Conserved signature indels and signature proteins as novel tools for understanding microbial phylogeny and systematics: Identification of molecular signatures that are specific for the phytopathogenic genera Dickeya, Pectobacterium and Brenneria

International Journal of Systematic and Evolutionary Microbiology

Volumn 64, Issue PART 2, 2014, Pages 366-383

  Naushad, Hafiz Sohail ^a   Lee, Brian ^a   Gupta, Radhey S ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

2 SUCCINYL 5 ENOLPYRUVYL 6 HYDROXY 3 CYCLOHEXENE 1 CARBOXYLATE SYNTHASE; 4 AMINO 4 DEOXY ARABINOSE TRANSFERASE; ACYLTRANSFERASE; ADENOSINE DEAMINASE; BETA GALACTOSIDASE; ELECTRON TRANSPORT COMPLEX RNFABCDGE TYPE C SUBUNIT; GLYCEROL 3 PHOSPHATE DEHYDROGENASE; MOLECULAR MARKER; MOLYBDENUM COFACTOR SYNTHESIS DOMAIN CONTAINING PROTEIN; MULTIDRUG RESISTANCE PROTEIN; PHOSPHORIBOSYL FORMYL GLYCINAMIDINE SYNTHASE; RECJ PROTEIN; REGULATOR PROTEIN; SIGMA E REGULATORY PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL STRAIN; BRENNERIA; CONSERVED SIGNATURE INDEL; CONSERVED SIGNATURE PROTEIN; DICKEYA; ENTEROBACTERIALES; FOOD CROP; GENE SEQUENCE; HORIZONTAL GENE TRANSFER; NONHUMAN; NUCLEOTIDE SEQUENCE; ORNAMENTAL PLANT; PECTOBACTERIUM; PHYLOGENETIC TREE; PRIORITY JOURNAL; TAXONOMY;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CONSERVED SEQUENCE; DNA, BACTERIAL; ENTEROBACTERIACEAE; INDEL MUTATION; MOLECULAR SEQUENCE DATA; PECTOBACTERIUM; PHYLOGENY; SEQUENCE ALIGNMENT;

EID: 84893518970     PISSN: 14665026     EISSN: None     Source Type: Journal    
DOI: 10.1099/ijs.0.054213-0     Document Type: Article

References (82)

1. Ahmod, N. Z., Gupta, R. S. & Shah, H. N. (2011). Identification of a Bacillus anthracis specific indel in the yeaC gene and development of a rapid pyrosequencing assay for distinguishing B. anthracis from the B. cereus group. J Microbiol Methods 87, 278-285.
2. Ajawatanawong, P. & Baldauf, S. L. (2013). Evolution of protein indels in plants, animals and fungi. BMC Evol Biol 13, 140.
3. Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W. & Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25, 3389-3402.
4. Bell, K. S., Sebaihia, M., Pritchard, L., Holden, M. T., Hyman, L. J., Holeva, M. C., Thomson, N. R., Bentley, S. D., Churcher, L. J. & other authors (2004). Genome sequence of the enterobacterial phytopathogen Erwinia carotovora subsp. atroseptica and characterization of virulence factors. Proc Natl Acad Sci U S A 101, 11105-11110.
5. Bhandari, V. & Gupta, R. S. (2014). Molecular signatures for the phylum (class) Thermotogae and a proposal for its division into three orders (Thermotogales, Kosmotogales ord. nov. and Petrotogales ord. nov.) containing four families (Thermotogaceae, Fervidobacteriaceae fam. nov., Kosmotogaceae fam. nov. and Petrotogaceae fam. nov.) and a new genus Pseudothermotoga gen. nov. with five new combinations. Antonie van Leeuwenhoek 105, 143-168.
6. Bhandari, V., Naushad, H. S. & Gupta, R. S. (2012). Protein based molecular markers provide reliable means to understand prokaryotic phylogeny and support Darwinian mode of evolution. Front Cell Infect Microbiol 2, 98.
