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  • Review Article
  • Published:

Rhizobia: from saprophytes to endosymbionts

Nature Reviews Microbiology volume 16, pages 291–303 (2018)Cite this article

Subjects

Key Points

  • Root secretion and plant immunity are key factors in controlling the assembly of root-associated microbiotas of which rhizobia are key members

  • Rhizobia exist in soil and compete with the general microbiota before infecting legumes, typically through root hairs, and forming N2-fixing bacteroids

  • Rhizobia have complex pan-genomes. Some strains also have large plasmids or symbiosis islands, which are crucial for fitness, nodulation and N2 fixation

  • Rhizobia have specific host plants, which makes them excellent models for studying the mechanisms, timing and location of root colonization in host and non-host plants

  • Some legumes, such as members of the invert repeat lacking clade, produce up to several hundred antimicrobial peptides to control bacteroid cell division and development

  • Bacteroids receive carbon as dicarboxylates from legumes, and in exchange, they fix N2 in a low O2 environment and secrete ammonia to the plant. Bacteroids must balance electron flow to nitrogenase, lipids, polyhydroxybutyrate and O2, and coordinate this process with reductant production by the tricarboxylic acid (TCA) cycle

Abstract

Rhizobia are some of the best-studied plant microbiota. These oligotrophic Alphaproteobacteria or Betaproteobacteria form symbioses with their legume hosts. Rhizobia must exist in soil and compete with other members of the microbiota before infecting legumes and forming N2-fixing bacteroids. These dramatic lifestyle and developmental changes are underpinned by large genomes and even more complex pan-genomes, which encompass the whole population and are subject to rapid genetic exchange. The ability to respond to plant signals and chemoattractants and to colonize nutrient-rich roots are crucial for the competitive success of these bacteria. The availability of a large body of genomic, physiological, biochemical and ecological studies makes rhizobia unique models for investigating community interactions and plant colonization.

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Figure 1: Rhizobial genome organization.
Figure 2: Rhizobial attachment and colonization of legume roots.
Figure 3: Molecular mechanisms of plant–rhizobia signalling.
Figure 4: Nutrient exchange and regulation of bacteroid development.

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Acknowledgements

The authors thank T. Haskett and B. Jorrín for help with figures and A. East and A. Tkacz for comments on the manuscript. This work was supported by the Biotechnology and Biological Sciences Research Council [grant numbers BB/K001868/1, BB/K001868/2, BB/J007749/1, BB/J007749/2, BB/K006134/1, BB/L011484/1, BB/N003608/1, BB/N013387/1].

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Authors and Affiliations

  1. Department of Plant Sciences, University of Oxford, South Parks Road, Oxford, OX1 3RB, UK

    Philip Poole & Vinoy Ramachandran

  2. Centre for Rhizobium Studies, School of Veterinary and Life Sciences, Murdoch University, South Street, Perth, 6150, WA, Australia

    Jason Terpolilli

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P.P., V.R. and J.T. substantially contributed to the discussion of content, wrote the article and reviewed and edited the manuscript before submission.

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Correspondence to Philip Poole.

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Glossary

Root cortex

The outermost layer of the plant root that lies between the epidermal cells on the outside and vascular cells on the inside.

Pan-genomes

The complete set of genes present in the members of a certain group; for example, the sum of all genes found in bacterial strains belonging to a species.

Saprophytes

Organisms that live on dead and decaying organic matter.

Oligotrophic lifestyle

The usage of a broad range of carbon sources in a nutritionally limited environment.

Lipochitooligosaccharide

(LCO). Microbial signalling molecule with a 1,4-linked N-acetylglucosamine backbone that induces nodule formation. Species-dependent side decorations determine plant specificity.

Integrative and conjugative elements

(ICEs). ICEs are mobile genetic elements that can excise from the host chromosome to form a plasmid-like entity capable of catalysing its own transfer through conjugation. In recipient cells, ICEs integrate site-specifically into the chromosome, usually at conserved sites within an aminoacyl-tRNA gene.

Phytoalexins

Antimicrobial compounds produced by plants to protect them from pathogens.

Endoreduplication

Repeated cycles of DNA replication without cell division, which leads to extensive amplification of the entire genome.

Nodule senescence

Old nodules cease N2 fixation, and viable rhizobia are released back into the soil. In terminally differentiated rhizobia (for example, bacteroids from IRLC legumes), only undifferentiated bacteria from infection threads will be viable.

Exergonic reaction

A chemical reaction that releases free energy.

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Poole, P., Ramachandran, V. & Terpolilli, J. Rhizobia: from saprophytes to endosymbionts. Nat Rev Microbiol 16, 291–303 (2018). https://doi.org/10.1038/nrmicro.2017.171

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