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Polyphasic Taxonomic Revision of the Ralstonia Solanacearum Species Complex

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Polyphasic Taxonomic Revision of the Ralstonia Solanacearum Species Complex International Journal of Systematic and Evolutionary Microbiology (2014), 64, 3087–3103 DOI 10.1099/ijs.0.066712-0 Polyphasic taxonomic revision of the Ralstonia solanacearum species complex: proposal to emend the descriptions of Ralstonia solanacearum and Ralstonia syzygii and reclassify current R. syzygii strains as Ralstonia syzygii subsp. syzygii subsp. nov., R. solanacearum phylotype IV strains as Ralstonia syzygii subsp. indonesiensis subsp. nov., banana blood disease bacterium strains as Ralstonia syzygii subsp. celebesensis subsp. nov. and R. solanacearum phylotype I and III strains as Ralstonia pseudosolanacearum sp. nov. Irda Safni,13 Ilse Cleenwerck,2 Paul De Vos,2 Mark Fegan,14 Lindsay Sly1 and Ulrike Kappler1 Correspondence 1School of Chemistry and Molecular Biosciences, Faculty of Science, University of Queensland, Lindsay Sly St Lucia, Queensland 4072, Australia [email protected] 2BCCM/LMG Bacteria Collection, Laboratory of Microbiology, Ghent University, Ulrike Kappler K. L. Ledeganckstraat 35, B-9000 Ghent, Belgium [email protected] The Ralstonia solanacearum species complex has long been recognized as a group of phenotypically diverse strains that can be subdivided into four phylotypes. Using a polyphasic taxonomic approach on an extensive set of strains, this study provides evidence for a taxonomic and nomenclatural revision of members of this complex. Data obtained from phylogenetic analysis of 16S-23S rRNA ITS gene sequences, 16S–23S rRNA intergenic spacer (ITS) region sequences and partial endoglucanase (egl) gene sequences and DNA–DNA hybridizations demonstrate that the R. solanacearum species complex comprises three genospecies. One of these includes the type strain of Ralstonia solanacearum and consists of strains of R. solanacearum phylotype II only. The second genospecies includes the type strain of Ralstonia syzygii and contains only phylotype IV strains. This genospecies is subdivided into three distinct groups, namely R. syzygii, the causal agent of Sumatra disease on clove trees in Indonesia, R. solanacearum phylotype IV strains isolated from different host plants mostly from Indonesia, and strains of the blood disease bacterium (BDB), the causal agent of the banana blood disease, a bacterial wilt disease in Indonesia that affects bananas and plantains. The last genospecies is composed of R. solanacearum strains that belong to phylotypes I and III. As these genospecies are also supported by phenotypic data that allow the differentiation of the three genospecies, the following taxonomic proposals are made: emendation of the descriptions of Ralstonia solanacearum and Ralstonia syzygii and descriptions of Ralstonia syzygii subsp. nov. (type strain 3Present address: Faculty of Agriculture, University of Sumatra Utara, Medan, 20155 North Sumatra, Indonesia. 4Present address: Department of Environment and Primary Industries, 5 Ring Rd, La Trobe University, Bundoora, Victoria 3083, Australia. Abbreviations: BDB, blood disease bacterium; ITS, intergenic spacer; MLSA, multilocus sequence analysis. The GenBank/EMBL/DDBJ accession numbers for the sequences determined in this study are KC757031–KC757076 and KC820937–KC820940 (16S- 23S rRNA ITS gene), KC756969–KC757029 (16S–23S rRNA gene ITS) and KC757078–KC757122 and KC820936 (egl gene), as detailed in Table S1. Nine supplementary tables and three supplementary figures are available with the online version of this paper. 066712 G 2014 IUMS Printed in Great Britain 3087 I. Safni and others R 001T5LMG 10661T5DSM 7385T) for the current R. syzygii strains, Ralstonia syzygii subsp. indonesiensis subsp. nov. (type strain UQRS 464T5LMG 27703T5DSM 27478T) for the current R. solanacearum phylotype IV strains, Ralstonia syzygii subsp. celebesensis subsp. nov. (type strain UQRS 627T5LMG 27706T5DSM 27477T) for the BDB strains and Ralstonia pseudosolanacearum sp. nov. (type strain UQRS 461T5LMG 9673T5NCPPB 1029T) for the strains of R. solanacearum phylotypes I and III. INTRODUCTION the causal agent of banana blood disease, which is one of the most destructive bacterial wilt diseases affecting bananas Ralstonia solanacearum is a soil-borne pathogen that causes (Musa acuminata) and plantains (Musa balbisiana6acumi- lethal vascular wilt diseases of over 200 plant species from nata) in Indonesia (Eden-Green, 1994). BDB was probably more than 50 families including solanaceous vegetable first isolated in the early 20th century and named crops, banana, ginger, custard apple, peanut, eucalyptus and ¨ many other crop plants (Hayward, 1994; Kelman, 1953). ‘Pseudomonas celebensis’(Gaumann, 1921). However, this Due to its lethality, persistence, wide host range and