Defining the <i>Rhizobium leguminosarum</i> Species Complex

Bacteria currently included in <i>Rhizobium leguminosarum</i> 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 distinc...

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Main Authors: J. Peter W. Young, Sara Moeskjær, Alexey Afonin, Praveen Rahi, Marta Maluk, Euan K. James, Maria Izabel A. Cavassim, M. Harun-or Rashid, Aregu Amsalu Aserse, Benjamin J. Perry, En Tao Wang, Encarna Velázquez, Evgeny E. Andronov, Anastasia Tampakaki, José David Flores Félix, Raúl Rivas González, Sameh H. Youseif, Marc Lepetit, Stéphane Boivin, Beatriz Jorrin, Gregory J. Kenicer, Álvaro Peix, Michael F. Hynes, Martha Helena Ramírez-Bahena, Arvind Gulati, Chang-Fu Tian
Format: Article
Language:English
Published: MDPI AG 2021-01-01
Series:Genes
Subjects:
Online Access:https://www.mdpi.com/2073-4425/12/1/111
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author J. Peter W. Young
Sara Moeskjær
Alexey Afonin
Praveen Rahi
Marta Maluk
Euan K. James
Maria Izabel A. Cavassim
M. Harun-or Rashid
Aregu Amsalu Aserse
Benjamin J. Perry
En Tao Wang
Encarna Velázquez
Evgeny E. Andronov
Anastasia Tampakaki
José David Flores Félix
Raúl Rivas González
Sameh H. Youseif
Marc Lepetit
Stéphane Boivin
Beatriz Jorrin
Gregory J. Kenicer
Álvaro Peix
Michael F. Hynes
Martha Helena Ramírez-Bahena
Arvind Gulati
Chang-Fu Tian
spellingShingle J. Peter W. Young
Sara Moeskjær
Alexey Afonin
Praveen Rahi
Marta Maluk
Euan K. James
Maria Izabel A. Cavassim
M. Harun-or Rashid
Aregu Amsalu Aserse
Benjamin J. Perry
En Tao Wang
Encarna Velázquez
Evgeny E. Andronov
Anastasia Tampakaki
José David Flores Félix
Raúl Rivas González
Sameh H. Youseif
Marc Lepetit
Stéphane Boivin
Beatriz Jorrin
Gregory J. Kenicer
Álvaro Peix
Michael F. Hynes
Martha Helena Ramírez-Bahena
Arvind Gulati
Chang-Fu Tian
Defining the <i>Rhizobium leguminosarum</i> Species Complex
Genes
<i>Rhizobium</i>
species complex
bacterial taxonomy
core genes
housekeeping genes
average nucleotide identity
author_facet J. Peter W. Young
Sara Moeskjær
Alexey Afonin
Praveen Rahi
Marta Maluk
Euan K. James
Maria Izabel A. Cavassim
M. Harun-or Rashid
Aregu Amsalu Aserse
Benjamin J. Perry
En Tao Wang
Encarna Velázquez
Evgeny E. Andronov
Anastasia Tampakaki
José David Flores Félix
Raúl Rivas González
Sameh H. Youseif
Marc Lepetit
Stéphane Boivin
Beatriz Jorrin
Gregory J. Kenicer
Álvaro Peix
Michael F. Hynes
Martha Helena Ramírez-Bahena
Arvind Gulati
Chang-Fu Tian
author_sort J. Peter W. Young
title Defining the <i>Rhizobium leguminosarum</i> Species Complex
title_short Defining the <i>Rhizobium leguminosarum</i> Species Complex
title_full Defining the <i>Rhizobium leguminosarum</i> Species Complex
title_fullStr Defining the <i>Rhizobium leguminosarum</i> Species Complex
title_full_unstemmed Defining the <i>Rhizobium leguminosarum</i> Species Complex
title_sort defining the <i>rhizobium leguminosarum</i> species complex
publisher MDPI AG
series Genes
issn 2073-4425
publishDate 2021-01-01
description Bacteria currently included in <i>Rhizobium leguminosarum</i> 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 <i>R. anhuiense</i>. 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: <i>R. laguerreae, R. sophorae, R. ruizarguesonis</i>, <i>“R. indicum”</i> and <i>R. leguminosarum</i> 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.
