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Evolution of symbiotic bacteria within the extra- and intra-cellular plant compartments: experimental evidence and mathematical simulation (Mini-review)

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Abstract

Using the example of nodular legume-rhizobia symbiosis (LRS), we discuss the evolution in plant micro-symbionts of mutualistic traits that are apparently host-beneficial and therefore the products of inter-species evolution. These traits include: in planta activation of N2 fixation machinery; exporting the products of nitrogenase reaction into the plant cells/tissues; and the terminal differentiation of bacteria into non-reproductive N2-fixing bacteroids. It seems probable that such adaptive traits evolved by natural selection within the populations of endosymbiotic bacteria that colonize the extra- and intra-cellular compartments provided by the hosts (i.e., infection threads and symbiosomes). This evolution would occur under the impacts of group (inter-deme, kin) selection pressures induced by the partners’ metabolic and regulatory feedbacks that ensure the high activity of symbiotic N2 fixation. These important feedbacks include: progressive allocation of C compounds into N2-fixing nodules; maintenance of micro-aerobic intracellular environments that are indispensable for intensive N2 fixation; and stringent control by the host over bacterial reproduction in planta. A computational simulation of the associated co-evolutionary processes reveals the trade-off between inter-species and individual species components of progressive and adaptive LRS evolution. This is expressed as a correlated increase of ecological efficiency, functional integrity and genotypic specificity of mutualistic symbiosis. Thus, the evolution of rhizobia in symbiosis may be represented by a progressive multi-level scenario based on increasing the dependency of bacteria on the host-provided nutrients accompanied by increasing complexity of the bacterial genomes and of the symbiosis-encoding gene networks.

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Acknowledgements

Our research is supported by RFBR (12-04-00409а), the Ministry of Education and Science of the Russian Federation (16.552.11.7085; 8056); NJB is Emeritus Fellow at the John Innes Centre, Norwich, UK.

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  1. All-Russia Research Institute for Agricultural Microbiology, Podbelsky Sh., 3, 196608, St.-Petersburg, Russia

    Nikolay A. Provorov, Anna V. Tsyganova, Viktor E. Tsyganov & Nikolay I. Vorobyov

  2. John Innes Centre, Norwich Research Park, Colney Lane, Norwich, NR4 7UH, UK

    Nicholas J. Brewin

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  1. Nikolay A. Provorov
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  2. Anna V. Tsyganova
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  3. Nicholas J. Brewin
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  4. Viktor E. Tsyganov
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Correspondence to Nikolay A. Provorov.

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Provorov, N.A., Tsyganova, A.V., Brewin, N.J. et al. Evolution of symbiotic bacteria within the extra- and intra-cellular plant compartments: experimental evidence and mathematical simulation (Mini-review). Symbiosis 58, 39–50 (2012). https://doi.org/10.1007/s13199-012-0220-0

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