Tardiphaga robiniae gen. nov., sp. nov., a new genus in the family Bradyrhizobiaceae isolated from Robinia pseudoacacia in Flanders (Belgium)

Systematic and Applied Microbiology

Volumn 35, Issue 4, 2012, Pages 205-214

  De Meyer, Sofie E ^a   Coorevits, An ^a,b   Willems, Anne ^a  

^a GHENT UNIVERSITY   (Belgium)

^b UNIVERSITY COLLEGE GHENT   (Belgium)

Author keywords

Alphaproteobacteria; Bradyrhizobiaceae; Housekeeping genes; Legumes; Rhizobiales; Robinia pseudoacacia; Root nodules; Symbiosis genes; Tardiphaga robiniae

Indexed keywords

FATTY ACID; GENOMIC DNA; RNA 16S;

ARTICLE; BACTERIAL STRAIN; BACTERIUM CULTURE; BACTERIUM ISOLATION; BIOCHEMISTRY; BRADYRHIZOBIACEAE; GRAM NEGATIVE BACTERIUM; HOSPITAL SERVICE; LIPID COMPOSITION; MOLECULAR PHYLOGENY; NITROBACTER; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPIC VARIATION; PLANT ROOT; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RHODOPSEUDOMONAS; ROBINIA; ROBINIA PSEUDOACACIA; SEQUENCE ANALYSIS; SPECIES IDENTIFICATION; TARDIPHAGA ROBINIAE;

BACTERIAL PROTEINS; BACTERIAL TYPING TECHNIQUES; BELGIUM; BRADYRHIZOBIACEAE; CLUSTER ANALYSIS; CYTOSOL; DNA, BACTERIAL; DNA, RIBOSOMAL; FATTY ACIDS; MOLECULAR SEQUENCE DATA; PHOSPHOLIPIDS; PHYLOGENY; PLANT ROOTS; RNA, RIBOSOMAL, 16S; ROBINIA; SEQUENCE ANALYSIS, DNA;

ALPHAPROTEOBACTERIA; BRADYRHIZOBIACEAE; BRADYRHIZOBIUM; NEGIBACTERIA; NITROBACTER; RHIZOBIALES; RHODOPSEUDOMONAS; ROBINIA PSEUDOACACIA;

EID: 84861663326     PISSN: 07232020     EISSN: 16180984     Source Type: Journal    
DOI: 10.1016/j.syapm.2012.02.002     Document Type: Article

References (64)

