Abstract
The current taxonomy of the order Xanthomonadales is highly problematic and no comprehensive phylogenomic studies have been completed that include the most divergent members within the order. In this work, we have completed a phylogenomic analysis of a wide range of genomes, five of which were sequenced for the first time for this work, representing the vast majority of the diversity within the order Xanthomonadales. Using comparative genomic techniques, we have identified a large number of conserved signature inserts/deletions (CSIs) that are specifically found in different groups of related organisms, at different taxonomic levels, within the order. Our phylogenetic analyses do not support a monophyletic grouping of the members of the order Xanthomonadales and no CSIs were identified which are uniquely shared by all sequenced species within this order. However, our work has identified 10 CSIs which are specific to all members of the family Xanthomonadaceae and an additional 10 and 11 CSIs that are specific to one of two phylogenetically well-defined clades within the family Xanthomonadaceae. On the basis of the identified CSIs and the results of phylogenomic analyses, we propose a new taxonomic framework for the order Xanthomonadales. In this proposal, the families Algiphilaceae and Solimonadaceae (Nevskiaceae), which do not branch with the other members of the order Xanthomonadales, are transferred into the order Nevskiales ord. nov. The remaining members of the order Xanthomonadales are divided into two families: the family Xanthomonadaceae, containing the genus Xanthomonas and its closest relatives, and a new family, Rhodanobacteraceae fam. nov., containing the genus Rhodanobacter and its closest relatives. Additionally, we have also emended descriptions of the order Lysobacterales, the family Lysobacteraceae, and the family Nevskiaceae to indicate that they are earlier synonyms of the order Xanthomonadales, the family Xanthomonadaceae, and the family Solimonadaceae, respectively.
This is a preview of subscription content, access via your institution.






Notes
The genus Steroidobacter does not branch monophyletically with the other members of the family Nevskiaceae in 16S rRNA gene based phylogenies. However, Steroidobacter is clearly distinct from the order Xanthomonadales and family Xanthomonadaceae in which it was previously placed. Its placement within the family Nevskiaceae is tentative until more detailed phylogenetic analysis can be completed for this genus.
References
Adeolu M, Gupta RS (2013) Phylogenomics and molecular signatures for the order Neisseriales: proposal for division of the order Neisseriales into the emended family Neisseriaceae and Chromobacteriaceae fam. nov. Anton Leeuw Int J G 104(1):1–24
Antunes A, Eder W, Fareleira P, Santos H, Huber R (2003) Salinisphaera shabanensis gen. nov., sp. nov., a novel, moderately halophilic bacterium from the brine–seawater interface of the Shaban Deep, Red Sea. Extremophiles 7(1):29–34
Bhandari V, Ahmod NZ, Shah HN, Gupta RS (2013) Molecular signatures for Bacillus species: demarcation of the Bacillus subtilis and Bacillus cereus clades in molecular terms and proposal to limit the placement of new species into the genus Bacillus. Int J Syst Evol Microbiol 63(7):2712–2726
Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17(4):540–552
Charlebois RL, Doolittle WF (2004) Computing prokaryotic gene ubiquity: Rescuing the core from extinction. Genome Res 14(12):2469–2477
Chatterjee S, Almeida RPP, Lindow S (2008) Living in two worlds: the plant and insect lifestyles of Xylella fastidiosa. Annu Rev Phytopathol 46:243–271
Chen J, Xie G, Han S, Chertkov O, Sims D, Civerolo EL (2010) Whole genome sequences of two Xylella fastidiosa strains (M12 and M23) causing almond leaf scorch disease in California. J Bacteriol 192(17):4534
Christensen P, Cook FD (1978) Lysobacter, a new genus of nonfruiting, gliding bacteria with a high base ratio. Int J Syst Bacteriol 28(3):367–393
Ciccarelli FD, Doerks T, Von Mering C, Creevey CJ, Snel B, Bork P (2006) Toward automatic reconstruction of a highly resolved tree of life. Science 311(5765):1283–1287