7. Brady, C. L., Cleenwerck, I., Denman, S., Venter, S. N., Rodríguez-Palenzuela, P., Coutinho, T. A. & De Vos, P. (2012). Proposal to reclassify Brenneria quercina (Hildebrand and Schroth 1967) Hauben et al. 1999 into a new genus, Lonsdalea gen. nov., as Lonsdalea quercina comb. nov., descriptions of Lonsdalea quercina subsp. quercina comb. nov., Lonsdalea quercina subsp. iberica subsp. nov. and Lonsdalea quercina subsp. britannica subsp. nov., emendation of the description of the genus Brenneria, reclassification of Dickeya dieffenbachiae as Dickeya dadantii subsp. dieffenbachiae comb. nov., and emendation of the description of Dickeya dadantii. Int J Syst Evol Microbiol 62, 1592-1602.
8. Brenner, D. J., McWhorter, A. C., Kai, A., Steigerwalt, A. G. & Farmer, J. J., III (1986). Enterobacter asburiae sp. nov., a new species found in clinical specimens, and reassignment of Erwinia dissolvens and Erwinia nimipressuralis to the genus Enterobacter as Enterobacter dissolvens comb. nov. and Enterobacter nimipressuralis comb. nov. J Clin Microbiol 23, 1114-1120.
9. Brown, E. W., Davis, R. M., Gouk, C. & van der Zwet, T. (2000). Phylogenetic relationships of necrogenic Erwinia and Brenneria species as revealed by glyceraldehyde-3-phosphate dehydrogenase gene sequences. Int J Syst Evol Microbiol 50, 2057-2068.
10. Bull, C. T., De Boer, S. H., Denny, T. P., Firrao, G., Fischer-Le Saux, M., Saddler, G. S., Scortichini, M., Stead, D. E. & Takikawa, Y. (2012) Letter to the Editor: List of new names of plant pathogenic bacteria (2008-2010). J. Plant Pathol 94, 21-27.
11. Castresana, J. (2000). Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17, 540-552.
12. Charkowski, A. (2006). The soft rot Erwinia. In Plant-Associated Bacteria, pp. 423-505. Edited by S. Gnanamanickam. Dordrecht: Springer.
13. Ciccarelli, F. D., Doerks, T., von Mering, C., Creevey, C. J., Snel, B. & Bork, P. (2006). Toward automatic reconstruction of a highly resolved tree of life. Science 311, 1283-1287.
14. Costechareyre, D., Balmand, S., Condemine, G. & Rahbé, Y. (2012). Dickeya dadantii, a plant pathogenic bacterium producing Cyt-like entomotoxins, causes septicemia in the pea aphid Acyrthosiphon pisum. PLoS ONE 7, e30702.
15. Czajkowski, R., Pérombelon, M. C. M., van Veen, J. A. & van der Wolf, J. M. (2011). Control of blackleg and tuber soft rot of potato caused by Pectobacterium and Dickeya species: a review. Plant Pathol 60, 999-1013.
16. Denman, S., Brady, C., Kirk, S., Cleenwerck, I., Venter, S., Coutinho, T. & De Vos, P. (2012). Brenneria goodwinii sp. nov., associated with acute oak decline in the UK. Int J Syst Evol Microbiol 62, 2451-2456.
17. Diallo, S., Latour, X., Groboillot, A., Smadja, B., Copin, P., Orange, N., Feuilloley, M. & Chevalier, S. (2009). Simultaneous and selective detection of two major soft rot pathogens of potato: Pectobacterium atrosepticum (Erwinia carotovora subsp. atrosepticum) and Dickeya spp. (Erwinia chrysanthemi). Eur J Plant Pathol 125, 349-354.
18. Dutilh, B. E., Snel, B., Ettema, T. J. & Huynen, M. A. (2008). Signature genes as a phylogenomic tool. Mol Biol Evol 25, 1659-1667.
