Relationship of Bacillus amyloliquefaciens clades associated with strains DSM 7 T and FZB42 T: A proposal for Bacillus amyloliquefaciens subsp. amyloliquefaciens subsp. nov. and bacillus amyloliquefaciens subsp. plantarum subsp. nov. based on complete genome sequence comparisons

International Journal of Systematic and Evolutionary Microbiology

Volumn 61, Issue 8, 2011, Pages 1786-1801

  Borriss, Rainer ^a   Chen, Xiao Hua ^a   Rueckert, Christian ^b   Blom, Jochen ^b   Becker, Anke ^b   Baumgarth, Birgit ^b   Fan, Ben ^a   Pukall, Rüdiger ^c   Schumann, Peter ^c   Spröer, Cathrin ^c   Junge, Helmut ^d   Vater, Joachim ^e   Pühler, Alfred ^b   Klenk, Hans Peter ^c  

^a HUMBOLDT UNIVERSITY   (Germany)

^b BIELEFELD UNIVERSITY   (Germany)

^c LEIBNIZ INSTITUTE DSMZ GERMAN COLLECTION OF MICROORGANISMS AND CELL CULTURES   (Germany)

^d ABiTEP   (Germany)

^e TECHNISCHE UNIVERSITÄT BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACILLOMYCIN D; BACTERIAL DNA; DIFFICIDIN; DNA TOPOISOMERASE (ATP HYDROLYSING) A; FENGYCIN; ITURIN A; LIPOPEPTIDE; MACROLACTIN; POLYKETIDE; RIBOSOME RNA; UNCLASSIFIED DRUG;

ARTICLE; BACILLUS AMYLOLIQUEFACIENS; BACTERIAL COLONIZATION; BACTERIAL GENOME; COMPARATIVE GENOMIC HYBRIDIZATION; DNA DNA HYBRIDIZATION; DNA MICROARRAY; GENE SEQUENCE; LASER SCANNING CYTOMETRY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; UNINDEXED SEQUENCE;

BACILLUS; BACTERIAL PROTEINS; BASE SEQUENCE; DNA, BACTERIAL; DNA, RIBOSOMAL; GENOME, BACTERIAL; MOLECULAR SEQUENCE DATA; PHYLOGENY; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SOIL MICROBIOLOGY;

ARABIDOPSIS; BACILLUS AMYLOLIQUEFACIENS; BACILLUS SUBTILIS; RHIZOBIUM;

EID: 79961051980     PISSN: 14665026     EISSN: None     Source Type: Journal    
DOI: 10.1099/ijs.0.023267-0     Document Type: Article

References (63)