very name was not included in the Approved Lists of Bacterial broad geographical distribution, R. solanacearum is one of Names and, as type or reference cultures of ‘P. celebensis’no the most devastating bacterial plant pathogens known longer exist, the name has no standing in nomenclature. The (Elphinstone, 2005). bacterium is currently referred to as BDB and classified as a member of phylotype IV of the R. solanacearum species R. solanacearum is a heterogeneous species, as evidenced by complex. its large host range, pathogenic specialization and cultural and physiological properties, as well as its phylogeny Recently, Wicker et al. (2012) further subdivided the R. (Hayward, 2000). Following its discovery, R. solanacearum solanacearum species complex into eight clades based on was originally classified as a member of the genus ‘Bac- multilocus sequence analysis (MLSA). Phylotypes I and III terium’ (Smith, 1896). The application of DNA-based were each contained in a single clade (1 and 6, respec- methods eventually resulted in its transfer to the genus tively), while phylotype II consisted of four separate clades Burkholderia (Yabuuchi et al., 1992) and then to the genus (2–5). Phylotype IV was composed of two clades (7 and 8), Ralstonia (Yabuuchi et al., 1995). Despite being classified as with clade 7 including BDB and R. solanacearum phylotype a single species, it has been accepted since the 1980s that IV strains and clade 8 containing R. syzygii strains and R. different strains of R. solanacearum may show DNA–DNA solanacearum phylotype IV strains isolated from clove relatedness values below 70 % (De Vos, 1980; Palleroni & trees. Phylotype IV was reported to be the most divergent Doudoroff, 1971) and therefore might be members of and ancestral phylotype, although ongoing diversification different species. As a result, the term ‘species complex’ was observed within phylotypes I, II and III (Wicker et al., (Gillings & Fahy, 1994), referring to ‘a cluster of closely 2012). In addition, the MLSA study indicated that phylo- related bacteria whose individual members may represent types I and III are more closely related to each other than more than one species’ (Fegan & Prior, 2006), has been to phylotypes II and IV, and the dendrograms also clearly applied to R. solanacearum. documented the close relationship between the phylotype IV strains. Within the R. solanacearum species complex, four phylo- types are recognized (Prior & Fegan, 2005) that can be Whole-genome sequences of several representatives of the distinguished based on the sequences of their 16S–23S R. solanacearum species complex have become available in rRNA gene intergenic spacer (ITS) region and the hrpB and recent years, and these include three representatives of egl genes as well as comparative genomic hybridization phylotype I (GMI1000, Y45, FQY-4), six phylotype II (Fegan & Prior, 2005; Guidot et al., 2007). Phylotypes I, II strains (IIA: K60; CFBP 2957; IIB: IPO1609, UW 551, and III are composed of strains mainly from Asia, America Po82, Molk2) and one representative each of phylotype III and Africa, respectively, and surrounding islands, while (CMR15) and the three main phylotype IV groups (R. phylotype IV is primarily composed of strains from Indo- solanacearum, PSI 07; R. syzygii, R 24; BDB, R 229) (see nesia and some isolates from Japan, Australia and the Table S2, available in the online Supplementary Material). Philippines. Phylotype IV is the most diverse group, as it Additional genomes have been sequenced but are not pub- consists of strains assigned to R. solanacearum, Ralstonia licly available at present (https://www.genoscope.cns.fr/agc/ syzygii and the blood disease bacterium (BDB). R. syzygii is microscope/about/collabprojects.php). All complete genomes the causal agent of the Sumatra disease of clove trees in consist of two replicative units, a chromosome of approxi- Indonesia (Roberts et al., 1990) and its status as a separate mately 3.7 Mb and a megaplasmid of 1.6–2.3 Mb, which species in the genus Ralstonia hasbeenproven(Vaneechoutte together encode approximately 5000 proteins. Comparative et al., 2004). However, it is also clearly a member of the R. studies found that each genome contained between 400 and solanacearum species complex (Taghavi et al., 1996). BDB is 600 unique genes, regardless of whether or not the genomes 3088 International Journal of Systematic and Evolutionary Microbiology 64 Taxonomic revision of the R. solanacearum species complex originated from the same phylotype (Remenant et al., 2010, and egl sequences included data for strains with published genome 2011). sequences as well as sequences deposited in GenBank as part of previous studies (Tables S1, S2 and S5). Recent work comparing eight complete genome sequences Strains were grown aerobically at 28 uC. For routine maintenance, from R. solanacearum (one from
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