1. Baele M., Baele P., Vaneechoutte M., Storms V., Butaye P., Devriese L.A., Verschraegen G., Gillis M., Haesebrouck F. Application of tRNA intergenic spacer PCR for identification of Enterococcus species. J. Clin. Microbiol. 2000, 38:4201-4207.
2. Bock E., Sundermeyer-Klinger H., Stackebrandt E. New facultative lithoautotrophic nitrite-oxidizing bacteria. Arch. Microbiol. 1983, 136:281-284.
3. Brenner D.J., Hollis D.G., Moss C.W., English C.K., Hall G.S., Vincent J., Radosevic J., Birkness K.A., Bibb W.F., Quinn F.D. Proposal of Afipia gen. nov., with Afipia felis sp. nov. (formerly the cat scratch disease bacillus), Afipia clevelandensis sp. nov. (formerly the Cleveland Clinic Foundation strain), Afipia broomeae sp. nov., and three unnamed genospecies. J. Clin. Microbiol. 1991, 29:2450-2460.
4. Brenner D.J., Krieg N.R., Staley J.T., Garrity G.M. The Proteobacteria. Bergey's Manual of Systematic Bacteriology 2005, vol. 2 partC. Springer, New York.
5. Cleenwerck I., Vandemeulebroecke K., Janssens D., Swings J. Re-examination of the genus Acetobacter, with descriptions of Acetobacter cerevisiae sp. nov. and Acetobacter malorum sp. nov. Int. J. Syst. Evol. Microbiol. 2002, 52:1551-1558.
6. Collins M.D., Jones D. Distribution of isoprenoid quinone structural types in bacteria and their taxonomic implications. Microbiol. Rev. 1981, 45:316-354.
7. Cruz-Martinez K., Suttle K.B., Brodie E.L., Power M.E., Andersen G.L., Banfield J.F. Despite strong seasonal responses, soil microbial consortia are more resilient to long-term changes in rainfall than overlying grassland. ISME J. 2009, 3:738-744.
8. Czurda V., Maresch E. Beitrag zur Kenntnis der Athiorhodobakterien-Gesellschaften. Arch. Microbiol. 1937, 8:99-124.
9. De Meyer S.E., Van Hoorde K., Vekeman B., Braeckman T., Willems A. Genetic diversity of rhizobia associated with indigenous legumes in different regions of Flanders (Belgium). Soil Biol. Biochem. 2011, 43:2384-2396.
10. Garrity G.M., Bell J.A., Liburn T. Family VII. Bradyrhizobiaceae. Bergey's Manual of Systematic Bacteriology 2005, 438-475. Springer, New York. D.J. Brenner, N.R. Krieg, J.T. Staley (Eds.).
11. Gaunt M.W., Turner S.L., Rigottier-Gois L., Lloyd-Macgilp S.A., Young J.P.W. Phylogenies of atpD and recA support the small subunit rRNA-based classification of rhizobia. Int. J. Syst. Evol. Microbiol. 2001, 51:2037-2048.
12. Gevers D., Huys G., Swings J. Applicability of rep-PCR fingerprinting for identification of Lactobacillus species. FEMS Microbiol. Lett. 2001, 205:31-36.
13. Han T.X., Wang E.T., Han L.L., Chen W.F., Sui X.H., Chen W.X. Molecular diversity and phylogeny of rhizobia associated with wild legumes native to Xinjiang, China. Syst. Appl. Microbiol. 2008, 31:287-301.
14. Haukka K., Lindström K., Young J.P.W. Three phylogenetic groups of nodA and nifH genes in Sinorhizobium and Mesorhizobium isolates from leguminous trees growing in Africa and Latin America. Appl. Environ. Microbiol. 1998, 64:419-426.
15. Hiraishi A., Santos T.S., Sugiyama J., Komagata K. Rhodopseudomonas rutila is a later subjective synonym of Rhodopseudomonas palustris. Int. J. Syst. Bacteriol. 1992, 42:186-188.
16. Hirsch A.M., Muller M. Blastobacter aggragatus sp. nov., Blastobacter capsulatus sp. nov., and Blastobacter denitrificans sp. nov., new budding bacteria from fresh water habitats. Syst. Appl. Microbiol. 1985, 6:281-286.
17. Hougardy A., Tindall B., Klemme J. Rhodopseudomonas rhenobacensis sp. nov., a new nitrate-reducing purple non-sulfur bacterium. Int. J. Syst. Evol. Microbiol. 2000, 50:985-992.