1. Auch, A. F., von Jan, M., Klenk, H.-P. & Göker, M. (2010a). Digital DNA-DNA hybridization for microbial species delineation by means of genome-to-genome sequence comparison. Stand Genomic Sci 2, 117-134.
2. Auch, A. F., Klenk, H.-P. & Göker, M. (2010b). Standard operating procedure for calculating genome-to-genome distances based on high-scoring segment pairs. Stand Genomic Sci 2, 142-148.
3. Barbe, V., Cruveiller, S., Kunst, F., Lenoble, P., Meurice, G., Sekowska, A., Vallenet, D., Wang, T., Moszer, I. & other authors (2009). From a consortium sequence to a unified sequence: the Bacillus subtilis 168 reference genome a decade later. Microbiology 155, 1758-1775.
4. Becker, A., Bergès, H., Krol, E., Bruand, C., Rüberg, S., Capela, D., Lauber, E., Meilhoc, E., Ampe, F. & other authors (2004). Global changes in gene expression in Sinorhizobium meliloti 1021 under microoxic and symbiotic conditions. Mol Plant Microbe Interact 17, 292-303.
5. Blom, J., Albaum, S. P., Doppmeier, D., Pühler, A., Vorhölter, F.-J., Zakrzewski, M. & Goesmann, A. (2009). EDGAR: a software framework for the comparative analysis of prokaryotic genomes. BMC Bioinformatics 10, 154.
6. Bochow, H., El-Sayed, S. F., Junge, H., Stavropoulo, A. & Schmiedeknecht, G. (2001). Use of Bacillus subtilis as biocontrol agent. IV. Salt-stress tolerance induction by Bacillus subtilis FZB24 seed treatment in tropical vegetable field crops, and its mode of action. J Plant Dis Prot 108, 21-30.
7. Brannen, P. M. & Kenney, D. S. (1997). Kodiak-a successful biological-control product for suppression of soil-borne plant pathogens of cotton. J Ind Microbiol Biotechnol 19, 169-171.
8. Cashion, P., Holder-Franklin, M. A., McCully, J. & Franklin, M. (1977). A rapid method for the base ratio determination of bacterial DNA. Anal Biochem 81, 461-466.
9. Chen, X. H., Vater, J., Piel, J., Franke, P., Scholz, R., Schneider, K. A., Koumoutsi, A., Hitzeroth, G., Grammel, N. & other authors (2006). Structural and functional characterization of three polyketide synthase gene clusters in Bacillus amyloliquefaciens FZB 42. J Bacteriol 188, 4024-4036.
10. Chen, X. H., Koumoutsi, A., Scholz, R., Eisenreich, A., Schneider, K., Heinemeyer, I., Morgenstern, B., Voss, B., Hess, W. R. & other authors (2007). Comparative analysis of the complete genome sequence of the plant growth-promoting bacterium Bacillus amylo-liquefaciens FZB42. Nat Biotechnol 25, 1007-1014.
11. Chen, X. H., Scholz, R., Borriss, M., Junge, H., Mögel, G., Kunz, S. & Borriss, R. (2009a). Difficidin and bacilysin produced by plant-associated Bacillus amyloliquefaciens are efficient in controlling fire blight disease. J Biotechnol 140, 38-44.
12. Chen, X. H., Koumoutsi, A., Scholz, R. & Borriss, R. (2009b). More than anticipated-production of antibiotics and other secondary metabolites by Bacillus amyloliquefaciens FZB42. J Mol Microbiol Biotechnol 16, 14-24.
13. Chun, J. & Bae, K. S. (2000). Phylogenetic analysis of Bacillus subtilis and related taxa based on partial gyrA gene sequences. Antonie van Leeuwenhoek 78, 123-127.
14. Cole, J. R., Konstantinidis, K., Farris, R. J. & Tiedje, J. M. (2010). Microbial diversity and phylogeny: extending from rRNAs to genomes. In Environmental Molecular Microbiology. pp.1-20. Edited by W.-T. Liu & J. K. Jansson. UK: Calster Academic Press Norfolk.
