Heavy metal tolerant Metalliresistens boonkerdii gen. nov., sp. nov., a new genus in the family Bradyrhizobiaceae isolated from soil in Thailand

Systematic and Applied Microbiology

Volumn 33, Issue 7, 2010, Pages 374-382

  Noisangiam, Rujirek ^a   Nuntagij, Achara ^b   Pongsilp, Neelawan ^c   Boonkerd, Nantakorn ^a   Denduangboripant, Jessada ^d   Ronson, Clive ^e   Teaumroong, Neung ^a  

^a SURANAREE UNIVERSITY OF TECHNOLOGY   (Thailand)

^b Soil Microbiology Research Group   (Thailand)

^c SILPAKORN UNIVERSITY   (Thailand)

^d CHULALONGKORN UNIVERSITY   (Thailand)

^e UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

Bradyrhizobiaceae; Heavy metal tolerance; Housekeeping genes; Metalliresistens boonkerdii; Multilocus sequence analysis; Phylogenetic analysis

Indexed keywords

HEAVY METAL; RNA 16S;

ARTICLE; BACTERIAL STRAIN; BACTERIUM ISOLATE; BRADYRHIZOBIACEAE; BRADYRHIZOBIUM; CLONING; FATTY ACID ANALYSIS; GENE SEQUENCE; METALLIRESISTENS BOONKERDII; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PHYLOGENY; PRIORITY JOURNAL; RHODOPSEUDOMONAS; SOIL; THAILAND;

BACTERIAL PROTEINS; BACTERIAL TYPING TECHNIQUES; BASE COMPOSITION; BASE SEQUENCE; BRADYRHIZOBIACEAE; COBALT; CULTURE MEDIA; DNA, BACTERIAL; DRUG RESISTANCE, BACTERIAL; FATTY ACIDS; GENES, RRNA; METALS, HEAVY; MOLECULAR SEQUENCE DATA; MULTILOCUS SEQUENCE TYPING; PHENOTYPE; PHYLOGENY; POLYMERASE CHAIN REACTION; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SOIL MICROBIOLOGY; SOYBEANS; SPECIES SPECIFICITY; SYMBIOSIS; THAILAND; ZINC;

BACTERIA (MICROORGANISMS); BRADYRHIZOBIACEAE; BRADYRHIZOBIUM; BRADYRHIZOBIUM ELKANII; BRADYRHIZOBIUM JAPONICUM; GLYCINE MAX; RHODOPSEUDOMONAS; UNCULTURED BACTERIUM;

EID: 78249267220     PISSN: 07232020     EISSN: 16180984     Source Type: Journal    
DOI: 10.1016/j.syapm.2010.06.002     Document Type: Article

References (69)