18. Hwang C.Y., Cho B.C. Cohaesibacter gelatinilyticus gen. nov., sp. nov., a marine bacterium that forms a distinct branch In the order Rhizobiales, and proposal of Cohaesibacteraceae fam. nov. Int. J. Syst. Evol. Microbiol. 2008, 58:267-277.
19. Imhoff J.F. Transfer of Rhodopseudomonas acidophila to the new genus Rhodoblastus as Rhodoblastus acidophilus gen. nov., comb. nov. Int. J. Syst. Evol. Microbiol. 2001, 51:1863-1866.
20. Imhoff J.F. Genus IX. Rhodopseudomonas. Bergey's Manual of Systematic Bacteriology 2005, 473-475. Springer, New York. D.J. Brenner, N.R. Krieg, J.T. Staley, G.M. Garrity (Eds.).
21. Imhoff J.F., Trüper H.G., Pfennig N. Rearrangement of the species and genera of the phototrophic purple nonsulfur bacteria. Int. J. Syst. Bacteriol. 1984, 34:340-343.
22. Kämpfer P., Buczolits S., Albrecht A., Busse H.J., Stackebrandt E. Towards a standardized format for the description of a novel species (of an established genus): Ochrobactrum gallinifaecis sp. nov. Int. J. Syst. Evol. Microbiol. 2003, 53:893-896.
23. Kennedy C. Genus III. Agromonas. Bergey's Manual of Systematic Bacteriology 2005, 448-451. Springer, New York. D.J. Brenner, N.R. Krieg, J.T. Staley, G.M. Garrity (Eds.).
24. Kuykendall L.D. Genus I. Bradyrhizobium. Bergey's Manual of Systematic Bacteriology 2005, 438-442. Springer, New York. D.J. Brenner, N.R. Krieg, J.T. Staley, G.M. Garrity (Eds.).
25. Liu J.-H., Wang Y.-X., Zhang X.-X., Wang Z.-G., Chen Y.-G., Wen M.-L., Xu L.-H., Peng Q., Cui X.-L. Salinarimonas rosea gen. nov., sp. nov., a new member of the {alpha}-2 subgroup of the Proteobacteria. Int. J. Syst. Evol. Microbiol. 2010, 60:55-60.
26. Ludwig W., Strunk O., Westram R., Richter L., Meier H., Yadhukumar Buchner A., Lai T., Steppi S., Jobb G., Forster W., Brettske I., Gerber S., Ginhart A.W., Gross O., Grumann S., Hermann S., Jost R., Konig A., Liss T., Lussmann R., May M., Nonhoff B., Reichel B., Strehlow R., Stamatakis A., Stuckmann N., Vilbig A., Lenke M., Ludwig T., Bode A., Schleifer K.H. ARB: a software environment for sequence data. Nucleic Acids Res. 2004, 32:1363-1371.
27. Martens M., Dawyndt P., Coopman R., Gillis M., De Vos P., Willems A. Advantages of multilocus sequence analysis for taxonomic studies: a case study using 10 housekeeping genes in the genus Ensifer (including former Sinorhizobium). Int. J. Syst. Evol. Microbiol. 2008, 58:200-214.
28. Martens M., Delaere M., Coopman R., De Vos P., Gillis M., Willems A. Multilocus sequence analysis of Ensifer and related taxa. Int. J. Syst. Evol. Microbiol. 2007, 57:489-503.
29. Menna P., Barcellos F.G., Hungria M. Phylogeny and taxonomy of a diverse collection of Bradyrhizobium strains based on multilocus sequence analysis of the 16S rRNA gene, ITS region and glnII, recA, atpD and dnaK genes. Int. J. Syst. Evol. Microbiol. 2009, 59:2934-2950.
30. Mesbah M., Premachandran U., Whitman W.B. Precise measurement of the G+C content of deoxyribonucleic-acid by high-performance liquid-chromatography. Int. J. Syst. Bacteriol. 1989, 39:159-167.
31. Meyer O.O. Genus VII. Oligotropha. Bergey's Manual of Systematic Bacteriology 2005, 468-470. Springer, New York. D.J. Brenner, N.R. Krieg, J.T. Staley, G.M. Garrity (Eds.).
32. Mhamdi R., Jebara M., Aouani M.E., Ghrir R., Mars M. Genotypic diversity and symbiotic effectiveness of rhizobia isolated from root nodules of Phaseolus vulgaris L. grown in Tunisian soils. Biol. Fertil. Soils 1999, 28:313-320.
33. Mierzwa B., Wdowiak-Wrobel S., Malek W. Phenotypic, genomic and phylogenetic characteristics of rhizobia isolated from root nodules of Robinia pseudoacacia (black locust) growing in Poland and Japan. Arch. Microbiol. 2009, 191:697-710.