15. Connor, N., Sikorski, J., Rooney, A. P., Kopac, S., Koeppel, A. F., Burger, A., Cole, S. G., Perry, E. B., Krizanc, D. & other authors (2010). Ecology of speciation in the genus Bacillus. Appl Environ Microbiol 76, 1349-1358.
16. De Ley, J., Cattoir, H. & Reynaerts, A. (1970). The quantitative measurement of DNA hybridization from renaturation rates. Eur J Biochem 12, 133-142.
17. Dondrup, M., Goesmann, A., Bartels, D., Kalinowski, J., Krause, L., Linke, B., Rupp, O., Sczyrba, A., Pühler, A. & Meyer, F. (2003). EMMA: a platform for consistent storage and efficient analysis of microarray data. J Biotechnol 106, 135-146.
18. Earl, A. M., Losick, R. & Kolter, R. (2007). Bacillus subtilis genome diversity. J Bacteriol 189, 1163-1170.
19. Eisen, M. B., Spellman, P. T., Brown, P. O. & Botstein, D. (1998). Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A 95, 14863-14868.
20. Felsenstein, J. (1989). PHYLIP: phylogeny interference package. Cladistics 5, 154-166.
21. Fritze, D. (2004). Taxonomy of the genus Bacillus and related genera: the aerobic endospore-forming bacteria. Phytopathology 94, 1245-1248.
22. Fukumoto, J. (1943). [Studies on the production of bacterial amylase. I. Isolation of bacteria secreting potent amylases and their distribution.] J Agric Chem Soc Jpn 19, 487-503 (in Japanese).
23. Gatson, J. W., Benz, B. F., Chandrasekaran, C., Satomi, M., Venkateswaran, K. & Hart, M. E. (2006). Bacillus tequilensis sp. nov., isolated from a 2000-year-old Mexican shaft-tomb, is closely related to Bacillus subtilis. Int J Syst Evol Microbiol 56, 1475-1484.
24. Giuntini, E., Mengoni, A., De Filippo, C., Cavalieri, D., Aubin-Horth, N., Landry, C. R., Becker, A. & Bazzicalupo, M. (2005). Large-scale genetic variation of the symbiosis-required megaplasmid pSymA revealed by comparative genomic analysis of Sinorhizobium meliloti natural strains. BMC Genomics 6, 158.
25. Gordon, R. E., Haynes, W. C. & Hor-Nai Pang, C. (1973). The genus Bacillus. Washington, DC: US Department of Agriculture.
26. Goto, K., Omura, T., Hara, Y. & Sadaie, Y. (2000). Application of the partial 16S rDNA sequence as an index for rapid identification of species in the genus Bacillus. J Gen Appl Microbiol 46, 1-8.
27. Grosch, R., Junge, H., Krebs, B. & Bochow, H. (1999). Use of Bacillus subtilis as biocontrol agent. III. Influence of Bacillus subtilis on fungal root diseases and on yield in soilless culture. J Plant Dis Prot 106, 568-580.
28. Hofemeister, J., Conrad, B., Adler, B., Hofemeister, B., Feesche, J., Kucheryava, N., Steinborn, G., Franke, P., Grammel, N. & other authors (2004). Genetic analysis of the biosynthesis of non-ribosomal peptide- and polyketide-like antibiotics, iron uptake and biofilm formation by Bacillus subtilis A1/3. Mol Genet Genomics 272, 363-378.
29. Huß, V. A. R., Festl, H. & Schleifer, K. H. (1983). Studies on the spectrophotometric determination of DNA hybridization from renaturation rates. Syst Appl Microbiol 4, 184-192.
30. Idris, E. E., Iglesias, D. J., Talon, M. & Borriss, R. (2007). Tryptophan-dependent production of indole-3-acetic acid (IAA) affects level of plant growth promotion by Bacillus amyloliquefaciens FZB42. Mol Plant Microbe Interact 20, 619-626.
31. Idriss, E. E., Makarewicz, O., Farouk, A., Rosner, K., Greiner, R., Bochow, H., Richter, T. & Borriss, R. (2002). Extracellular phytase activity of Bacillus amyloliquefaciens FZB45 contributes to its plant-growth-promoting effect. Microbiology 148, 2097-2109.