Cole J, Wang Q, Fish J, Chai B, McGarrell D, Sun Y, Brown C, Porras-Alfaro A, Kuske C, Tiedje J (2014) Ribosomal database project: data and tools for high throughput rRNA analysis. Nucleic Acids Res 42(1):D633
Crossman LC, Gould VC, Dow JM, Vernikos GS, Okazaki A, Sebaihia M, Saunders D, Arrowsmith C, Carver T, Peters N (2008) The complete genome, comparative and functional analysis of Stenotrophomonas maltophilia reveals an organism heavily shielded by drug resistance determinants. Genome Biol 9(4):R74
Cutino-Jimenez AM, Martins-Pinheiro M, Lima WC, Martin-Tornet A, Morales OG, Menck CFM (2010) Evolutionary placement of Xanthomonadales based on conserved protein signature sequences. Mol Phylogen Evol 54(2):524–534
da Silva AR, Ferro JA, Reinach F, Farah C, Furlan L, Quaggio R, Monteiro-Vitorello C, Van Sluys M, Almeida N, Alves L (2002) Comparison of the genomes of two Xanthomonas pathogens with differing host specificities. Nature 417(6887):459–463
Darrasse A, Carrere S, Barbe V, Boureau T, Arrieta-Ortiz ML, Bonneau S, Briand M, Brin C, Cociancich S, Durand K et al (2013) Genome sequence of Xanthomonas fuscans subsp. fuscans strain 4834-R reveals that flagellar motility is not a general feature of xanthomonads. BMC Genomics 14:761
De Clercq D, Van Trappen S, Cleenwerck I, Ceustermans A, Swings J, Coosemans J, Ryckeboer J (2006) Rhodanobacter spathiphylli sp. nov., a gammaproteobacterium isolated from the roots of Spathiphyllum plants grown in a compost-amended potting mix. Int J Syst Evol Microbiol 56(Pt 8):1755–1759
Gao B, Gupta RS (2012a) Microbial systematics in the post-genomics era. Anton Leeuw Int J G 101(1):45–54
Gao B, Gupta RS (2012b) Phylogenetic framework and molecular signatures for the main clades of the phylum Actinobacteria. Microbiol Mol Biol Rev 76(1):66–112
Gao B, Mohan R, Gupta RS (2009) Phylogenomics and protein signatures elucidating the evolutionary relationships among the Gammaproteobacteria. Int J Syst Evol Microbiol 59(2):234–247
Gupta RS (1998) Protein phylogenies and signature sequences: a reappraisal of evolutionary relationships among archaebacteria, eubacteria, and eukaryotes. Microbiol Mol Biol Rev 62(4):1435
Gupta RS (2010) Applications of conserved indels for understanding microbial phylogeny. In: Oren A, Papke RT (eds) Molecular phylogeny of microorganisms. Caister Academic Press, Norfolk, pp 135–150
Gupta RS (2014) Identification of conserved indels that are useful for classification and evolutionary studies Methods in Microbiology, vol 41. Academic Press: 10.1016/bs.mim.2014.05.003
Gupta RS, Lali R (2013) Molecular signatures for the phylum Aquificae and its different clades: proposal for division of the phylum Aquificae into the emended order Aquificales, containing the families Aquificaceae and Hydrogenothermaceae, and a new order Desulfurobacteriales ord. nov., containing the family Desulfurobacteriaceae. Anton Leeuw Int J G 104(3):349–368
Gupta RS, Mahmood S, Adeolu M (2013) A phylogenomic and molecular signature based approach for characterization of the phylum Spirochaetes and its major clades: proposal for a taxonomic revision of the phylum. Frontiers in microbiology 4:217
Gutierrez T, Green DH, Whitman WB, Nichols PD, Semple KT, Aitken MD (2012) Algiphilus aromaticivorans gen. nov., sp. nov., an aromatic hydrocarbon-degrading bacterium isolated from a culture of the marine dinoflagellate Lingulodinium polyedrum, and proposal of Algiphilaceae fam. nov. Int J Syst Evol Microbiol 62(11):2743–2749
Henrici AT, Johnson DE (1935) Studies of Freshwater Bacteria: II. Stalked Bacteria, a New Order of Schizomycetes. J Bacteriol 30(1):61–93
Im WT, Lee ST, Yokota A (2004) Rhodanobacter fulvus sp. nov., a beta-galactosidase-producing gammaproteobacterium. J Gen Appl Microbiol 50(3):143–147
Jalan N, Kumar D, Yu F, Jones JB, Graham JH, Wang N (2013) Complete genome sequence of Xanthomonas citri subsp. citri Strain Aw12879, a restricted-host-range citrus canker-causing bacterium. Genome Announc 1(3):e00235-13
Jaufeerally-Fakim Y, Dookun A (2000) Extraction of high quality DNA from polysaccharides-secreting xanthomonads. Sci Technol Res J Univ Maurit 6:33–40
Jeanmougin F, Thompson JD, Gouy M, Higgins DG, Gibson TJ (1998) Multiple sequence alignment with clustal X. Trends Biochem Sci 23(10):403
