A LuxRI‐family regulatory system controls excision and transfer of the <i>Mesorhizobium loti</i> strain R7A symbiosis island by activating expression of two conserved hypothetical genes

Ramsay, Joshua P.; Sullivan, John T.; Jambari, Nuzul Noorahya; Ortori, Catharine A.; Heeb, Stephan; Williams, Paul; Barrett, David A.; Lamont, Iain L.; Ronson, Clive W.

doi:10.1111/j.1365-2958.2009.06843.x

Cited by 60 publications

(100 citation statements)

References 55 publications

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“…S6). Because these bacteria use AHL-based QS (8,(25)(26)(27), we asked whether promotion of long-chain AHL sensing is a common trait of their FadL proteins. For this, fadL homologs from these species were ectopically expressed in the S. meliloti sinI fadL mutant by introduction of plasmid-localized heterologous fadL genes driven by an IPTG-inducible lac promoter.…”

Section: Resultsmentioning

confidence: 99%

Rhizobial homologs of the fatty acid transporter FadL facilitate perception of long-chain acyl-homoserine lactone signals

Krol

Becker

2014

Proc. Natl. Acad. Sci. U.S.A.

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Significance Bacterial intercellular communication is crucial for developing population and community structures and for pathogenic and symbiotic interactions with eukaryotic hosts. Many Gram-negative bacteria use N-acyl-homoserine lactones (AHLs) in quorum sensing-related signaling. Although it is likely that specific transport mechanisms are required for long-chain AHLs to overcome the outer membrane, mechanisms promoting uptake have not been reported so far. Here we present evidence that homologs of the outer membrane long-chain fatty acid transporter FadL facilitate uptake of long-chain AHLs, which closes an important gap in our understanding of quorum sensing signaling. Our findings suggest that bacteria responding to long-chain AHLs have evolved specificity of FadL toward these signal molecules and have partly lost the ability to transport long-chain fatty acid by this protein.

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Section: Resultsmentioning

confidence: 99%

Rhizobial homologs of the fatty acid transporter FadL facilitate perception of long-chain acyl-homoserine lactone signals

Krol

Becker

2014

Proc. Natl. Acad. Sci. U.S.A.

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“…Rhizobia are phylogenetically disparate bacteria distributed in many genera of a-and b-proteobacteria intermixed with saprophytes and pathogens from which they may have evolved (Bontemps et al, 2010;Sachs et al, 2011). A bulk of evidence indicates that the large phylogenetic diversity of rhizobia originates from repeated and independent events of lateral gene transfer (LGT) of key symbiotic functions carried by plasmids or islands to nonsymbiotic bacterial recipient genomes (Sullivan and Ronson, 1998;Rogel et al, 2001;Ramsay et al, 2006Ramsay et al, , 2009. Nodulation genes notably bring the capacity to synthesize morphogenic Nod factors signals that trigger the plant developmental program required for root hair infection and nodule organogenesis (Gough and Cullimore, 2011;Oldroyd et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

Experimental evolution of nodule intracellular infection in legume symbionts

et al. 2013

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Soil bacteria known as rhizobia are able to establish an endosymbiosis with legumes that takes place in neoformed nodules in which intracellularly hosted bacteria fix nitrogen. Intracellular accommodation that facilitates nutrient exchange between the two partners and protects bacteria from plant defense reactions has been a major evolutionary step towards mutualism. Yet the forces that drove the selection of the late event of intracellular infection during rhizobium evolution are unknown. To address this question, we took advantage of the previous conversion of the plant pathogen Ralstonia solanacearum into a legume-nodulating bacterium that infected nodules only extracellularly. We experimentally evolved this draft rhizobium into intracellular endosymbionts using serial cycles of legume-bacterium cocultures. The three derived lineages rapidly gained intracellular infection capacity, revealing that the legume is a highly selective environment for the evolution of this trait. From genome resequencing, we identified in each lineage a mutation responsible for the extracellular-intracellular transition. All three mutations target virulence regulators, strongly suggesting that several virulence-associated functions interfere with intracellular infection. We provide evidence that the adaptive mutations were selected for their positive effect on nodulation. Moreover, we showed that inactivation of the type three secretion system of R. solanacearum that initially allowed the ancestral draft rhizobium to nodulate, was also required to permit intracellular infection, suggesting a similar checkpoint for bacterial invasion at the early nodulation/root infection and late nodule cell entry levels. We discuss our findings with respect to the spread and maintenance of intracellular infection in rhizobial lineages during evolutionary times.