32. Joshi, R. & McSpadden Gardener, B. B. (2006). Identification and characterization of novel genetic markers associated with biological control activity in Bacillus subtilis. Phytopathology 96, 145-154.
33. Keay, L. (1970). The action of Bacillus subtilis saccharifying amylase on starch and b-cyclodextrin. Die Stärke (Starch) 22, 153-157.
34. Klatte, S., Kroppenstedt, R. M. & Rainey, F. A. (1994). Rhodococcus opacus sp. nov., an unusual nutritionally versatile Rhodococcus-species. Syst Appl Microbiol 17, 355-360.
35. Kloepper, J. W., Leong, J., Teintze, M. & Schroth, M. (1980). Enhancing plant growth by siderophores produces by plant-growth-promoting rhizobacteria. Nature 286, 885-886.
36. Koumoutsi, A., Chen, X. H., Henne, A., Liesegang, H., Hitzeroth, G., Franke, P., Vater, J. & Borriss, R. (2004). Structural and functional characterization of gene clusters directing nonribosomal synthesis of bioactive cyclic lipopeptides in Bacillus amyloliquefaciens strain FZB42. J Bacteriol 186, 1084-1096.
37. Krebs, B., Höding, B., Kübart, S. M., Workie, A., Junge, H., Schmiedeknecht, G., Grosch, R., Bochow, H. & Hevesi, M. (1998). Use of Bacillus subtlis as biocontrol agent. 1. Activities and characterization of Bacillus subtilis strains. J Plant Dis Prot 105, 181-197.
38. Leenders, F., Stein, T. H., Kablitz, B., Franke, P. & Vater, J. (1999). Rapid typing of Bacillus subtilis strains by their secondary metabolites using matrix assisted laser desorption/ionisation mass spectrometry of intact cells. Rapid Commun Mass Spectrom 13, 943-949.
39. Li, B., Xu, L. H., Lou, M. M., Li, F., Zhang, Y. D. & Xie, G. L. (2008). Isolation and characterization of antagonistic bacteria against bacterial leaf spot of Euphorbia pulcherrima. Lett Appl Microbiol 46, 450-455.
40. Linke, B., McHardy, A. C., Neuweger, H., Krause, L. & Meyer, F. (2006). REGANOR: a gene prediction server for prokaryotic genomes and a database of high quality gene predictions for prokaryotes. Appl Bioinformatics 5, 193-198.
41. Logan, N. A., Berge, O., Bishop, A. H., Busse, H.-J., De Vos, P., Fritze, D., Heyndrickx, M., Kämpfer, P., Rabinovitch, L. & other authors (2009). Proposed minimal standards for describing new taxa of aerobic, endospore-forming bacteria. Int J Syst Evol Microbiol 59, 2114-2121.
42. Meyer, F., Goesmann, A., McHardy, A. C., Bartels, D., Bekel, T., Clausen, J., Kalinowski, J., Linke, B., Rupp, O. & other authors (2003). GenDB-an open source genome annotation system for prokaryote genomes. Nucleic Acids Res 31, 2187-2195.
43. Nakamura, L. K. (1989). Taxonomic relationship of black-pigmented Bacillus subtilis strains and a proposal for Bacillus atrophaeus sp. nov. Int J Syst Bacteriol 39, 295-300.
44. Nakamura, L. K., Roberts, M. S. & Cohan, F. M. (1999). Relationship of Bacillus subtilis clades associated with strains 168 and W23: a proposal for Bacillus subtilis subsp. subtilis subsp. nov. and Bacillus subtilis subsp. spizizenii subsp. nov. Int J Syst Bacteriol 49, 1211-1215.
45. Palmisano, M. M., Nakamura, L. K., Duncan, K. E., Istock, C. A. & Cohan, F. M. (2001). Bacillus sonorensis sp. nov., a close relative of Bacillus licheniformis, isolated from soil in the Sonoran Desert, Arizona. Int J Syst Evol Microbiol 51, 1671-1679.
46. Priest, F. G., Goodfellow, M., Shute, L. A. & Berkeley, W. (1987). Bacillus amyloliquefaciens sp. nov., nom. rev. Int J Syst Bacteriol 37, 69-71.
47. Raupach, G. S. & Kloepper, J. W. (1998). Mixtures of plant growth-promoting rhizobacteria enhance biological control of multiple cucumber pathogens. Phytopathology 88, 1158-1164.