19. Dye, D. W. (1968). A taxonomic study of the genus Erwinia I: the 'amylovora' group. N Z J Sci 11, 590-607.
20. Euzéby, J. P. (2013). List of bacterial names with standing in nomenclature: a folder available on the Internet. [Last full update 22 November 2013] http://www.bacterio.cict.fr
21. Fang, G., Rocha, E. & Danchin, A. (2005). How essential are nonessential genes? Mol Biol Evol 22, 2147-2156.
22. Gao, B. & Gupta, R. S. (2005). Conserved indels in protein sequences that are characteristic of the phylum Actinobacteria. Int J Syst Evol Microbiol 55, 2401-2412.
23. Gao, B. & Gupta, R. S. (2007). Phylogenomic analysis of proteins that are distinctive of Archaea and its main subgroups and the origin of methanogenesis. BMC Genomics 8, 86.
24. Gao, B. & Gupta, R. S. (2012a). Microbial systematics in the postgenomics era. Antonie van Leeuwenhoek 101, 45-54.
25. Gao, B. & Gupta, R. S. (2012b). Phylogenetic framework and molecular signatures for the main clades of the phylum Actinobacteria. Microbiol Mol Biol Rev 76, 66-112.
26. Gao, B., Mohan, R. & Gupta, R. S. (2009a). Phylogenomics and protein signatures elucidating the evolutionary relationships among the Gammaproteobacteria. Int J Syst Evol Microbiol 59, 234-247.
27. Gao, B., Sugiman-Marangos, S., Junop, M. S. & Gupta, R. S. (2009b). Structural and phylogenetic analysis of a conserved actinobacteriaspecific protein (ASP1; SCO1997) from Streptomyces coelicolor. BMC Struct Biol 9, 40.
28. Gardan, L., Gouy, C., Christen, R. & Samson, R. (2003). Elevation of three subspecies of Pectobacterium carotovorum to species level: Pectobacterium atrosepticum sp. nov., Pectobacterium betavasculorum sp. nov. and Pectobacterium wasabiae sp. nov. Int J Syst Evol Microbiol 53, 381-391.
29. Gavini, F., Mergaert, J., Beji, A., Mielcarek, C., Izard, D., Kersters, K. & De Ley, J. (1989). Transfer of Enterobacter agglomerans (Beijerinck 1888) Ewing and Fife 1972 to Pantoea gen. nov. as Pantoea agglomerans comb. nov. and description of Pantoea dispersa sp. nov. Int J Syst Bacteriol 39, 337-345.
30. Glasner, J. D., Marquez-Villavicencio, M., Kim, H. S., Jahn, C. E., Ma, B., Biehl, B. S., Rissman, A. I., Mole, B., Yi, X. & other authors (2008). Niche-specificity and the variable fraction of the Pectobacterium pangenome. Mol Plant Microbe Interact 21, 1549-1560.
31. Glasner, J. D., Yang, C. H., Reverchon, S., Hugouvieux-Cotte-Pattat, N., Condemine, G., Bohin, J. P., Van Gijsegem, F., Yang, S., Franza, T. & other authors (2011). Genome sequence of the plant-pathogenic bacterium Dickeya dadantii 3937. J Bacteriol 193, 2076-2077.
32. Griffiths, E. & Gupta, R. S. (2004). Signature sequences in diverse proteins provide evidence for the late divergence of the Order Aquificales. Int Microbiol 7, 41-52.
33. Griffiths, E. & Gupta, R. S. (2006). Lateral transfers of serine hydroxymethyltransferase (glyA) and UDP-N-acetylglucosamine enolpyruvyl transferase (murA) genes from free-living Actinobacteria to the parasitic chlamydiae. J Mol Evol 63, 283-296.
34. Gupta, R. S. (1998). Protein phylogenies and signature sequences: a reappraisal of evolutionary relationships among archaebacteria, eubacteria, and eukaryotes. Microbiol Mol Biol Rev 62, 1435-1491.
