Population genomics of the symbiotic plasmids of sympatric nitrogen‐fixing <i>Rhizobium</i> species associated with <i>Phaseolus vulgaris</i>

Pérez-Carrascal, Olga María; VanInsberghe, David; Juárez, Soledad; Polz, Martin F.; Vinuesa, Pablo; González, Víctor

doi:10.1111/1462-2920.13415

Cited by 51 publications

(49 citation statements)

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“…These results lend support to the hypothesis that host plant selection contributes to the adaptive evolution of pSyms and structuring of rhizobial communities on host legume rhizosperes, root surfaces and nodules (Miranda‐Sánchez et al ., ; Remigi et al ., ). In addition, most of the pSyms are conjugative and have lower diversity, higher recombination rates and different codon usage bias compared with both the common accessory PUCs and the main chromosomes (Pérez Carrascal et al ., ). These evolutionary characteristics indicate that most of the pSyms do not appear to have co‐evolved with the chromosomes or accessory plasmids.…”

Section: Discussionmentioning

confidence: 97%

“…Additionally, our conclusion is consistent with previous finding in the reference R . etli CFN42 genome, where the plasmids p42b (PUC 6), p42c (PUC 1), p42e (PUC 2) and p42f (PUC 3) are strongly related functionally and have co‐evolved with the chromosomes over a long period, while p42a (PUC 15) and p42d_Sym (PUC 8) were only recently acquired (González et al ., ; Pérez Carrascal et al ., ; Bañuelos‐Vazquez et al ., ). Increasing evidence has been mounting regarding the accessory plasmids' influence on legume‐rhizobia symbiosis under stress, such as resistance to heat, acid, antibiotics, heavy metals, pesticides and oxidative stress protection (Kurchak et al ., ; Streit et al ., , 234; Anjum et al ., ; Vercruysse et al ., ; Naamala et al ., ).…”

Section: Discussionmentioning

confidence: 99%

“…Furthermore, the plasmids are crucial mediators of horizontal gene transfer (HGT), permitting spread of symbiotic ability (Li et al, 2018). The prominent characters of plasmids, such as plasticity, dynamics and diversity, owing to transposition, HGT, plasmid-DNA recombination and genome rearrangement are well documented (Freiberg et al, 1997;Zhang et al, 2001;González, 2003;Brom et al, 2004;López-Guerrero et al, 2012;Pérez Carrascal et al, 2016). For example, the genome of Rhizobium sp.…”

Section: Introductionmentioning

confidence: 99%

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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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Section: Discussionmentioning

confidence: 97%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Exploring the evolutionary dynamics of Rhizobium plasmids through bipartite network analysis

Wang

Tong

et al. 2019

Environmental Microbiology

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“…In an issue of Environmental Microbiology , Pérez‐Carrascal et al . () leverage natural populations of rhizobia to address fundamental questions about bacterial evolution. Using Illumina whole‐genome sequencing of 33 strains of Rhizobium collected from the roots and rhizospheres of 6 common bean plants from a field in Mexico, they find five evolutionarily‐distinct clusters (“species” defined at 95% nucleotide identity).…”

Section: Rhizobia As Models Of Mutualism Coevolutionmentioning

confidence: 99%

Rhizobia: tractable models for bacterial evolutionary ecology

Heath

Grillo

2016

Environmental Microbiology

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“…The primary conclusion of these 297 studies is that poor, if any, symbiotic abilities are transferred to the recipient strain. This 298 observation is perhaps surprising considering that natural lateral transfer of symbiotic plasmids 299 and islands between related strains results in a gain of symbiotic abilities (Mozo et al 1988, 300 Laguerre 1992, Sullivan et al 1995, Sullivan and Ronson 1998, Pérez Carrascal et al 2016, 301 Haskett et al 2016). However, non-fixing outcomes after inter-species heterologous gene transfer 302 may be due to an incomplete complement of symbiotic functions in the transconjugant strains, or 303 due to incompatible alleles of a common gene (diCenzo et al 2017c 15 is being used for identification of the necessary and sufficient set of symbiotic genes on these 309…”

mentioning

confidence: 99%

Multi-disciplinary approaches for studying rhizobium – legume symbioses

diCenzo

Zamani

Checcucci

et al. 2018

Preprint

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24The rhizobium-legume symbiosis is a major source of fixed nitrogen (ammonia) in the 25 biosphere. The potential for this process to increase agricultural yield while reducing the reliance 26 on nitrogen-based fertilizers has generated interest in understanding and manipulating this process. 27For decades, rhizobium research has benefited from the use of leading techniques from a very 28 broad set of fields, including population genetics, molecular genetics, genomics, and systems 29 biology. In this review, we summarize many of the research strategies that have been employed in 30 the study of rhizobia and the unique knowledge gained from these diverse tools, with a focus on 31 genome and systems-level approaches. We then describe ongoing synthetic biology approaches 32 aimed at improving existing symbioses or engineering completely new symbiotic interactions. The 33 review concludes with our perspective of the future directions and challenges of the field, with an 34 emphasis on how the application of a multi-disciplinary approach and the development of new 35 methods will be necessary to ensure successful biotechnological manipulation of the symbiosis. SYMBIOTIC NITROGEN FIXATION: CHALLENGES AND PROSPECTS 60Biological nitrogen fixation (BNF) is an agriculturally and ecologically crucial process that 61 is performed by prokaryotes in two ecological groups: i) BNF performed by free-living cells often 62 in close association with plants, or ii) by rhizobia that fix nitrogen during an endosymbiotic 63 relationship with legumes. The fixation of N2-gas into ammonia by root-nodule bacteria (rhizobia) 64 is referred to as symbiotic nitrogen fixation (SNF), and it is a more efficient process in terms of 65 supplying nitrogen to the plant. Phylogenetically, most rhizobia are α-proteobacteria, but some 66 rhizobia are β-proteobacteria ( Figure 1). The various genetic, biochemical, and evolutionary 67 aspects of the symbiotic interaction have been reviewed over the years (Long 1996, Gage 2004, 68 MacLean et al. 2007, Jones et al. 2007, Gibson et al. 2008, Oldroyd and Downie 2008, Masson-69 Boivin et al. 2009, Downie 2010, Oldroyd et al. 2011, Udvardi and Poole 2013, Haag et al. 2013, 70 Remigi et al. 2016, Mus et al. 2016, Poole et al. 2018. In brief, the symbiosis is initiated following 71an exchange of signals between the roots of the plant and free-living rhizobia in root-proximal soil 72 (the rhizosphere). As root nodule tissue develops (Figure 2), the rhizobia enter this specialized 73 tissue through an extracellular infection thread; as these inwardly growing threads reach 74 differentiated nodule cells, the bacteria become surrounded by a plant-derived membrane and 75 taken up into the plant cytosol, where they are known as bacteroids. The nascent bacteroids then 76 undergo major morphological and transcriptional changes, leading to active nitrogen fixation, 77 which is the conversion of atmospheric N2 into NH3 for the plant. 78It has been estimated that BNF contributes several teragrams of nitr...

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Population genomics of the symbiotic plasmids of sympatric nitrogen‐fixing Rhizobium species associated with Phaseolus vulgaris

Cited by 51 publications

References 89 publications

Exploring the evolutionary dynamics of Rhizobium plasmids through bipartite network analysis

Exploring the evolutionary dynamics of Rhizobium plasmids through bipartite network analysis

Rhizobia: tractable models for bacterial evolutionary ecology

Multi-disciplinary approaches for studying rhizobium – legume symbioses

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