34. Mierzwa B., Wdowiak-Wrobel S., Malek W. Robinia pseudoacacia in Poland and Japan is nodulated by Mesorhizobium amorphae strains. Antonie Van Leeuwenhoek. 2010, 97:351-361.
35. Noisangiam R., Nuntagij A., Pongsilp N., Boonkerd N., Denduangboripant J., Ronson C., Teaumroong N. Heavy metal tolerant Metalliresistens boonkerdii gen. nov., sp. nov., a new genus in the family Bradyrhizobiaceae isolated from soil in Thailand. Syst. Appl. Microbiol. 2010, 33:374-382.
36. Noisangiam R., Nuntagij A., Pongsilp N., Boonkerd N., Denduangboripant J., Ronson C., Teaumroong N. Erratum to Heavy metal tolerant Metalliresistens boonkerdii gen. nov., sp. nov., a new genus in the family Bradyrhizobiaceae isolated from soil in Thailand [Syst. Appl. Microbiol. 33 (2010) 374-382]. Proposal of Rhodopseudomonas boonkerdii sp. nov., a new heavy metal tolerant bacterium isolated from Thailand. Syst. Appl. Microbiol. 2011, 34:166-168.
37. Nzoué A., Miché L., Klonowska A., Laguerre G., de Lajudie P., Moulin L. Multilocus sequence analysis of bradyrhizobia isolated from Aeschynomene species in Senegal. Syst. Appl. Microbiol. 2009, 32:400-412.
38. Oda Y., Larimer F.W., Chain P.S.G., Malfatti S., Shin M.V., Vergez L.M., Hauser L., Land M.L., Braatsch S., Beatty J.T., Pelletier D.A., Schaefer A.L., Harwood C.S. Multiple genome sequences reveal adaptations of a phototrophic bacterium to sediment microenvironments. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:18543-18548.
39. Ohta H., Hattori T. Agromonas oligotrophica gen. nov., sp. nov., a nitrogen-fixing bacterium. Antonie Leeuwenhoek 1983, 49:429-446.
40. Okamura K., Takata K., Hiraishi A. Intrageneric relationships of members of the genus Rhodopseudomonas. J. Gen. Appl. Microbiol. 2009, 55:469-478.
41. Paul D., Kumar R., Nanduri B., French T., Pendarvis K., Brown A., Lawrence M.L., Burgess S.C. Proteome and membrane fatty acid analyses on Oligotropha carboxidovorans OM5 grown under chemolithoautotrophic and heterotrophic conditions. PLoS One 2011, 6:e17111.
42. Pruesse E., Quast C., Knittel K., Fuchs B.M., Ludwig W., Peplies J., Glöckner F.O. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res. 2007, 35:7188-7196.
43. Rivas R., Martens M., de Lajudie P., Willems A. Multilocus sequence analysis of the genus Bradyrhizobium. Syst. Appl. Microbiol. 2009, 32:101-110.
44. Saito A., Mitsui H., Hattori R., Minamisawa K., Hattori T. Slow-growing and oligotrophic soil bacteria phylogenetically close to Bradyrhizobium japonicum. FEMS Microbiol. Ecol. 1998, 25:277-286.
45. Seewaldt E., Schleifer K.H., Bock E., Stackebrandt E. The close relationship of Nitrobacter and Rhodopseudomonas palustris. Arch. Microbiol. 1982, 131:287-290.
46. Shiraishi A., Matsushita N., Hougetsu T. Nodulation in black locust by the Gammaproteobacteria Pseudomonas sp. and the Betaproteobacteria Burkholderia sp. Syst. Appl. Microbiol. 2010, 33:269-274.
47. Simon C., Wiezer A., Strittmatter A.W., Daniel R. Phylogenetic diversity and metabolic potential revealed in a glacier ice metagenome. Appl. Environ. Microbiol. 2009, 75:7519-7526.
48. Sorokin D.Y., Muyzer G., Brinkhoff T., Gijs Kuenen J., Jetten M.S.M. Isolation and characterization of a novel facultatively alkaliphilic Nitrobacter species, N. alkalicus sp. nov. Arch. Microbiol. 1998, 170:345-352.
49. Spieck E., Bock E. Genus VI. Nitrobacter. Bergey's Manual of Systematic Bacteriology 2005, 461-467. Springer, New York. D.J. Brenner, N.R. Krieg, J.T. Staley, G.M. Garrity (Eds.).
