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Article

Defining the Rhizobium leguminosarum Species Complex

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Department of Biology, University of York, York YO10 5DD, UK
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Department of Molecular Biology and Genetics, Aarhus University, 8000 Aarhus, Denmark
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Laboratory for Genetics of Plant-Microbe Interactions, ARRIAM, Pushkin, 196608 Saint-Petersburg, Russia
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National Centre for Microbial Resource, National Centre for Cell Science, Pune 411007, India
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Ecological Sciences, The James Hutton Institute, Invergowrie, Dundee DD2 5DA, UK
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Department of Ecology and Evolutionary Biology, University of California, Los Angeles, CA 90095, USA
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Biotechnology Division, Bangladesh Institute of Nuclear Agriculture (BINA), Mymensingh 2202, Bangladesh
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Ecosystems and Environment Research Programme, Faculty of Biological and Environmental Sciences, University of Helsinki, FI-00014 Helsinki, Finland
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Department of Microbiology and Immunology, University of Otago, Dunedin 9016, New Zealand
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Departamento de Microbiología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Ciudad De México 11340, Mexico
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Departamento de Microbiología y Genética, Universidad de Salamanca, Instituto Hispanoluso de Investigaciones Agrarias (CIALE), Unidad Asociada Grupo de Interacción planta-microorganismo (Universidad de Salamanca-IRNASA-CSIC), 37007 Salamanca, Spain
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Department of Microbial Monitoring, ARRIAM, Pushkin, 196608 Saint-Petersburg, Russia
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Department of Crop Science, Agricultural University of Athens, Iera Odos 75, Votanikos, 11855 Athens, Greece
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CICS-UBI—Health Sciences Research Centre, University of Beira Interior, 6201-506 Covilhã, Portugal
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Department of Microbial Genetic Resources, National Gene Bank (NGB), Agricultural Research Center (ARC), Giza 12619, Egypt
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Institut Sophia Agrobiotech, UMR INRAE 1355, Université Côte d’Azur, CNRS, 06903 Sophia Antipolis, France
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Laboratoire des Symbioses Tropicales et Méditerranéennes, UMR INRAE-IRD-CIRAD-UM2-SupAgro, Campus International de Baillarguet, TA-A82/J, CEDEX 05, 34398 Montpellier, France
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Department of Plant Sciences, University of Oxford, Oxford OX1 3RB, UK
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Royal Botanic Garden Edinburgh, 20A Inverleith Row, Edinburgh EH3 5LR, UK
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Instituto de Recursos Naturales y Agrobiología de Salamanca (IRNASA-CSIC), Unidad Asociada Grupo de Interacción Planta-Microorganismo (Universidad de Salamanca-IRNASA-CSIC), 37008 Salamanca, Spain
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Department of Biological Sciences, University of Calgary, 2500 University Drive NW, Calgary, AB T2N 1N4, Canada
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Departamento de Didáctica de las Matemáticas y de las Ciencias Experimentales. Universidad de Salamanca, 37008 Salamanca, Spain
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Microbial Prospection, CSIR-Institute of Himalayan Bioresource Technology, Palampur (H.P.) 176 061, India
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State Key Laboratory of Agrobiotechnology, Rhizobium Research Center, and College of Biological Sciences, China Agricultural University, Beijing 100193, China
*
Author to whom correspondence should be addressed.
Genes 2021, 12(1), 111; https://doi.org/10.3390/genes12010111
Received: 11 December 2020 / Revised: 8 January 2021 / Accepted: 13 January 2021 / Published: 18 January 2021
(This article belongs to the Special Issue Genes at Ten)
Bacteria currently included in Rhizobium leguminosarum are too diverse to be considered a single species, so we can refer to this as a species complex (the Rlc). We have found 429 publicly available genome sequences that fall within the Rlc and these show that the Rlc is a distinct entity, well separated from other species in the genus. Its sister taxon is R. anhuiense. We constructed a phylogeny based on concatenated sequences of 120 universal (core) genes, and calculated pairwise average nucleotide identity (ANI) between all genomes. From these analyses, we concluded that the Rlc includes 18 distinct genospecies, plus 7 unique strains that are not placed in these genospecies. Each genospecies is separated by a distinct gap in ANI values, usually at approximately 96% ANI, implying that it is a ‘natural’ unit. Five of the genospecies include the type strains of named species: R. laguerreae, R. sophorae, R. ruizarguesonis, “R. indicum” and R. leguminosarum itself. The 16S ribosomal RNA sequence is remarkably diverse within the Rlc, but does not distinguish the genospecies. Partial sequences of housekeeping genes, which have frequently been used to characterize isolate collections, can mostly be assigned unambiguously to a genospecies, but alleles within a genospecies do not always form a clade, so single genes are not a reliable guide to the true phylogeny of the strains. We conclude that access to a large number of genome sequences is a powerful tool for characterizing the diversity of bacteria, and that taxonomic conclusions should be based on all available genome sequences, not just those of type strains. View Full-Text
Keywords: Rhizobium; species complex; bacterial taxonomy; core genes; housekeeping genes; average nucleotide identity; speciation; genospecies Rhizobium; species complex; bacterial taxonomy; core genes; housekeeping genes; average nucleotide identity; speciation; genospecies
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MDPI and ACS Style

Young, J.P.W.; Moeskjær, S.; Afonin, A.; Rahi, P.; Maluk, M.; James, E.K.; Cavassim, M.I.A.; Rashid, M.H.-o.; Aserse, A.A.; Perry, B.J.; Wang, E.T.; Velázquez, E.; Andronov, E.E.; Tampakaki, A.; Flores Félix, J.D.; Rivas González, R.; Youseif, S.H.; Lepetit, M.; Boivin, S.; Jorrin, B.; Kenicer, G.J.; Peix, Á.; Hynes, M.F.; Ramírez-Bahena, M.H.; Gulati, A.; Tian, C.-F. Defining the Rhizobium leguminosarum Species Complex. Genes 2021, 12, 111. https://doi.org/10.3390/genes12010111

AMA Style

Young JPW, Moeskjær S, Afonin A, Rahi P, Maluk M, James EK, Cavassim MIA, Rashid MH-o, Aserse AA, Perry BJ, Wang ET, Velázquez E, Andronov EE, Tampakaki A, Flores Félix JD, Rivas González R, Youseif SH, Lepetit M, Boivin S, Jorrin B, Kenicer GJ, Peix Á, Hynes MF, Ramírez-Bahena MH, Gulati A, Tian C-F. Defining the Rhizobium leguminosarum Species Complex. Genes. 2021; 12(1):111. https://doi.org/10.3390/genes12010111

Chicago/Turabian Style

Young, J. P.W., Sara Moeskjær, Alexey Afonin, Praveen Rahi, Marta Maluk, Euan K. James, Maria I.A. Cavassim, M. H.-o. Rashid, Aregu A. Aserse, Benjamin J. Perry, En T. Wang, Encarna Velázquez, Evgeny E. Andronov, Anastasia Tampakaki, José D. Flores Félix, Raúl Rivas González, Sameh H. Youseif, Marc Lepetit, Stéphane Boivin, Beatriz Jorrin, Gregory J. Kenicer, Álvaro Peix, Michael F. Hynes, Martha H. Ramírez-Bahena, Arvind Gulati, and Chang-Fu Tian. 2021. "Defining the Rhizobium leguminosarum Species Complex" Genes 12, no. 1: 111. https://doi.org/10.3390/genes12010111

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