35. Gupta, R. S. (2000). The phylogeny of Proteobacteria: relationships to other eubacterial phyla and eukaryotes. FEMS Microbiol Rev 24, 367-402.
36. Gupta, R. S. (2009). Protein signatures (molecular synapomorphies) that are distinctive characteristics of the major cyanobacterial clades. Int J Syst Evol Microbiol 59, 2510-2526.
37. Gupta, R. S. (2010). Applications of conserved indels for understanding microbial phylogeny. In Molecular Phylogeny of Microorganisms, pp. 135-150. Edited by A. Oren & R. T. Papke. Norwich: Caister Academic Press.
38. Gupta, R. S. & Gao, B. (2010). Recent advances in understanding microbial systematics. In Microbial Population Genetics, pp. 1-14. Edited by J. Xu. Norwich: Caister Academic Press.
39. Gupta, R. S. & Griffiths, E. (2002). Critical issues in bacterial phylogeny. Theor Popul Biol 61, 423-434.
40. Gupta, R. S. & Mathews, D. W. (2010). Signature proteins for the major clades of Cyanobacteria. BMC Evol Biol 10, 24.
41. Gupta, R. S. & Mok, A. (2007). Phylogenomics and signature proteins for the alpha proteobacteria and its main groups. BMCMicrobiol 7, 106.
42. Hauben, L., Moore, E. R., Vauterin, L., Steenackers, M., Mergaert, J., Verdonck, L. & Swings, J. (1998). Phylogenetic position of phytopathogens within the Enterobacteriaceae. Syst Appl Microbiol 21, 384-397.
43. Hauben, L., Gijsegem, F. V. & Swings, J. (2005). Genus XXIV. Pectobacterium. In Bergey's Manual of Systematic Bacteriology, pp. 721-730. Edited by G. M. Garrity. New York: Springer.
44. Jones, L. R. (1901). A soft rot of carrot and other vegetabels caused by Bacillus carotovorus. Vt Agric Exp Stn Annu Rep 13, 299-332.
45. Jones, D. T., Taylor, W. R. & Thornton, J. M. (1992). The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8, 275-282.
46. Koskinen, J. P., Laine, P., Niemi, O., Nykyri, J., Harjunpää, H., Auvinen, P., Paulin, L., Pirhonen, M., Palva, T. & Holm, L. (2012). Genome sequence of Pectobacterium sp. strain SCC3193. J Bacteriol 194, 6004.
47. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A. & other authors (2007). CLUSTAL W and CLUSTAL_X version 2.0. Bioinformatics 23, 2947-2948.
48. Lerat, E., Daubin, V., Ochman, H. & Moran, N. A. (2005). Evolutionary origins of genomic repertoires in bacteria. PLoS Biol 3, e130.
49. Lorenzini, E., Singer, A., Singh, B., Lam, R., Skarina, T., Chirgadze, N. Y., Savchenko, A. & Gupta, R. S. (2010). Structure and protein-protein interaction studies on Chlamydia trachomatis protein CT670 (YscO homolog). J Bacteriol 192, 2746-2756.
50. Ludwig, W. & Klenk, H.-P. (2005). Overview: a phylogenetic backbone and taxonomic framework for prokaryotic systamatics. In Bergey's Manual of Systematic Bacteriology, pp. 49-65. Edited by D. J. Brenner, N. R. Krieg, J. T. Staley & G. M. Garrity. Berlin: Springer-Verlag.
51. Ma, B., Hibbing, M. E., Kim, H. S., Reedy, R. M., Yedidia, I., Breuer, J., Breuer, J., Glasner, J. D., Perna, N. T. & other authors (2007). Host range and molecular phylogenies of the soft rot enterobacterial genera Pectobacterium and Dickeya. Phytopathology 97, 1150-1163.
52. Marrero, G., Schneider, K. L., Jenkins, D. M. & Alvarez, A. M. (2013). Phylogeny and classification of Dickeya based on multilocus sequence analysis. Int J Syst Evol Microbiol 63, 3524-3539.
