Exploring Genetic Diversity and Signatures of Horizontal Gene Transfer in Nodule Bacteria Associated with <i>Lotus japonicus</i> in Natural Environments

Bamba, Masaru; Aoki, Seishiro; Kajita, Tadashi; Setoguchi, Hiroaki; Tsuchimatsu, Takashi

doi:10.1094/mpmi-02-19-0039-r

Cited by 9 publications

(15 citation statements)

References 83 publications

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“…The presence of identical nodA and nifH in Cupriavidus sp. and in C. taiwanensis might be evidence that lateral transfer of symbiosis gene between these two species has happened, as reported in the Lotusnodulation Mesorhizobium species (Bamba et al, 2019). The situation in the three Rhizobium species was similar.…”

Section: Mimosa-nodulating Rhizobial Community In Southern Chinasupporting

confidence: 57%

Diversity and Geographic Distribution of Microsymbionts Associated With Invasive Mimosa Species in Southern China

et al. 2020

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In order to investigated diversity and geographic distribitution of rhizobia associated with invasive Mimosa species, Mimosa nodules and soils around the plants were sampled from five provinces in southern China. In total, 361 isolates were obtained from Mimosa pudica and Mimosa diplotricha in 25 locations. A multi-locus sequence analysis (MLSA) including 16S rRNA, atpD, dnaK, glnA, gyrB, and recA identified the isolates into eight genospecies corresponding to Paraburkhleria mimosarum, Paraburkholderia phymatum, Paraburkholeria carbensis, Cupriavidus taiwanensis, Cupriavidus sp., Rhizobium altiplani, Rhizobium mesoamericanum, and Rhizobium etli. The majority of the isolates were Cupriavidus (62.6%), followed by Paraburkholderia (33.5%) and Rhizobium (2.9%). Cupriavidus strains were more predominant in nodules of M. diplotricha (76.2) than in M. pudica (59.9%), and the distribution of P. phymatum in those two plant species was reverse (3.4:18.2%). Four symbiotypes were defined among the isolates based upon the phylogeny of nodA-nifH genes, represented by P. mimosarum, P. phymatum-P. caribensis, Cupriavidus spp., and Rhizobium spp. The species affiliation and the symbiotype division among the isolates demonstrated the multiple origins of Mimosa rhizobia in China: most were similar to those found in the original centers of Mimosa plants, but Cupriavidus sp. might have a local origin. The unbalanced distribution of symbionts between the two Mimosa species might be related to the soil pH, organic matter and available nitrogen; Cupriavidus spp. generally dominated most of the soils colonized by Mimosa in this study, but it had a particular preference for neutral-alkaline soils with low fertility whereas. While Paraburkholderia spp. preferred more acidic and fertile soils. The Rhizobium spp. tended to prefer neutral-acidic soils with high fertility soils.

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Section: Mimosa-nodulating Rhizobial Community In Southern Chinasupporting

confidence: 57%

Diversity and Geographic Distribution of Microsymbionts Associated With Invasive Mimosa Species in Southern China

et al. 2020

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“…Importantly, natural populations of Lotus japonicus commonly form from 10 to over 100 nodules (Bamba et al. 2019, Bamba personal communication ), so we were able to simulate some of the natural variation expressed in this species, albeit under highly controlled biotic and abiotic conditions.…”

Section: Resultsmentioning

confidence: 99%

“…In natural populations in Japan, Lotus japonicus commonly form up to 100 nodules (Bamba et al. 2019; Bamba personal communication), so it is possible that the conflict we induced over nodule formation occurs in natural populations.…”

