Comparative Genomics of Aeschynomene Symbionts: Insights into the Ecological Lifestyle of Nod-Independent Photosynthetic Bradyrhizobia

Mornico, Damien; Miché, Lucie; Béna, Gilles; Nouwen, Nico; Vermeglio, André; Vallenet, David; Smith, Alexander; Giraud, Éric; Médigue, Claudine; Moulin, Lionel

doi:10.3390/genes3010035

Cited by 30 publications

(30 citation statements)

References 59 publications

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“…Among these aquatic species, A. indica (CI group 3) forms stem and/or root nodules with PB strains (2,37). These data were congruent with our results; the PB strains SUT-PR48 and SUT-PR64 could form nodules with A. indica (African ecotype) (Fig.…”

Section: Discussionsupporting

confidence: 82%

“…The CalvinBenson-Bassham (CBB) cycle from Bradyrhizobium species plays an important role in chemoautotrophic growth (42), and it is important for efficient symbiosis with A. indica (43) by controlling the oxygen tension of the early stage of symbiosis (44). In addition, the ancestors of B. japonicum and A. indica symbionts were photosynthetic free-living bacteria (37). If this scenario is true, it should be hypothesized that strains SUT-PR48 and SUT-PR64 still preserve some ancestral properties of the PB group.…”

Section: Discussionmentioning

confidence: 99%

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Preferential Association of Endophytic Bradyrhizobia with Different Rice Cultivars and Its Implications for Rice Endophyte Evolution

Piromyou

Greetatorn

Teamtisong

et al. 2015

Appl Environ Microbiol

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Plant colonization by bradyrhizobia is found not only in leguminous plants but also in nonleguminous species such as rice. To understand the evolution of the endophytic symbiosis of bradyrhizobia, the effect of the ecosystems of rice plantations on their associations was investigated. Samples were collected from various rice (Oryza sativa) tissues and crop rotational systems. The rice endophytic bradyrhizobia were isolated on the basis of oligotrophic properties, selective medium, and nodulation on siratro (Macroptilium atropurpureum). Six bradyrhizobial strains were obtained exclusively from rice grown in a crop rotational system. The isolates were separated into photosynthetic bradyrhizobia (PB) and nonphotosynthetic bradyrhizobia (non-PB). Thai bradyrhizobial strains promoted rice growth of Thai rice cultivars better than the Japanese bradyrhizobial strains. This implies that the rice cultivars possess characteristics that govern rice-bacterium associations. To examine whether leguminous plants in a rice plantation system support the persistence of rice endophytic bradyrhizobia, isolates were tested for legume nodulation. All PB strains formed symbioses with Aeschynomene indica and Aeschynomene evenia. On the other hand, non-PB strains were able to nodulate Aeschynomene americana, Vigna radiata, and M. atropurpureum but unable to nodulate either A. indica or A. evenia. Interestingly, the nodABC genes of all of these bradyrhizobial strains seem to exhibit low levels of similarity to those of Bradyrhizobium diazoefficiens USDA110 and Bradyrhizobium sp. strain ORS285. From these results, we discuss the evolution of the plant-bradyrhizobium association, including nonlegumes, in terms of photosynthetic lifestyle and nod-independent interactions. P lant infection and colonization by bradyrhizobia are found in not only leguminous plants but also nonleguminous species such as rice (1, 2). However, the symbiosis mechanisms governing the relationship between Bradyrhizobium bacteria and rice have been absolutely unclear although the evolution of the bradyrhizobium-rice association may have occurred earlier than the bradyrhizobium-legume symbiosis. In addition, rice is the most important food crop in Asia. High-yield rice production requires huge amounts of nitrogen fertilizers. Biological nitrogen fixation (BNF) from rice root-associated bacteria has a great potential to improve sustainable rice production. Rice-legume rotational cropping systems are useful for rice production since legumes can be planted after the rice season, and nitrogen from the legumes can be provided for rice. Bradyrhizobia are well recognized for their ability to fix atmospheric dinitrogen into ammonia in the nodules of legumes, thus providing ammonia to host plants. The bradyrhizobium-legume symbiosis has been reported to increase the legume productivity of agricultural farms (3-5).Bradyrhizobium has been well defined as an oligotrophic bacteria which can survive under nutrient-deprived conditions (6, 7). In addition, a renewed interest in endop...

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Section: Discussionsupporting

confidence: 82%

Section: Discussionmentioning

confidence: 99%

Preferential Association of Endophytic Bradyrhizobia with Different Rice Cultivars and Its Implications for Rice Endophyte Evolution

Piromyou

Greetatorn

Teamtisong

et al. 2015

Appl Environ Microbiol

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“…The T3SS of the photosynthetic Bradyrhizobium ORS285 strain is not required for NF-independent symbiosis but contributes to the NF-dependent nodulation Unlike other photosynthetic Bradyrhizobium strains with sequenced genomes, the ORS285 strain contains nod genes and a T3SS gene cluster (Mornico et al, 2011). The composition and organization of this T3SS cluster is exactly the same as found in B. elkanii and B. japonicum USDA110 suggesting that it is functional (Supplementary Figure 3).…”