50. Stepkowski T., Czaplinska M., Miedzinska K., Moulin L. The variable part of the dnaK gene as an alternative marker for phylogenetic studies of rhizobia and related alpha Proteobacteria. Syst. Appl. Microbiol. 2003, 26:483-494.
51. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. MEGA5: Molecular evolutionary genetics analysis using Maximum Likelihood, evolutionary distance, and Maximum Parismony methods. Mol. Biol. Evol. 2011, 28:2731-2739.
52. Tindall B.J. A comparative study of the lipid composition of Halobacterium saccharovorum from various sources. Syst. Appl. Microbiol. 1990, 13:128-130.
53. Tindall B.J. Lipid composition of Halobacterium lacusprofundi. FEMS Microbiol. Lett. 1990, 66:199-202.
54. Ulrich A., Zaspel I. Phylogenetic diversity of rhizobial strains nodulating Robinia pseudoacacia L. Microbiology-Uk. 2000, 146:2997-3005.
55. Urdiain M., López-López A., Gonzalo C., Busse H.J., Langer S., Kämpfer P., Rosselló-Móra R. Reclassification of Rhodobium marinum and Rhodobium pfennigii as Afifella marina gen. nov comb. nov and Afifella pfennigii comb. nov., a new genus of photoheterotrophic Alphaproteobacteria and emended descriptions of Rhodobium, Rhodobium orientis and Rhodobium gokarnense. Syst. Appl. Microbiol. 2008, 31:339-351.
56. Van Berkum P., Lelbold J.M., Eardly B.D. Proposal for combining Bradyrhizobium spp. (Aeschynomene indica) with Blastobacter denitrificans and to transfer Blastobacter denitrificans (Hirsch and Muller, 1985) to the genus Bradyrhizobium as Bradyrhizobium denitrificans (comb. nov.). Syst. Appl. Microbiol. 2006, 29:207-215.
57. Vancanneyt M., Mengaud J., Cleenwerck I., Vanhonacker K., Hoste B., Dawyndt P., Degivry M.C., Ringuet D., Janssens D., Swings J. Reclassification of Lactobacillus kefirgranum Takizawa et al. 1994 as Lactobacillus kefiranofaciens subsp. kefirgranum subsp. nov. and emended description of L. kefiranofaciens Fujisawa et al. 1988. Int. J. Syst. Evol. Microbiol. 2004, 54:551-556.
58. Vauterin L., Yang P., Hoste B., Vancanneyt M., Civerolo E.L., Swings J., Kersters K. Differentiation of Xanthomonas campestris pv. citri strains by sodium dodecyl sulfate-polyacrylamide gel electrophoresis of proteins, fatty acid analysis, and DNA-DNA hybridization. Int. J. Syst. Bacteriol. 1991, 41:535-542.
59. Vincent, J.M. A manual for the practical study of the root-nodule bacteria. International Biological Programme Handbook, 15th ed., Oxford, UK Blackwell Scientific Pubilications.
60. Wei G.H., Chen W.M., Zhu W.F., Chen C., Young J.P.W., Bontemps C. Invasive Robinia pseudoacacia in China is nodulated by Mesorhizobium and Sinorhizobium species that share similar nodulation genes with native American symbionts. FEMS Microbiol. Ecol. 2009, 68:320-328.
61. Weyant R.S., Whitney A.M. Genus II. Afipia. Bergey's Manual of Systematic Bacteriology 2005, 443-447. Springer, New York. D.J. Brenner, N.R. Krieg, J.T. Staley, G.M. Garrity (Eds.).
62. Willems A., Gillis M., De Ley J. Transfer of Rhodocyclus gelatinosus to Rubrivivax gelatinosus gen. nov., comb. nov., and phylogenetic relationships with Leptothrix, Sphaerotilus natans, Pseudomonas saccharophila and Alcaligenes latus. Int. J. Syst. Bacteriol. 1991, 41:65-73.
63. Wilson K. Preparation of genomic DNA from bacteria. Current Protocols in Molecular Biology 1987, 241-245. Green Publishing and Wiley-Interscience, New York. F.M. Ausubel, R. Brent, R.E. Kimston, D.D. Moore, J.G. Seidman, J.A. Smith, K. Sthrul (Eds.).
64. Zhou P.F., Chen W.M., Wei G.H. Mesorhizobium robiniae sp. nov., isolated from root nodules of Robinia pseudoacacia. Int. J. Syst. Evol. Microbiol. 2010, 60:2552-2556.