Section: Discussionmentioning

confidence: 99%

Dysregulation of host‐control causes interspecific conflict over host investment into symbiotic organs

et al. 2021

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Microbial mutualists provide substantial benefits to hosts that feed back to enhance the fitness of the associated microbes. In many systems, beneficial microbes colonize symbiotic organs, specialized host structures that house symbionts and mediate resources exchanged between parties. Mutualisms are characterized by net benefits exchanged among members of different species, however, inequalities in the magnitude of these exchanges could result in evolutionary conflict, destabilizing the mutualism. We investigated joint fitness effects of root nodule formation, the symbiotic organ of legumes that house nitrogen‐fixing rhizobia in planta. We quantified host and symbiont fitness parameters dependent on the number of nodules formed using near‐isogenic Lotus japonicus and Mesorhizobium loti mutants, respectively. Empirically estimated fitness functions suggest that legume and rhizobia fitness is aligned as the number of nodules formed increases from zero until the host optimum is reached, a point where aligned fitness interests shift to diverging fitness interests between host and symbiont. However, fitness conflict was only inferred when analyzing wild‐type hosts along with their mutants dysregulated for control over nodule formation. These data demonstrate that to avoid conflict, hosts must tightly regulate investment into symbiotic organs maximizing their benefit to cost ratio of associating with microbes.

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“…These nine strains were sampled from three geographically distinct localities, , Aomori (131-2-1, 131-2-5 and 131-3-5) and Miyakojima (L-2-11, L-8-3 and L-8-10) (Supporting Information Table S1), where L. japonicus natural accessions of the Natural BioResource Project also originated (MG50 from Tottori, MG23 from Aomori and MG20 from Miyakojima; Supporting Information Table S2). Details of the sampling localities have been described by Bamba et al (2019b).…”

Section: Bacterial Strainsmentioning

confidence: 99%

“…Among L. japonicus-associated symbionts, fullgenome sequence information is available from two strains, Mesorhizobium japonicum MAFF303099 and M. loti TONO (Kaneko et al 2000;Shimoda et al 2016). Bamba et al (2019b) explored the genetic diversity of L. japonicus-associated symbionts, finding that L. japonicus in natural populations were associated with highly diverse Mesorhizobium bacteria. However, they used only three housekeeping and five symbiotic genes, and the detailed genomic variations of L. japonicus-associated symbionts are still unknown.…”

Section: Introductionmentioning

confidence: 99%

Massive rhizobial genomic variation associated with partner quality in Lotus–Mesorhizobium symbiosis

Bamba

Aoki

Kajita

et al. 2020

FEMS Microbiology Ecology

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Variation in partner quality is commonly observed in diverse cooperative relationships, despite the theoretical prediction that selection favoring high-quality partners should eliminate such variation. Here, we investigated how genetic variation in partner quality could be maintained in the nitrogen-fixing mutualism between Lotus japonicus and Mesorhizobium bacteria. We reconstructed de novo assembled full-genome sequences from nine rhizobial symbionts, finding massive variation in the core genome and the similar symbiotic islands, indicating recent horizontal gene transfer (HGT) of the symbiosis islands into diverse Mesorhizobium lineages. A cross-inoculation experiment using nine sequenced rhizobial symbionts and 15 L. japonicus accessions revealed extensive quality variation represented by plant growth phenotypes, including genotype-by-genotype interactions. Variation in quality was not associated with the presence/absence variation in known symbiosis-related genes in the symbiosis island; rather, it showed significant correlation with the core genome variation. Given the recurrent HGT of the symbiosis islands into diverse Mesorhizobium strains, local Mesorhizobium communities could serve as a major source of variation for core genomes, which might prevent variation in partner quality from fixing, even in the presence of selection favoring high-quality partners. These findings highlight the novel role of HGT of symbiosis islands in maintaining partner quality variation in the legume-rhizobia symbiosis.

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Exploring Genetic Diversity and Signatures of Horizontal Gene Transfer in Nodule Bacteria Associated with Lotus japonicus in Natural Environments

Cited by 9 publications

References 83 publications

Diversity and Geographic Distribution of Microsymbionts Associated With Invasive Mimosa Species in Southern China

Diversity and Geographic Distribution of Microsymbionts Associated With Invasive Mimosa Species in Southern China

Dysregulation of host‐control causes interspecific conflict over host investment into symbiotic organs

Massive rhizobial genomic variation associated with partner quality in Lotus–Mesorhizobium symbiosis

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