53. Nandan, D., Lopez, M., Ban, F., Huang, M., Li, Y., Reiner, N. E. & Cherkasov, A. (2007). Indel-based targeting of essential proteins in human pathogens that have close host orthologue(s): discovery of selective inhibitors for Leishmania donovani elongation factor-1a. Proteins 67, 53-64.
54. Narra, H. P., Cordes, M. H. & Ochman, H. (2008). Structural features and the persistence of acquired proteins. Proteomics 8, 4772-4781.
55. Naum, M., Brown, E. W. & Mason-Gamer, R. J. (2008). Is 16S rDNA a reliable phylogenetic marker to characterize relationships below the family level in the Enterobacteriaceae? J Mol Evol 66, 630-642.
56. Naum, M., Brown, E. W. & Mason-Gamer, R. J. (2011). Is a robust phylogeny of the enterobacterial plant pathogens attainable? Cladistics 27, 80-93.
57. Naushad, H. S. & Gupta, R. S. (2013). Phylogenomics and molecular signatures for species from the plant pathogen-containing order Xanthomonadales. PLoS ONE 8, e55216.
58. Nykyri, J., Niemi, O., Koskinen, P., Nokso-Koivisto, J., Pasanen, M., Broberg, M., Plyusnin, I., Törönen, P., Holm, L. & other authors (2012). Revised phylogeny and novel horizontally acquired virulence determinants of the model soft rot phytopathogen Pectobacterium wasabiae SCC3193. PLoS Pathog 8, e1003013.
59. Olsen, G. J. & Woese, C. R. (1993). Ribosomal RNA: a key to phylogeny. FASEB J 7, 113-123.
60. Oren, A. (2010) Microbial systematics. In Handbook of Environmental Engineering, Vol. 10: Environmental Biotechnology, pp. 81-120. Edited by L. K. Wang, V. Ivanov, J.-H. Tay & Y. T. Hung. New York: Springer Science + Business Media.
61. Park, T. H., Choi, B. S., Choi, A. Y., Choi, I. Y., Heu, S. & Park, B. S. (2012). Genome sequence of Pectobacterium carotovorum subsp. carotovorum strain PCC21, a pathogen causing soft rot in Chinese cabbage. J Bacteriol 194, 6345-6346.
62. Parkinson, N., Stead, D., Bew, J., Heeney, J., Tsror Lahkim, L. & Elphinstone, J. (2009). Dickeya species relatedness and clade structure determined by comparison of recA sequences. Int J Syst Evol Microbiol 59, 2388-2393.
63. Pritchard, L., Humphris, S., Saddler, G. S., Parkinson, N. M., Bertrand, V. & Elphinstone, J. G., and Toth, I. K. (2013a) Detection of phytopathogens of the genus Dickeya using a PCR primer prediction pipeline for draft bacterial genome sequences. Plant Pathol 62, 587-596.
64. Pritchard, L., Humphris, S., Baeyen, S., Maes, M., Van Vaerenbergh, J., Elphinstone, J., Saddler, G., and Toth, I. (2013b) Draft genome sequences of four Dickeya dianthicola and four Dickeya solani strains. Genome Announc 1, e00087-12.
65. Rokas, A. & Holland, P. W. (2000). Rare genomic changes as a tool for phylogenetics. Trends Ecol Evol 15, 454-459.
66. Samson, R., Legendre, J. B., Christen, R., Fischer-Le Saux, M., Achouak, W. & Gardan, L. (2005). Transfer of Pectobacterium chrysanthemi (Burkholder et al. 1953) Brenner et al. 1973 and Brenneria paradisiaca to the genus Dickeya gen. nov. as Dickeya chrysanthemi comb. nov. and Dickeya paradisiaca comb. nov. and delineation of four novel species, Dickeya dadantii sp. nov., Dickeya dianthicola sp. nov., Dickeya dieffenbachiae sp. nov. and Dickeya zeae sp. nov. Int J Syst Evol Microbiol 55, 1415-1427.
