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Identification of the symbiosis island of Bradyrhizobium paxllaeri LMTR 21T.

ABSTRACT: The complete symbiosis island (SI) of Bradyrhizobium paxllaeri LMTR 21T, a mutualistic symbiont of the legume Phaseolus lunatus, was identified and analyzed. The SI was 646 kb in size, had lower G+C content than the genome average, and encoded not only nodulation and nitrogen fixation functions but also those for hydrogen uptake, vitamin and phytohormone biosynthesis, molybdenum transport, nonribosomal peptide synthesis, and type III secretion. Additionally, two divergent nodA genes were encoded in the SI.

SUBMITTER: Ormeno-Orrillo E

PROVIDER: S-EPMC7203309 | biostudies-literature | 2020 Jun

REPOSITORIES: biostudies-literature

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Identification of the symbiosis island of Bradyrhizobium paxllaeri LMTR 21<sup>T</sup>.

Ormeño-Orrillo Ernesto E Martínez-Romero Esperanza E Zúñiga-Dávila Doris D

Brazilian journal of microbiology : [publication of the Brazilian Society for Microbiology] 20191030 2

The complete symbiosis island (SI) of Bradyrhizobium paxllaeri LMTR 21<sup>T</sup>, a mutualistic symbiont of the legume Phaseolus lunatus, was identified and analyzed. The SI was 646 kb in size, had lower G+C content than the genome average, and encoded not only nodulation and nitrogen fixation functions but also those for hydrogen uptake, vitamin and phytohormone biosynthesis, molybdenum transport, nonribosomal peptide synthesis, and type III secretion. Additionally, two divergent nodA genes w ...[more]

PMID: 31667798

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Project description:The symbioses between leguminous plants and nitrogen-fixing bacteria known as rhizobia are well known for promoting plant growth and sustainably increasing soil nitrogen. Recent evidence indicates that hopanoids, a family of steroid-like lipids, promote Bradyrhizobium symbioses with tropical legumes. To characterize hopanoids in Bradyrhizobium symbiosis with soybean, we validated a recently published cumate-inducible hopanoid mutant of Bradyrhizobium diazoefficiens USDA110, Pcu-shc::∆shc. GC-MS analysis showed that this strain does not produce hopanoids without cumate induction, and under this condition, is impaired in growth in rich medium and under osmotic, temperature, and pH stress. In planta, Pcu-shc::∆shc is an inefficient soybean symbiont with significantly lower rates of nitrogen fixation and low survival within the host tissue. RNA-seq revealed that hopanoid loss reduces the expression of flagellar motility and chemotaxis-related genes, further confirmed by swim plate assays, and enhances the expression of genes related to nitrogen metabolism and protein secretion. These results suggest that hopanoids provide a significant fitness advantage to B. diazoefficiens in legume hosts and provide a foundation for future mechanistic studies of hopanoid function in protein secretion and motility.A major problem for global sustainability is feeding our exponentially growing human population while available arable land decreases. Harnessing the power of plant-beneficial microbes is a potential solution, including increasing our reliance on the symbioses of leguminous plants and nitrogen-fixing rhizobia. This study examines the role of hopanoid lipids in the symbiosis between Bradyrhizobium diazoefficiens USDA110, an important commercial inoculant strain, and its economically significant host soybean. Our research extends our knowledge of the functions of bacterial lipids in symbiosis to an agricultural context, which may one day help improve the practical applications of plant-beneficial microbes in agriculture.

Project description:BACKGROUND:Specialized interactions help structure communities, but persistence of specialized organisms is puzzling because a generalist can occupy more environments and partake in more beneficial interactions. The "Jack-of-all-trades is a master of none" hypothesis asserts that specialists persist because the fitness of a generalist utilizing a particular habitat is lower than that of a specialist adapted to that habitat. Yet, there are many reasons to expect that mutualists will generalize on partners.Plant-soil feedbacks help to structure plant and microbial communities, but how frequently are soil-based symbiotic mutualistic interactions sufficiently specialized to influence species distributions and community composition? To address this question, we quantified realized partner richness and phylogenetic breadth of four wild-grown native legumes (Lupinus bicolor, L. arboreus, Acmispon strigosus and A. heermannii) and performed inoculation trials to test the ability of two hosts (L. bicolor and A. strigosus) to nodulate (fundamental partner richness), benefit from (response specificity), and provide benefit to (effect specificity) 31 Bradyrhizobium genotypes. RESULTS:In the wild, each Lupinus species hosted a broader genetic range of Bradyrhizobium than did either Acmispon species, suggesting that Acmispon species are more specialized. In the greenhouse, however, L. bicolor and A. strigosus did not differ in fundamental association specificity: all inoculated genotypes nodulated both hosts. Nevertheless, A. strigosus exhibited more specificity, i.e., greater variation in its response to, and effect on, Bradyrhizobium genotypes. Lupinus bicolor benefited from a broader range of genotypes but averaged less benefit from each. Both hosts obtained more fitness benefit from symbionts isolated from conspecific hosts; those symbionts in turn gained greater fitness benefit from hosts of the same species from which they were isolated. CONCLUSIONS:This study affirmed two important tenets of evolutionary theory. First, as predicted by the Jack-of-all-trades is a master of none hypothesis, specialist A. strigosus obtained greater benefit from its beneficial symbionts than did generalist L. bicolor. Second, as predicted by coevolutionary theory, each test species performed better with partner genotypes isolated from conspecifics. Finally, positive fitness feedback between the tested hosts and symbionts suggests that positive plant-soil feedback could contribute to their patchy distributions in this system.

Dataset Information

Identification of the symbiosis island of Bradyrhizobium paxllaeri LMTR 21T.

Publications

Identification of the symbiosis island of Bradyrhizobium paxllaeri LMTR 21<sup>T</sup>.

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