Kostka JE, Green SJ, Rishishwar L, Prakash O, Katz LS, Marino-Ramirez L, Jordan IK, Munk C, Ivanova N, Mikhailova N et al (2012) Genome sequences for six Rhodanobacter strains, isolated from soils and the terrestrial subsurface, with variable denitrification capabilities. J Bacteriol 194(16):4461–4462
Kyrpides N, Overbeek R, Ouzounis C (1999) Universal protein families and the functional content of the last universal common ancestor. J Mol Evol 49(4):413–423
Lee B-M, Park Y-J, Park D-S, Kang H-W, Kim J-G, Song E-S, Park I-C, Yoon U-H, Hahn J-H, Koo B-S (2005) The genome sequence of Xanthomonas oryzae pathovar oryzae KACC10331, the bacterial blight pathogen of rice. Nucleic Acids Res 33(2):577–586
Lee CS, Kim KK, Aslam Z, Lee ST (2007) Rhodanobacter thiooxydans sp. nov., isolated from a biofilm on sulfur particles used in an autotrophic denitrification process. Int J Syst Evol Microbiol 57(Pt 8):1775–1779
Lee SH, Jin HM, Lee HJ, Kim JM, Jeon CO (2012) Complete genome sequence of the BTEX-degrading bacterium Pseudoxanthomonas spadix BD-a59. J Bacteriol 194(2):544
Looney WJ, Narita M, Mühlemann K (2009) Stenotrophomonas maltophilia: an emerging opportunist human pathogen. Lancet Infect Dis 9(5):312–323
Losey NA, Stevenson BS, Verbarg S, Rudd S, Moore ER, Lawson PA (2013) Fontimonas thermophila gen. nov., sp. nov., a moderately thermophilic bacterium isolated from a freshwater hot spring, and proposal of Solimonadaceae fam. nov. to replace Sinobacteraceae Zhou et al. 2008. Int J Syst Evol Microbiol 63(1):254–259
Meidanis J, Braga MD, Verjovski-Almeida S (2002) Whole-genome analysis of transporters in the plant pathogen Xylella fastidiosa. Microbiol Mol Biol Rev 66(2):272–299
Nalin R, Simonet P, Vogel TM, Normand P (1999) Rhodanobacter lindaniclasticus gen. nov., sp. nov., a lindane-degrading bacterium. Int J Syst Bacteriol 49(1):19–23
Naushad HS, Gupta RS (2013) Phylogenomics and molecular signatures for species from the plant pathogen-containing order Xanthomonadales. PLoS ONE 8(2):e55216
Oren A (2010) The phyla of prokaryotes—cultured and uncultured. In: Oren A, Papke RT (eds) Molecular phylogeny of microorganisms. Caister Academic Press, Norfolk, pp 85–107
Park JH, Kim R, Aslam Z, Jeon CO, Chung YR (2008) Lysobacter capsici sp. nov., with antimicrobial activity, isolated from the rhizosphere of pepper, and emended description of the genus Lysobacter. Int J Syst Evol Microbiol 58(2):387–392
Parte AC (2013) LPSN–list of prokaryotic names with standing in nomenclature. Nucleic Acids Res 42:D613–D616
Pieretti I, Royer M, Barbe V, Carrere S, Koebnik R, Cociancich S, Couloux A, Darrasse A, Gouzy J, Jacques MA et al (2009) The complete genome sequence of Xanthomonas albilineans provides new insights into the reductive genome evolution of the xylem-limited Xanthomonadaceae. BMC Genomics 10:616
Qian W, Jia Y, Ren SX, He YQ, Feng JX, Lu LF, Sun Q, Ying G, Tang DJ, Tang H et al (2005) Comparative and functional genomic analyses of the pathogenicity of phytopathogen Xanthomonas campestris pv. campestris. Genome Res 15(6):757–767
Rokas A, Holland PWH (2000) Rare genomic changes as a tool for phylogenetics. Trends Ecol Evol 15(11):454–459
Rokas A, Williams BL, King N, Carroll SB (2003) Genome-scale approaches to resolving incongruence in molecular phylogenies. Nature 425(6960):798–804
Ryan RP, Vorhölter F-J, Potnis N, Jones JB, Van Sluys M-A, Bogdanove AJ, Dow JM (2011) Pathogenomics of Xanthomonas: understanding bacterium–plant interactions. Nat Rev Microbiol 9(5):344–355
Saddler GS, Bradbury JF (2005a) Order III. Xanthomonadales ord. nov. In: Brenner DJ, Krieg NR, Staley JT, Garrity GM, Boone, Vos P, Goodfellow M, Rainey FA, Schleifer K-H (eds) Bergey’s manual of systematic bacteriology. Springer, Austin, pp 63–122
Saddler GS, Bradbury JF (2005b) Xanthomonadaceae fam. nov Validation of publication of new names and new combinations previously effectively published outside the IJSEM, List no 106. Int J Syst Evol Microbiol 55:2235–2238
Salzberg SL, Sommer DD, Schatz MC, Phillippy AM, Rabinowicz PD, Tsuge S, Furutani A, Ochiai H, Delcher AL, Kelley D (2008) Genome sequence and rapid evolution of the rice pathogen Xanthomonas oryzae pv. oryzae PXO99A. BMC Genomics 9(1):204
