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The Genome of Rhizobium Leguminosarum Has Recognizable Core and Accessory Components

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The Genome of Rhizobium Leguminosarum Has Recognizable Core and Accessory Components This is a repository copy of The genome of Rhizobium leguminosarum has recognizable core and accessory components. White Rose Research Online URL for this paper: https://eprints.whiterose.ac.uk/1739/ Article: Young, J P W orcid.org/0000-0001-5259-4830, Crossman, L C, Johnston, A W B et al. (29 more authors) (2006) The genome of Rhizobium leguminosarum has recognizable core and accessory components. Genome biology. R34. -. ISSN 1474-760X https://doi.org/10.1186/gb-2006-7-4-r34 Reuse Items deposited in White Rose Research Online are protected by copyright, with all rights reserved unless indicated otherwise. They may be downloaded and/or printed for private study, or other acts as permitted by national copyright laws. The publisher or other rights holders may allow further reproduction and re-use of the full text version. 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[email protected] https://eprints.whiterose.ac.uk/ Research2006YoungetVolume al. 7, Issue 4, Article R34 Open Access The genome of Rhizobium leguminosarum has recognizable core and comment accessory components J Peter W Young*, Lisa C Crossman†, Andrew WB Johnston‡, Nicholas R Thomson†, Zara F Ghazoui*, Katherine H Hull*, Margaret Wexler‡, Andrew RJ Curson‡, Jonathan D Todd‡, Philip S Poole§, Tim H Mauchline§, Alison K East§, Michael A Quail†, Carol Churcher†, Claire Arrowsmith†, Inna Cherevach†, Tracey Chillingworth†, Kay Clarke†, reviews Ann Cronin†, Paul Davis†, Audrey Fraser†, Zahra Hance†, Heidi Hauser†, Kay Jagels†, Sharon Moule†, Karen Mungall†, Halina Norbertczak†, Ester Rabbinowitsch†, Mandy Sanders†, Mark Simmonds†, Sally Whitehead† and Julian Parkhill† reports Addresses: *Department of Biology, University of York, York, UK. †The Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Cambridge, UK. ‡School of Biological Sciences, University of East Anglia, Norwich, UK. §School of Biological Sciences, University of Reading, Reading, UK. Correspondence: J Peter W Young. Email: [email protected] deposited research Published: 26 April 2006 Received: 3 January 2006 Revised: 20 February 2006 Genome Biology 2006, 7:R34 (doi:10.1186/gb-2006-7-4-r34) Accepted: 22 March 2006 The electronic version of this article is the complete one and can be found online at http://genomebiology.com/2006/7/4/R34 © 2006 Young et al.; licensee BioMed Central Ltd. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. The<p>Therevealing Rhizobium genome a 'core' leguminosarum sequenceand an 'accessory' of the genomeα-proteobacterial component.</p> N2-fixing symbiont of legumes, <it>Rhizobium leguminosarum</it>, is described, research refereed Abstract Background: Rhizobium leguminosarum is an α-proteobacterial N2-fixing symbiont of legumes that has been the subject of more than a thousand publications. Genes for the symbiotic interaction with plants are well studied, but the adaptations that allow survival and growth in the soil environment are poorly understood. We have sequenced the genome of R. leguminosarum biovar viciae strain 3841. interactions Results: The 7.75 Mb genome comprises a circular chromosome and six circular plasmids, with 61% G+C overall. All three rRNA operons and 52 tRNA genes are on the chromosome; essential protein-encoding genes are largely chromosomal, but most functional classes occur on plasmids as well. Of the 7,263 protein-encoding genes, 2,056 had orthologs in each of three related genomes (Agrobacterium tumefaciens, Sinorhizobium meliloti, and Mesorhizobium loti), and these genes were over- represented in the chromosome and had above average G+C. Most supported the rRNA-based phylogeny, confirming A. tumefaciens to be the closest among these relatives, but 347 genes were incompatible with this phylogeny; these were scattered throughout the genome but were over-represented on the plasmids. An unexpectedly large number of genes were shared by all three rhizobia but were missing from A. tumefaciens. information Conclusion: Overall, the genome can be considered to have two main components: a 'core', which is higher in G+C, is mostly chromosomal, is shared with related organisms, and has a consistent phylogeny; and an 'accessory' component, which is sporadic in distribution, lower in G+C, and located on the plasmids and chromosomal islands. The accessory genome has a different nucleotide composition from the core despite a long history of coexistence. Genome Biology 2006, 7:R34 R34.2 