Section: Some Non-photosynthetic Bradyrhizobium Strains Induce Nitrogmentioning

confidence: 86%

“…Furthermore, besides lacking nod genes, most photosynthetic bradyrhizobia lack a T3SS. Again the ORS285 strain is an exception and probably acquired nod and T3SS genes simultaneously by lateral gene transfer (Mornico et al, 2011). This indicates that photosynthetic bradyrhizobia could interact with Aeschynomene using another pathway than the one operating during the interaction between a NF-deficient B. elkanii mutant and soybean.…”

Section: Introductionmentioning

confidence: 98%

Rhizobium–legume symbiosis in the absence of Nod factors: two possible scenarios with or without the T3SS

et al. 2015

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The occurrence of alternative Nod factor (NF)-independent symbiosis between legumes and rhizobia was first demonstrated in some Aeschynomene species that are nodulated by photosynthetic bradyrhizobia lacking the canonical nodABC genes. In this study, we revealed that a large diversity of non-photosynthetic bradyrhizobia, including B. elkanii, was also able to induce nodules on the NFindependent Aeschynomene species, A. indica. Using cytological analysis of the nodules and the nitrogenase enzyme activity as markers, a gradient in the symbiotic interaction between bradyrhizobial strains and A. indica could be distinguished. This ranged from strains that induced nodules that were only infected intercellularly to rhizobial strains that formed nodules in which the host cells were invaded intracellularly and that displayed a weak nitrogenase activity. In all nonphotosynthetic bradyrhizobia, the type III secretion system (T3SS) appears required to trigger nodule organogenesis. In contrast, genome sequence analysis revealed that apart from a few exceptions, like the Bradyrhizobium ORS285 strain, photosynthetic bradyrhizobia strains lack a T3SS. Furthermore, analysis of the symbiotic properties of an ORS285 T3SS mutant revealed that the T3SS could have a positive or negative role for the interaction with NF-dependent Aeschynomene species, but that it is dispensable for the interaction with all NF-independent Aeschynomene species tested. Taken together, these data indicate that two NF-independent symbiotic processes are possible between legumes and rhizobia: one dependent on a T3SS and one using a so far unknown mechanism.

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“…3). However, it is unclear whether these genes play important roles in the infection of A. indica, because they are absent in the genomes of ORS278, BTAi1, and other strains lacking the nod genes (39).…”

Section: Resultsmentioning

confidence: 99%

Genome Analysis Suggests that the Soil Oligotrophic Bacterium Agromonas oligotrophica (Bradyrhizobium oligotrophicum) Is a Nitrogen-Fixing Symbiont of Aeschynomene indica

Okubo

Fukushima

Itakura

et al. 2013

Appl Environ Microbiol

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T is a nitrogen-fixing oligotrophic bacterium isolated from paddy field soil that is able to grow in extra-low-nutrient environments. Here, the complete genome sequence of S58 was determined. The S58 genome was found to comprise a circular chromosome of 8,264,165 bp with an average GC content of 65.1% lacking nodABC genes and the typical symbiosis island. The genome showed a high level of similarity to the genomes of Bradyrhizobium sp. ORS278 and Bradyrhizobium sp. BTAi1, including nitrogen fixation and photosynthesis gene clusters, which nodulate an aquatic legume plant, Aeschynomene indica, in a Nod factor-independent manner. Although nonsymbiotic (brady)rhizobia are significant components of rhizobial populations in soil, we found that most genes important for nodule development (ndv) and symbiotic nitrogen fixation (nif and fix) with A. indica were well conserved between the ORS278 and S58 genomes. Therefore, we performed inoculation experiments with five A. oligotrophica strains (S58, S42, S55, S72, and S80). Surprisingly, all five strains of A. oligotrophica formed effective nitrogen-fixing nodules on the roots and/or stems of A. indica, with differentiated bacteroids. Nonsymbiotic (brady)rhizobia are known to be significant components of rhizobial populations without a symbiosis island or symbiotic plasmids in soil, but the present results indicate that soil-dwelling A. oligotrophica generally possesses the ability to establish symbiosis with A. indica. Phylogenetic analyses suggest that Nod factor-independent symbiosis with A. indica is a common trait of nodABC-and symbiosis island-lacking strains within the members of the photosynthetic Bradyrhizobium clade, including A. oligotrophica.

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Comparative Genomics of Aeschynomene Symbionts: Insights into the Ecological Lifestyle of Nod-Independent Photosynthetic Bradyrhizobia

Cited by 30 publications

References 59 publications

Preferential Association of Endophytic Bradyrhizobia with Different Rice Cultivars and Its Implications for Rice Endophyte Evolution

Preferential Association of Endophytic Bradyrhizobia with Different Rice Cultivars and Its Implications for Rice Endophyte Evolution

Rhizobium–legume symbiosis in the absence of Nod factors: two possible scenarios with or without the T3SS

Genome Analysis Suggests that the Soil Oligotrophic Bacterium Agromonas oligotrophica (Bradyrhizobium oligotrophicum) Is a Nitrogen-Fixing Symbiont of Aeschynomene indica

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