48. Reva, O. N., Dixelius, C., Meijer, J. & Priest, F. G. (2004). Taxonomic characterization and plant colonizing abilities of some bacteria related to Bacillus amyloliquefaciens and Bacillus subtilis. FEMS Microbiol Ecol 48, 249-259.
49. Riedel, K., Schroeter, A., Liebs, P., Graba, J.-P., Hecker, M. & Schrapel, D. (1987). Formation of extracellular neutral proteinase and the stringent response in Bacillus subtilis. Folia Microbiol (Praha) 32, 96-100.
50. Roberts, R. J., Wilson, G. A. & Young, F. E. (1977). Recognition sequence of specific endonuclease BamH.I from Bacillus amylolique-faciens H. Nature 265, 82-84.
51. Roberts, M. S., Nakamura, L. K. & Cohan, F. M. (1994). Bacillus mojavensis sp. nov., distinguishable from Bacillus subtilis by sexual isolation, divergence in DNA sequence, and differences in fatty acid composition. Int J Syst Bacteriol 44, 256-264.
52. Roberts, M. S., Nakamura, L. K. & Cohan, F. M. (1996). Bacillus vallismortis sp. nov., a close relative of Bacillus subtilis, isolated from soil in Death Valley, California. Int J Syst Bacteriol 46, 470-475.
53. Rooney, A. P., Price, N. P., Ehrhardt, C., Swezey, J. L. & Bannan, J. D. (2009). Phylogeny and molecular taxonomy of the Bacillus subtilis species complex and description of Bacillus subtilis subsp. inaquo-sorum subsp. nov. Int J Syst Evol Microbiol 59, 2429-2436.
54. Sasser, M. (1990). Identification of bacteria by gas chromatography of cellular fatty acids. USFCC Newsl 20, 16.
55. Schmiedeknecht, G., Bochow, H. & Junge, H. (1998). Use of Bacillus subtilis as biocontrol agent. II. Biological control of potato diseases. J Plant Dis Prot 105, 376-386.
56. Schneider, K., Chen, X.-H., Vater, J., Franke, P., Nicholson, G., Borriss, R. & Süssmuth, R. D. (2007). Macrolactin is the polyketide biosynthesis product of the pks2 cluster of Bacillus amyloliquefaciens FZB42. J Nat Prod 70, 1417-1423.
57. Suzuki, K., Goodfellow, M. & O'Donnell, A. G. (1993). Cell envelopes and classification. In Handbook of New Bacterial Systematics. pp. 195-250. Edited by M. Goodfellow & A. G. O'Donnell. London, San Diego, New York: Academic Press.
58. Thompson, J. D., Higgins, D. G. & Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22, 4673-4680.
59. Tindall, B. J., Rosselló -Móra, R., Busse, H.-J., Ludwig, W. & Kämpfer, P. (2010). Notes on the characterization of prokaryote strains for taxonomic purposes. Int J Syst Evol Microbiol 60, 249-266.
60. Vater, J., Kablitz, B., Wilde, C., Franke, P., Mehta, N. & Cameotra, S. S. (2002). Matrix-assisted laser desorption ionization-time of flight mass spectrometry of lipopeptide biosurfactants in whole cells and culture filtrates of Bacillus subtilis C-1 isolated from petroleum sludge. Appl Environ Microbiol 68, 6210-6219.
61. Welker, N. E. & Campbell, L. L. (1967). Unrelatedness of Bacillus amyloliquefaciens and Bacillus subtilis. J Bacteriol 94, 1124-1130.
62. Wolf, M., Geczi, A., Simon, O. & Borriss, R. (1995). Genes encoding xylan and b-glucan hydrolysing enzymes in Bacillus subtilis: characterization, mapping and construction of strains deficient in lichenase, cellulase and xylanase. Microbiology 141, 281-290.
63. Yao, A. V., Bochow, H., Karimov, S., Boturov, U., Sanginboy, S. & Sharipov, K. (2006). Effect of FZB42 Bacillus subtilis as a biofertilizer on cotton yields in field tests. Arch Phytopathol Plant Prot 39, 323-328.