Microevolution, speciation and macroevolution in rhizobia: Genomic mechanisms and selective patterns

Nodule bacteria (rhizobia), N2-fixing symbionts of leguminous plants, represent an excellent model to study the fundamental issues of evolutionary biology, including the tradeoff between microevolution, speciation, and macroevolution, which remains poorly understood for free-living organisms. Taxono...

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Main Authors: Nikolay A. Provorov, Evgeny E. Andronov, Anastasiia K. Kimeklis, Olga P. Onishchuk, Anna A. Igolkina, Evgeny S. Karasev
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-10-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2022.1026943/full
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author Nikolay A. Provorov
Evgeny E. Andronov
Evgeny E. Andronov
Anastasiia K. Kimeklis
Anastasiia K. Kimeklis
Olga P. Onishchuk
Anna A. Igolkina
Evgeny S. Karasev
author_facet Nikolay A. Provorov
Evgeny E. Andronov
Evgeny E. Andronov
Anastasiia K. Kimeklis
Anastasiia K. Kimeklis
Olga P. Onishchuk
Anna A. Igolkina
Evgeny S. Karasev
author_sort Nikolay A. Provorov
collection DOAJ
description Nodule bacteria (rhizobia), N2-fixing symbionts of leguminous plants, represent an excellent model to study the fundamental issues of evolutionary biology, including the tradeoff between microevolution, speciation, and macroevolution, which remains poorly understood for free-living organisms. Taxonomically, rhizobia are extremely diverse: they are represented by nearly a dozen families of α-proteobacteria (Rhizobiales) and by some β-proteobacteria. Their genomes are composed of core parts, including house-keeping genes (hkg), and of accessory parts, including symbiotically specialized (sym) genes. In multipartite genomes of evolutionary advanced fast-growing species (Rhizobiaceae), sym genes are clustered on extra-chromosomal replicons (megaplasmids, chromids), facilitating gene transfer in plant-associated microbial communities. In this review, we demonstrate that in rhizobia, microevolution and speciation involve different genomic and ecological mechanisms: the first one is based on the diversification of sym genes occurring under the impacts of host-induced natural selection (including its disruptive, frequency-dependent and group forms); the second one—on the diversification of hkgs under the impacts of unknown factors. By contrast, macroevolution represents the polyphyletic origin of super-species taxa, which are dependent on the transfer of sym genes from rhizobia to various soil-borne bacteria. Since the expression of newly acquired sym genes on foreign genomic backgrounds is usually restricted, conversion of resulted recombinants into the novel rhizobia species involves post-transfer genetic changes. They are presumably supported by host-induced selective processes resulting in the sequential derepression of nod genes responsible for nodulation and of nif/fix genes responsible for symbiotic N2 fixation.
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spelling doaj.art-e862deaa231f4ecab06a3d0a0ed2412e2022-12-22T02:35:46ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2022-10-011310.3389/fpls.2022.10269431026943Microevolution, speciation and macroevolution in rhizobia: Genomic mechanisms and selective patternsNikolay A. Provorov0Evgeny E. Andronov1Evgeny E. Andronov2Anastasiia K. Kimeklis3Anastasiia K. Kimeklis4Olga P. Onishchuk5Anna A. Igolkina6Evgeny S. Karasev7Laboratory of Microbiological Monitoring and Bioremediation of Soils, All-Russian Research Institute for Agricultural Microbiology, Pushkin, RussiaLaboratory of Microbiological Monitoring and Bioremediation of Soils, All-Russian Research Institute for Agricultural Microbiology, Pushkin, RussiaLaboratory of Soil Biology and Biochemistry, V.V. Dokuchaev Soil Science Institute, Moscow, RussiaLaboratory of Microbiological Monitoring and Bioremediation of Soils, All-Russian Research Institute for Agricultural Microbiology, Pushkin, RussiaDepartment of Applied Ecology, St. Petersburg State University, Saint-Petersburg, RussiaLaboratory of Microbiological Monitoring and Bioremediation of Soils, All-Russian Research Institute for Agricultural Microbiology, Pushkin, RussiaGregor Mendel Institute, Austrian Academy of Sciences, Vienna BioCenter, Vienna, AustriaLaboratory of Microbiological Monitoring and Bioremediation of Soils, All-Russian Research Institute for Agricultural Microbiology, Pushkin, RussiaNodule bacteria (rhizobia), N2-fixing symbionts of leguminous plants, represent an excellent model to study the fundamental issues of evolutionary biology, including the tradeoff between microevolution, speciation, and macroevolution, which remains poorly understood for free-living organisms. Taxonomically, rhizobia are extremely diverse: they are represented by nearly a dozen families of α-proteobacteria (Rhizobiales) and by some β-proteobacteria. Their genomes are composed of core parts, including house-keeping genes (hkg), and of accessory parts, including symbiotically specialized (sym) genes. In multipartite genomes of evolutionary advanced fast-growing species (Rhizobiaceae), sym genes are clustered on extra-chromosomal replicons (megaplasmids, chromids), facilitating gene transfer in plant-associated microbial communities. In this review, we demonstrate that in rhizobia, microevolution and speciation involve different genomic and ecological mechanisms: the first one is based on the diversification of sym genes occurring under the impacts of host-induced natural selection (including its disruptive, frequency-dependent and group forms); the second one—on the diversification of hkgs under the impacts of unknown factors. By contrast, macroevolution represents the polyphyletic origin of super-species taxa, which are dependent on the transfer of sym genes from rhizobia to various soil-borne bacteria. Since the expression of newly acquired sym genes on foreign genomic backgrounds is usually restricted, conversion of resulted recombinants into the novel rhizobia species involves post-transfer genetic changes. They are presumably supported by host-induced selective processes resulting in the sequential derepression of nod genes responsible for nodulation and of nif/fix genes responsible for symbiotic N2 fixation.https://www.frontiersin.org/articles/10.3389/fpls.2022.1026943/fullrhizobiamicro- and macro-evolutionspeciationnatural selectionplant–microbe symbiosesevolutionary genomics
spellingShingle Nikolay A. Provorov
Evgeny E. Andronov
Evgeny E. Andronov
Anastasiia K. Kimeklis
Anastasiia K. Kimeklis
Olga P. Onishchuk
Anna A. Igolkina
Evgeny S. Karasev
Microevolution, speciation and macroevolution in rhizobia: Genomic mechanisms and selective patterns
Frontiers in Plant Science
rhizobia
micro- and macro-evolution
speciation
natural selection
plant–microbe symbioses
evolutionary genomics
title Microevolution, speciation and macroevolution in rhizobia: Genomic mechanisms and selective patterns
title_full Microevolution, speciation and macroevolution in rhizobia: Genomic mechanisms and selective patterns
title_fullStr Microevolution, speciation and macroevolution in rhizobia: Genomic mechanisms and selective patterns
title_full_unstemmed Microevolution, speciation and macroevolution in rhizobia: Genomic mechanisms and selective patterns
title_short Microevolution, speciation and macroevolution in rhizobia: Genomic mechanisms and selective patterns
title_sort microevolution speciation and macroevolution in rhizobia genomic mechanisms and selective patterns
topic rhizobia
micro- and macro-evolution
speciation
natural selection
plant–microbe symbioses
evolutionary genomics
url https://www.frontiersin.org/articles/10.3389/fpls.2022.1026943/full
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