Transient Hypermutagenesis Accelerates the Evolution of Legume Endosymbionts following Horizontal Gene Transfer

Remigi, Philippe; Capela, Delphine; Clérissi, Camille; Tasse, Léna; Torchet, Rachel; Bouchez, Olivier; Batut, Jacques; Cruveiller, Stéphane; Rocha, Eduardo P. C.; Masson‐Boivin, Catherine

doi:10.1371/journal.pbio.1001942

Cited by 60 publications

(63 citation statements)

References 67 publications

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“…We found that plant compounds enhance HGT and initiate the nodulation process that ensures massive and specific multiplication, through the interaction with ICElocated regulatory genes. Interestingly, it was recently shown that the dissemination of symbiotic plasmids to different taxa is assisted by error-prone DNA polymerases encoded in the transferred element, which are more active in the plant environment (43). Altogether, these observations support the view that both the plant and the symbiosis element manipulate in concert with the bacterium (8).…”

Section: Discussionmentioning

confidence: 68%

Plant nodulation inducers enhance horizontal gene transfer of Azorhizobium caulinodans symbiosis island

Ling

Wang

et al. 2016

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

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Horizontal gene transfer (HGT) of genomic islands is a driving force of bacterial evolution. Many pathogens and symbionts use this mechanism to spread mobile genetic elements that carry genes important for interaction with their eukaryotic hosts. However, the role of the host in this process remains unclear. Here, we show that plant compounds inducing the nodulation process in the rhizobium-legume mutualistic symbiosis also enhance the transfer of symbiosis islands. We demonstrate that the symbiosis island of the Sesbania rostrata symbiont, Azorhizobium caulinodans, is an 87.6-kb integrative and conjugative element (ICE Ac ) that is able to excise, form a circular DNA, and conjugatively transfer to a specific site of gly-tRNA gene of other rhizobial genera, expanding their host range. The HGT frequency was significantly increased in the rhizosphere. An ICE Aclocated LysR-family transcriptional regulatory protein AhaR triggered the HGT process in response to plant flavonoids that induce the expression of nodulation genes through another LysR-type protein, NodD. Our study suggests that rhizobia may sense rhizosphere environments and transfer their symbiosis gene contents to other genera of rhizobia, thereby broadening rhizobial host-range specificity.horizontal gene transfer | host-range | integrative and conjugative element | naringenin | nodulation

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Section: Discussionmentioning

confidence: 68%

Plant nodulation inducers enhance horizontal gene transfer of Azorhizobium caulinodans symbiosis island

Ling

Wang

et al. 2016

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

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“…All findings in this study from the PU‐HPC bipartite network analysis underscore the importance of undertaking subsequent sequencing and experiment projects in resolving the issue concerning genomic annotation and interaction of rhizobial plasmids (diCenzo et al ., 2014). Further work aimed at identifying the selective forces acting on both symbiotic and accessory plasmids and responsible for variation in nitrogen fixation efficiency should also help in understanding their co‐evolutionary framework ruling the evolution of Rhizobium ‐legume symbiosis (Remigi et al ., ). Given the increasing availability and utilization of multiomics sequencing with the rapid development of network analysis approaches, such as multipartite network and multilayer network, we can expect to better understand these intriguing genetic elements in various lifestyles of all rhizobial bacteria (diCenzo et al ., ; Marx et al ., ).…”

Section: Discussionmentioning

confidence: 97%

Exploring the evolutionary dynamics of Rhizobium plasmids through bipartite network analysis

Wang

Tong

et al. 2019

Environmental Microbiology

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Summary The genus Rhizobium usually has a multipartite genome architecture with a chromosome and several plasmids, making these bacteria a perfect candidate for plasmid biology studies. As there are no universally shared genes among typical plasmids, network analyses can complement traditional phylogenetics in a broad‐scale study of plasmid evolution. Here, we present an exhaustive analysis of 216 plasmids from 49 complete genomes of Rhizobium by constructing a bipartite network that consists of two classes of nodes, the plasmids and homologous protein families that connect them. Dissection of the network using a hierarchical clustering strategy reveals extensive variety, with 34 homologous plasmid clusters. Four large clusters including one cluster of symbiotic plasmids and two clusters of chromids carrying some truly essential genes are widely distributed among Rhizobium. In contrast, the other clusters are quite small and rare. Symbiotic clusters and rare accessory clusters are exogenetic and do not appear to have co‐evolved with the common accessory clusters; the latter ones have a large coding potential and functional complementarity for different lifestyles in Rhizobium. The bipartite network also provides preliminary evidence of Rhizobium plasmid variation and formation including genetic exchange, plasmid fusion and fission, exogenetic plasmid transfer, host plant selection, and environmental adaptation.

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“…In a particularly notable case, interspecies transfer of a symbiotic plasmid was coupled with laboratory evolution in an ongoing attempt to yield a symbiosiscompetent strain. The researchers established Ralstonia solanacearum (a plant pathogen) carrying the symbiotic plasmid of the rhizobium species Cupriavidus taiwanensis as the test system (Marchetti et al 2010(Marchetti et al , 2014Guan et al 2013;Remigi et al 2014;Capela et al 2017). Although initially unable to form nodules, adaptive mutations, such as in the type III secretion system, were identified that allowed for nodulation to occur (Marchetti et al 2010).…”

Section: Large-scale Genome Manipulationsmentioning

confidence: 99%

Multidisciplinary approaches for studying rhizobium–legume symbioses

et al. 2019

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The rhizobium-legume symbiosis is a major source of fixed nitrogen (ammonia) in the biosphere. The potential for this process to increase agricultural yield while reducing the reliance on nitrogen-based fertilizers has generated interest in understanding and manipulating this process. For decades, rhizobium research has benefited from the use of leading techniques from a very broad set of fields, including population genetics, molecular genetics, genomics, and systems biology. In this review, we summarize many of the research strategies that have been employed in the study of rhizobia and the unique knowledge gained from these diverse tools, with a focus on genome- and systems-level approaches. We then describe ongoing synthetic biology approaches aimed at improving existing symbioses or engineering completely new symbiotic interactions. The review concludes with our perspective of the future directions and challenges of the field, with an emphasis on how the application of a multidisciplinary approach and the development of new methods will be necessary to ensure successful biotechnological manipulation of the symbiosis.

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Transient Hypermutagenesis Accelerates the Evolution of Legume Endosymbionts following Horizontal Gene Transfer

Abstract: Stress-responsive error-prone DNA polymerase genes transferred along with key symbiotic genes ease the evolution of a soil bacterium into a legume endosymbiont by accelerating adaptation of the recipient bacterial genome to its new plant host.

Cited by 60 publications

References 67 publications

Plant nodulation inducers enhance horizontal gene transfer of Azorhizobium caulinodans symbiosis island

Plant nodulation inducers enhance horizontal gene transfer of Azorhizobium caulinodans symbiosis island

Exploring the evolutionary dynamics of Rhizobium plasmids through bipartite network analysis

Multidisciplinary approaches for studying rhizobium–legume symbioses

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