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other·preclinical research, biomedical research, agriculture, animal science·PMC10316601

Rhizobial nitrogen fixation efficiency shapes endosphere bacterial communities and Medicago truncatula host growth

Microbiome · 15 authors, 6 centres

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TL;DR

This preclinical study inoculated the model legume Medicago truncatula with Sinorhizobium strains varying in nitrogen-fixing efficiency across three soil types to assess impacts on microbiome recruitment and plant nutrition. High-efficiency rhizobial strains reshaped endosphere bacterial community structure—particularly enriching Actinobacteria—and enhanced plant nutrient uptake and growth, with effects modulated by soil type.

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This preclinical laboratory study examined how rhizobial nitrogen-fixing efficiency modulates plant growth, nutrition, and microbiome recruitment in Medicago truncatula across three agriculturally relevant soil types. The authors inoculated plants with Sinorhizobium meliloti or S. medicae strains differing in nodulation and nitrogen-fixation efficiency, alongside mock-inoculated controls. High-efficiency symbiosis enriched Actinobacteria in the endosphere and increased shoot levels of nitrogen, carbon, magnesium, phosphorus, potassium, and calcium. The plant actively sanctions low-efficiency strains via nodule senescence.

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other

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preclinical research

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ORIGINAL PAPER

PMC10316601

Rhizobial nitrogen fixation efficiency shapes endosphere bacterial communities and Medicago truncatula host growth

Microbiome

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ABSTRACT

Background Despite the knowledge that the soil–plant–microbiome nexus is shaped by interactions amongst its members, very little is known about how individual symbioses regulate this shaping. Even less is known about how the agriculturally important symbiosis of nitrogen-fixing rhizobia with legumes is impacted according to soil type, yet this knowledge is crucial if we are to harness or improve it. We asked how the plant, soil and microbiome are modulated by symbiosis between the model legume Medicago truncatula and different strains of Sinorhizobium meliloti or Sinorhizobium medicae whose nitrogen-fixing efficiency varies, in three distinct soil types that differ in nutrient fertility, to examine the role of the soil environment upon the plant–microbe interaction during nodulation. Results The outcome of symbiosis results in installment of a potentially beneficial microbiome that leads to increased nutrient uptake that is not simply proportional to soil nutrient abundance. A number of soil edaphic factors including Zn and Mo, and not just the classical N/P/K nutrients, group with microbial community changes, and alterations in the microbiome can be seen across different soil fertility types. Root endosphere emerged as the plant microhabitat more affected by this rhizobial efficiency-driven community reshaping, manifested by the accumulation of members of the phylum Actinobacteria. The plant in turn plays an active role in regulating its root community, including sanctioning low nitrogen efficiency rhizobial strains, leading to nodule senescence in particular plant–soil–rhizobia strain combinations. Conclusions The microbiome–soil–rhizobial dynamic strongly influences plant nutrient uptake and growth, with the endosphere and rhizosphere shaped differentially according to plant–rhizobial interactions with strains that vary in nitrogen-fixing efficiency levels. These results open up the possibility to select inoculation partners best suited for plant, soil type and microbial community. Video Abstract Supplementary Information The online version contains supplementary material available at 10.1186/s40168-023-01592-0.

CITATION EXPORT

Beatriz Lagunas, Luke Richards, Chrysi Sergaki et al.. Rhizobial nitrogen fixation efficiency shapes endosphere bacterial communities and Medicago truncatula host growth. Microbiome. (2023). https://doi.org/10.1186/s40168-023-01592-0

AUTHORS

15 · 6 CENTRES

Beatriz Lagunas, Luke Richards, Chrysi Sergaki, Jamie Burgess, Alonso Javier Pardal, Rana M. F. Hussain, Bethany L. Richmond, Laura Baxter, Proyash Roy, Anastasia Pakidi, Gina Stovold, Saúl Vázquez, Sascha Ott, Patrick Schäfer, Miriam L. Gifford

1grid.7372.10000 0000 8809 1613School of Life Sciences, University of Warwick, Coventry, CV4 7AL UK
2grid.7372.10000 0000 8809 1613Warwick Medical School, University of Warwick, Coventry, CV4 7AL UK
3grid.8198.80000 0001 1498 6059Department of Genetic Engineering & Biotechnology, University of Dhaka, Dhaka, Bangladesh
4grid.4563.40000 0004 1936 8868University of Nottingham, Sutton Bonington Campus, Sutton Bonington, Nottingham, LE12 5RD UK
5grid.8664.c0000 0001 2165 8627Present Address: Institute of Phytopathology, Research Centre for BioSystems, Land Use and Nutrition, Justus Liebig University, Giessen, 35392 Germany
6grid.7372.10000 0000 8809 1613Warwick Integrative Synthetic Biology Centre, University of Warwick, Coventry, CV47AL UK