topic <i>Rhizobium</i>
species complex
bacterial taxonomy
core genes
housekeeping genes
average nucleotide identity
url https://www.mdpi.com/2073-4425/12/1/111
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spelling doaj-da942dadc3e04d80afc37120714afa6f2021-01-19T00:02:42ZengMDPI AGGenes2073-44252021-01-011211111110.3390/genes12010111Defining the <i>Rhizobium leguminosarum</i> Species ComplexJ. Peter W. Young0Sara Moeskjær1Alexey Afonin2Praveen Rahi3Marta Maluk4Euan K. James5Maria Izabel A. Cavassim6M. Harun-or Rashid7Aregu Amsalu Aserse8Benjamin J. Perry9En Tao Wang10Encarna Velázquez11Evgeny E. Andronov12Anastasia Tampakaki13José David Flores Félix14Raúl Rivas González15Sameh H. Youseif16Marc Lepetit17Stéphane Boivin18Beatriz Jorrin19Gregory J. Kenicer20Álvaro Peix21Michael F. Hynes22Martha Helena Ramírez-Bahena23Arvind Gulati24Chang-Fu Tian25Department of Biology, University of York, York YO10 5DD, UKDepartment of Molecular Biology and Genetics, Aarhus University, 8000 Aarhus, DenmarkLaboratory for Genetics of Plant-Microbe Interactions, ARRIAM, Pushkin, 196608 Saint-Petersburg, RussiaNational Centre for Microbial Resource, National Centre for Cell Science, Pune-411007, IndiaEcological Sciences, James Hutton Institute, Invergowrie, Dundee DD2 5DA, UKEcological Sciences, James Hutton Institute, Invergowrie, Dundee DD2 5DA, UKDepartment of Ecology and Evolutionary Biology, University of California, Los Angeles, CA 90095, USABiotechnology Division, Bangladesh Institute of Nuclear Agriculture (BINA), Mymensingh-2202, BangladeshEcosystems and Environment Research Programme, Faculty of Biological and Environmental Sciences, University of Helsinki, FI-00014 Helsinki, FinlandDepartment of Microbiology and Immunology, University of Otago, Dunedin 9016, New ZealandDepartamento de Microbiología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Ciudad De México 11340, MexicoDepartamento 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, SpainDepartment of Microbial Monitoring, ARRIAM, Pushkin, 196608 Saint-Petersburg, RussiaDepartment of Crop Science, Agricultural University of Athens, Iera Odos 75, Votanikos, 11855 Athens, GreeceCICS-UBI—Health Sciences Research Centre, University of Beira Interior, 6201-506 Covilhã, PortugalDepartamento 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, SpainDepartment of Microbial Genetic Resources, National Gene Bank (NGB), Agricultural Research Center (ARC), Giza 12619, EgyptInstitut Sophia Agrobiotech, UMR INRAE 1355, Université Côte d'Azur, CNRS, 06903 Sophia Antipolis, FranceLaboratoire des Symbioses Tropicales et Méditerranéennes, UMR INRAE-IRD-CIRAD-UM2-SupAgro, Campus International de Baillarguet, TA-A82/J, CEDEX 05, 34398 Montpellier, FranceDepartment of Plant Sciences, University of Oxford, Oxford OX1 3RB, UKRoyal Botanic Garden Edinburgh, 20A Inverleith Row, Edinburgh EH3 5LR, UKInstituto de Recursos Naturales y Agrobiología de Salamanca (IRNASA-CSIC). Unidad Asociada Grupo de Interacción Planta-Microorganismo (Universidad de Salamanca-IRNASA-CSIC), 37008 Salamanca, SpainDepartment of Biological Sciences, University of Calgary, 2500 University Drive NW, Calgary, AB T2N 1N4, CanadaDepartamento de Didáctica de las Matemáticas y de las Ciencias Experimentales. Universidad de Salamanca, 37008 Salamanca, SpainMicrobial Prospection, CSIR-Institute of Himalayan Bioresource Technology, Palampur (H.P.) 176 061, IndiaState Key Laboratory of Agrobiotechnology, Rhizobium Research Center, and College of Biological Sciences, China Agricultural University, Beijing 100193, ChinaBacteria currently included in <i>Rhizobium leguminosarum</i> 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 <i>R. anhuiense</i>. 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: <i>R. laguerreae, R. sophorae, R. ruizarguesonis</i>, <i>“R. indicum”</i> and <i>R. leguminosarum</i> 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.https://www.mdpi.com/2073-4425/12/1/111<i>Rhizobium</i>species complexbacterial taxonomycore geneshousekeeping genesaverage nucleotide identity