession no. CAD31444) (18). However, the predicted product of RMQ03963 shows 48% identity in local pair-wise alignments with Msi039 and 29% and 26% identity, respectively, with MlaI and MsaI (15). RMQ03963 is probably not part of an operon. In its upstream region, RMQ03963 is flanked by an ORF predicted to encode a transposase and in the downstream region by an ORF predicted to encode MobC, involved in conjugation (5) (Fig. 1A). The RMQ03963 gene product is remarkably short, since described LuxI homologs are 180 to 230 amino acids long (6). Protein sequence alignment showed that eight conserved residues in LuxI-type enzymes were not pres...

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Methylobacterium extorquens AM1 produces a novel type of acyl‐homoserine lactone with a double unsaturated side chain under methylotrophic growth conditions

Cited by 38 publications

References 29 publications

Microbial interactions associated with biofilms attached to Trichodesmium spp. and detrital particles in the ocean

Microbial interactions associated with biofilms attached to Trichodesmium spp. and detrital particles in the ocean

Nitrite-Oxidizing Bacterium Nitrobacter winogradskyi Produces N -Acyl-Homoserine Lactone Autoinducers

A Plasmid-Borne Truncated luxI Homolog Controls Quorum-Sensing Systems and Extracellular Carbohydrate Production in Methylobacterium extorquens AM1

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