Genome Biology 2006, Volume 7, Issue 4, Article R34 Young et al. http://genomebiology.com/2006/7/4/R34 Background A more important distinction, in our view, is between 'core' The symbiosis between legumes and N2-fixing bacteria and 'accessory' genomes. This distinction predates the (rhizobia) is of huge agronomic benefit, allowing many crops genomics era; indeed, it has been discussed for more than a to be grown without N fertilizer. It is a sophisticated example quarter of a century. Davey and Reanney [18] contrasted 'uni- of coupled development between bacteria and higher plants, versal' and 'peripheral' genes, or 'conserved' and 'experimen- culminating in the organogenesis of root nodules [1]. There tal' DNA. Campbell [19] wrote of 'euchromosomal' and have been many genetic analyses of rhizobia, notably of 'accessory' DNA and explained how gene transfer was impor- Sinorhizobium meliloti (the symbiont of alfalfa), Bradyrhizo- tant in shaping the latter. He pointed out that genes carried by bium japonicum (soybean), and Rhizobium leguminosarum, plasmids or transposons were 'available to all cells of the spe- which has biovars that nodulate peas and broad beans (biovar cies, though not actually present in them' and 'should typi- viciae), clovers (biovar trifolii), or kidney beans (biovar pha- cally be genes that are needed occasionally rather than seoli). continually under natural conditions'. Furthermore, the need to function in different genetic backgrounds meant that 'evo- The Rhizobiales, an α-proteobacterial order that also includes lution must limit the development of specific interactions mammalian pathogens Bartonella and Brucella and phy- between their products and those of universal genes'. This topathogenic Agrobacterium, have diverse genomic architec- would tend to sharpen the separation between the euchromo- tures. The single chromosome of Bartonella is small (1.6-1.9 somal and accessory gene pools, although transfer between Mb [2]), but the larger (approximately 3.3 Mb) Brucella them would remain possible. genomes comprise two circles [3-5]. Genomes of the plant- associated bacteria are larger still; that of A. tumefaciens is The expectation is that particular accessory genes will often about 5.6 Mb, with one circular and one linear chromosome, be absent from closely related strains or species, and as com- plus two native plasmids [6,7]. To date, three rhizobial parative data became available such genes were indeed found genomes have been sequenced. S. meliloti 1021 has a 3.5 Mb in large numbers [20]. They often had a nucleotide composi- chromosome plus two megaplasmids, namely pSymA (1.35 tion different from the bulk of the genome, and this property Mb) and pSymB (1.68 Mb), with the former having genes for had previously been interpreted as evidence that they were nodulation (nod) and symbiotic N2 fixation (nif and fix) [8]. 'foreign' genes [21]. This is plausible because nucleotide com- In contrast, the symbiosis genes of Mesorhizobium loti position can be quite different between distantly related bac- MAFF303099 (which nodulates Lotus) and of B. japonicum teria even though it is relatively consistent within genomes USDA110 are on chromosomal 'symbiosis islands', with the [22]. This pattern is thought to reflect biased mutation rates chromosome of the latter (9.1 Mb) being among the largest that tend to create a distinctive composition for each genome yet known in bacteria [9,10]. [23], and if these 'foreign' genes remained long enough they would gradually ameliorate toward the local composition Rhizobium leguminosarum has yet another genomic archi- [20]. Unusual composition is not an infallible indicator of tecture: one circular chromosome and several large plasmids, recent acquisition [24], although there is a strong tendency the plasmid portfolio varying markedly among isolates in for genes acquired by Escherichia coli to be A+T rich [25]. terms of sizes, numbers, and incompatibility groups [11-14]. Amelioration will be expected if genes of unusual composi- The subject of the present study, R. leguminosarum biovar tion are normal genes that reflect the composition of some viciae (Rlv) strain 3841 (a spontaneous streptomycin-resist- distant donor species [20], but an alternative explanation is ant mutant of field isolate 300 [15,16]), has six large plas- that they represent a class of genes that maintain a distinct mids; pRL10 is the pSym (symbiosis plasmid) and pRL7 and composition. Daubin and coworkers [26] pointed out that pRL8 are transferable by conjugation [17]. phage and insertion sequences are generally A+T rich, and suggested that many of the apparently
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