Shimane Y, Tsuruwaka Y, Miyazaki M, Mori K, Minegishi H, Echigo A, Ohta Y, Maruyama T, Grant WD, Hatada Y (2013) Salinisphaera japonica sp. nov., a moderately halophilic bacterium isolated from the surface of a deep-sea fish, Malacocottus gibber, and emended description of the genus Salinisphaera. Int J Syst Evol Microbiol 63(6):2180–2185
Skerman VBD, McGowan V, Sneath PHA (1980) Approved lists of bacterial names. Int J Syst Bacteriol 30(1):225–420
Studholme DJ, Wasukira A, Paszkiewicz K, Aritua V, Thwaites R, Smith J, Grant M (2011) Draft genome sequences of Xanthomonas sacchari and two banana-associated xanthomonads reveal insights into the Xanthomonas group 1 clade. Genes 2(4):1050–1065
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739
Tavaré S (1986) Some probabilistic and statistical problems in the analysis of DNA sequences. In: Miura RM (ed) Lectures on mathematics in the life sciences, 17th edn. American Mathematical Society, Providence, pp 57–86
Tindall B (2014a) Names at the rank of class, subclass and order, their typification and current status: supplementary information to Opinion 79. Judicial commission of the international committee on systematics of prokaryotes. Int J Syst Evol Microbiol 64(10):3599–3602
Tindall BJ (2014b) The family name Solimonadaceae Losey et al. 2013 is illegitimate, proposals to create the names ‘Sinobacter soli’ comb. nov. and ‘Sinobacter variicoloris’ contravene the Code, the family name Xanthomonadaceae Saddler and Bradbury 2005 and the order name Xanthomonadales Saddler and Bradbury 2005 are illegitimate and notes on the application of the family names Solibacteraceae Zhou et al. 2008, Nevskiaceae Henrici and Johnson 1935 (Approved Lists 1980) and Lysobacteraceae Christensen and Cook 1978 (Approved Lists 1980) and order name Lysobacteriales Christensen and Cook 1978 (Approved Lists 1980) with respect to the classification of the corresponding type genera Solibacter Zhou et al. 2008 Nevskia Famintzin 1892 (Approved Lists 1980) and Lysobacter Christensen and Cook 1978 (Approved Lists 1980) and importance of accurately expressing the link between a taxonomic name, its authors and the corresponding description/circumscription/emendation. Int J Syst Evol Microbiol 64(1):293–297
Van Sluys MA, de Oliveira MC, Monteiro-Vitorello CB, Miyaki CY, Furlan LR, Camargo LE, da Silva AC, Moon DH, Takita MA, Lemos EG et al (2003) Comparative analyses of the complete genome sequences of Pierce’s disease and citrus variegated chlorosis strains of Xylella fastidiosa. J Bacteriol 185(3):1018–1026
Williams KP, Gillespie JJ, Sobral BW, Nordberg EK, Snyder EE, Shallom JM, Dickerman AW (2010) Phylogeny of gammaproteobacteria. J Bacteriol 192(9):2305–2314
Wilson K (1987) Preparation of genomic DNA from bacteria. In: Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K (eds) Current protocols in molecular biology. Wiley, New York, pp 2.4.1–2.4.2
Wu D, Hugenholtz P, Mavromatis K, Pukall R, Dalin E, Ivanova NN, Kunin V, Goodwin L, Wu M, Tindall BJ (2009) A phylogeny-driven genomic encyclopaedia of Bacteria and Archaea. Nature 462(7276):1056–1060
Yilmaz P, Parfrey LW, Yarza P, Gerken J, Pruesse E, Quast C, Schweer T, Peplies J, Ludwig W, Glöckner FO (2013) The SILVA and “all-species living tree project (LTP)” taxonomic frameworks. Nucleic Acids Res. doi:10.1093/nar/gkt1209
Zhou Y, Zhang Y-Q, Zhi X-Y, Wang X, Dong J, Chen Y, Lai R, Li W-J (2008) Description of Sinobacter flavus gen. nov., sp. nov., and proposal of Sinobacteraceae fam. nov. Int J Syst Evol Microbiol 58(1):184–189
Acknowledgments
We thank Professor Iain Sutcliffe for valuable comments and suggestions for improvement of this manuscript. This work was supported by a research grant from the Natural Science and Engineering Research Council of Canada to RSG.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Naushad, S., Adeolu, M., Wong, S. et al. A phylogenomic and molecular marker based taxonomic framework for the order Xanthomonadales: proposal to transfer the families Algiphilaceae and Solimonadaceae to the order Nevskiales ord. nov. and to create a new family within the order Xanthomonadales, the family Rhodanobacteraceae fam. nov., containing the genus Rhodanobacter and its closest relatives. Antonie van Leeuwenhoek 107, 467–485 (2015). https://doi.org/10.1007/s10482-014-0344-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10482-014-0344-8