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“…After a 7-y period, only ∼20% of L. corniculatus root nodules contained R7A; the other 80% of nodules contained a diverse mix of native mesorhizobia that had acquired symbiosis genes from R7A (11). Molecular analyses revealed these new symbionts had acquired a 502-kb symbiosis ICE, subsequently named ICEMlSym R7A (12)(13)(14).The mechanism and regulation of ICEMlSym R7A integration and excision have been investigated in detail (12,(15)(16)(17)(18). Integration of ICEMlSym R7A is catalyzed by the integrase IntS, which recombines the attachment (att) site attP located on the circularized ICEMlSym R7A with the attB site located at the 3′ end of the sole phetRNA gene present in Mesorhizobium genomes.…”

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confidence: 99%

“…The mechanism and regulation of ICEMlSym R7A integration and excision have been investigated in detail (12,(15)(16)(17)(18). Integration of ICEMlSym R7A is catalyzed by the integrase IntS, which recombines the attachment (att) site attP located on the circularized ICEMlSym R7A with the attB site located at the 3′ end of the sole phetRNA gene present in Mesorhizobium genomes.…”

mentioning

confidence: 99%

Assembly and transfer of tripartite integrative and conjugative genetic elements

Haskett

Terpolilli

Bekuma

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Integrative and conjugative elements (ICEs) are ubiquitous mobile genetic elements present as "genomic islands" within bacterial chromosomes. Symbiosis islands are ICEs that convert nonsymbiotic mesorhizobia into symbionts of legumes. Here we report the discovery of symbiosis ICEs that exist as three separate chromosomal regions when integrated in their hosts, but through recombination assemble as a single circular ICE for conjugative transfer. Whole-genome comparisons revealed exconjugants derived from nonsymbiotic mesorhizobia received three separate chromosomal regions from the donor Mesorhizobium ciceri WSM1271. The three regions were each bordered by two nonhomologous integrase attachment (att) sites, which together comprised three homologous pairs of attL and attR sites. Sequential recombination between each attL and attR pair produced corresponding attP and attB sites and joined the three fragments to produce a single circular ICE, ICEMcSym 1271 . A plasmid carrying the three attP sites was used to recreate the process of tripartite ICE integration and to confirm the role of integrase genes intS, intM, and intG in this process. Nine additional tripartite ICEs were identified in diverse mesorhizobia and transfer was demonstrated for three of them. The transfer of tripartite ICEs to nonsymbiotic mesorhizobia explains the evolution of competitive but suboptimal N 2 -fixing strains found in Western Australian soils. The unheralded existence of tripartite ICEs raises the possibility that multipartite elements reside in other organisms, but have been overlooked because of their unusual biology. These discoveries reveal mechanisms by which integrases dramatically manipulate bacterial genomes to allow cotransfer of disparate chromosomal regions.integrative and conjugative elements | integrase | recombination | conjugation | symbiosis H orizontal gene transfer plays an instrumental role in prokaryotic evolution because it facilitates the rapid acquisition of complex phenotypic traits required for pathogenicity, symbiosis, metabolism, fitness, and antimicrobial resistance (1-8). Integrative and conjugative elements (ICEs) are an abundant class of conjugative elements in bacteria, but they are also the most recently recognized and least characterized (8,9). An ICE integrates site-specifically within the chromosome of its host and is flanked by a direct repeat sequence that demarcates the insertion site. Before transfer, site-specific recombination between the flanking sequences results in excision and circularization of the ICE and restoration of the host chromosome. A single-stranded DNA copy of the circularized ICE is then formed via rollingcircle replication and transferred to recipient cells via an ICEencoded conjugative type IV secretion system. Following delivery of the ICE to the recipient cell, the second DNA strand of the ICE is synthesized and the circularized ICE integrates sitespecifically into the recipient genome (10).Symbiosis islands are the largest documented ICEs and their transfer converts nonsymb...

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A LuxRI‐family regulatory system controls excision and transfer of the Mesorhizobium loti strain R7A symbiosis island by activating expression of two conserved hypothetical genes

Cited by 60 publications

References 55 publications

Rhizobial homologs of the fatty acid transporter FadL facilitate perception of long-chain acyl-homoserine lactone signals

Rhizobial homologs of the fatty acid transporter FadL facilitate perception of long-chain acyl-homoserine lactone signals

Experimental evolution of nodule intracellular infection in legume symbionts

Assembly and transfer of tripartite integrative and conjugative genetic elements

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