67. Singh, B. & Gupta, R. S. (2009). Conserved inserts in the Hsp60 (GroEL) and Hsp70 (DnaK) proteins are essential for cellular growth. Mol Genet Genomics 281, 361-373.
68. Skerman, V. B. D., McGowan, V. & Sneath, P. H. A. (1980). Approved lists of bacterial names. Int J Syst Bacteriol 30, 225-420.
69. Spröer, C., Mendrock, U., Swiderski, J., Lang, E. & Stackebrandt, E. (1999). The phylogenetic position of Serratia, Buttiauxella and some other genera of the family Enterobacteriaceae. Int J Syst Bacteriol 49, 1433-1438.
70. Stackebrandt, E. (2006). Defining taxonomic ranks. In The Prokaryotes, pp. 29-57. Edited by M. Dworkin, S. Falkow, E. Rosenberg, K.-H. Schleifer & E. Stackebrandt. New York: Springer.
71. Tamura, K., Dudley, J., Nei, M. & Kumar, S. (2007). MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24, 1596-1599.
72. Toth, I. K., van der Wolf, J. M., Saddler, G., Lojkowska, E., Helias, V. & Porhonen, M. (2011). Dickeya species: an emerging problem for potato production in Europe. Plant Pathol 60, 385-399.
73. Van Vaerenbergh, J., Baeyen, S., De Vos, P. & Maes, M. (2012). Sequence diversity in the Dickeya fliC gene: phylogeny of the Dickeya genus and TaqMan1 PCR for 'D. solani', new biovar 3 variant on potato in Europe. PLoS ONE 7, e35738.
74. Waldee, E. L. (1945). Comparative studies of some peritrichous phytopathogenic bacteria. Iowa State Coll J Sci 19, 435-484.
75. Whelan, S. & Goldman, N. (2001). A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol 18, 691-699.
76. Williams, K. P., Gillespie, J. J., Sobral, B. W., Nordberg, E. K., Snyder, E. E., Shallom, J. M. & Dickerman, A. W. (2010). Phylogeny of gammaproteobacteria. J Bacteriol 192, 2305-2314.
77. Winslow, C. E., Broadhurst, J., Buchanan, R. E., Krumwiede, C., Rogers, L. A. & Smith, G. H. (1917). The families and genera of the Bacteria: Preliminary report of the Committee of the Society of American Bacteriologists on characterization and classification of bacterial types. J Bacteriol 2, 505-566.
78. Woese, C. R. (1998). Default taxonomy: Ernst Mayr's view of the microbial world. Proc Natl Acad Sci U S A 95, 11043-11046.
79. Wu, D., Hugenholtz, P., Mavromatis, K., Pukall, R., Dalin, E., Ivanova, N. N., Kunin, V., Goodwin, L., Wu, M. & other authors (2009). A phylogeny-driven genomic encyclopaedia of Bacteria and Archaea. Nature 462, 1056-1060.
80. Yarza, P., Ludwig, W., Euzéby, J., Amann, R., Schleifer, K. H., Glöckner, F. O. & Rosselló-Móra, R. (2010). Update of the All-Species Living Tree Project based on 16S and 23S rRNA sequence analyses. Syst Appl Microbiol 33, 291-299.
81. Yishay, M., Burdman, S., Valverde, A., Luzzatto, T., Ophir, R. & Yedidia, I. (2008). Differential pathogenicity and genetic diversity among Pectobacterium carotovorum ssp. carotovorum isolates from monocot and dicot hosts support early genomic divergence within this taxon. Environ Microbiol 10, 2746-2759.
82. Young, J. M. & Park, D. C. (2007). Relationships of plant pathogenic enterobacteria based on partial atpD, carA, and recA as individual and concatenated nucleotide and peptide sequences. Syst Appl Microbiol 30, 343-354.