1. Bao Z., Sato Y., Kubota M., Ohta H. Isolation and characterization of thallium-tolerant bacteria from heavy metal-polluted river sediment and non-polluted soils. Microbes Environ. 2006, 21:251-260.
2. Barrett C.F., Parker M.A. Coexistence of Burkholderia, Cupriavidus, and Rhizobium sp. nodule bacteria on two Mimosa spp. in Costa Rica. Appl. Environ. Microbiol. 2006, 72:1198-1206.
3. Béjà O., Suzuki M.T., Heidelberg J.F., Nelson W.C., Preston C.M., Hamada T., Eisen J.A., Fraser C.M., DeLong E.F. Unsuspected diversity among marine aerobic anoxygenic phototrophs. Nature 2002, 415:630-633.
4. Bott M., Bolliger M., Hennecke H. Genetic analysis of the cytochrome c-aa3 branch of the Bradyrhizobium japonicum respiratory chain. Mol. Microbiol. 1990, 4:2147-2157.
5. 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.
6. Cashion P., Holder-Franklin M.A., McCully J., Franklin M. A rapid method for the base ratio determination of bacterial DNA. Anal. Biochem. 1977, 81:461-466.
7. Chen W.-M., James E.K., Coenye T., Chou J.-H., Barrios E., de Faria S.M., Elliott G.N., Sheu S.-Y., Sprent J.I., Vandamme P. Burkholderia mimosarum sp. nov., isolated from root nodules of Mimosa spp. from Taiwan and South America. Int. J. Syst. Evol. Microbiol. 2006, 56:1847-1851.
8. Chen W.X., Yan G.H., Li J.L. Numerical taxonomic study of fast-growing soybean rhizobia and a proposal that Rhizobium fredii be assigned to Sinorhizobium gen. nov. Int. J. Syst. Bacteriol. 1988, 38:392-397.
9. Das S.K., Mishra A.K., Tindall B.J., Rainey F.A., Stackebrandt E. Oxidation of thiosulfate by a new bacterium, Bosea thiooxidans.(strain BI-42) gen. nov., sp. nov.: analysis of phylogeny based on chemotaxonomy and 16S ribosomal DNA sequencing. Int. J. Syst. Evol. Microbiol. 1996, 46:981-987.
10. de Lajudie P., Laurent-Fulele E., Willems A., Torek U., Coopman R., Collins M.D., Kersters K., Dreyfus B., Gillis M. Allorhizobium undicola gen. nov., sp. nov., nitrogen-fixing bacteria that efficiently nodulate Neptunia natans in Senegal. Int. J. Syst. Evol. Microbiol. 1998, 48:1277-1290.
11. Dereeper A., Guignon V., Blanc G., Audic S., Buffet S., Chevenet F., Dufayard J.F., Guindon S., Lefort V., Lescot M. Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 2008, 1-5.
12. 2-fixing rhizobium: characteristics. Nitrogen Fixation: Achievements and Objectives 1990, 805-811. Chapman and Hall, New York. P.M. Gresshoff, L.E. Roth, G. Stacey, W.L. Newton (Eds.).
13. Ehrich S., Behrens D., Lebedeva E., Ludwig W., Bock E. A new obligately chemolithoautotrophic, nitrite-oxidizing bacterium, Nitrospira moscoviensis sp. nov. and its phylogenetic relationship. Arch. Microbiol. 1995, 164:16-23.
14. Eisen J.A. The RecA protein as a model molecule for molecular systematic studies of bacteria: comparison of trees of RecAs and 16S rRNAs from the same species. J. Mol. Evol. 1995, 41:1105-1123.
15. Elkan G.H. Taxonomy of the rhizobia. Can. J. Microbiol. 1992, 38:446-450.
16. Fleischman D.E., Evans W.R., Miller I.M. Bacteriochlorophyll-containing Rhizobium Species 1995, Kluwer Academic Publishers, Dordrecht.
17. Garrity, G. M., Bell, J. A. and Lilburn, T. (2005) Family VII. Bradyrhizobiaceae fam. nov. in: Garrity, G M, Brenner, D J, Krieg, N R and Staley, J R (Eds.), Bergey's Manual of Systematic Bacteriology, The Proteobacteria, part C: The Alpha-, Beta-, Delta-, and Epsilonproteobacteria, vol. 2, Springer, New York, pp. 438-476.
18. Guindon S., Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 2003, 52:696-704.
19. Inui M., Roh J.H., Zahn K., Yukawa H. Sequence analysis of the cryptic plasmid pMG101 from Rhodopseudomonas palustris and construction of stable cloning vectors. Appl. Environ. Microbiol. 2000, 66:54-63.
20. Jordan D.C. Transfer of Rhizobium japonicum Buchanan 1980 to Bradyrhizobium gen. nov., a genus of slow-growing, root nodule bacteria from leguminous plants. Int. J. Syst. Bacteriol. 1982, 32:136-139.
21. Karlin S., Weinstock G.M., Brendel V. Bacterial classifications derived from RecA protein sequence comparisons. J. Bacteriol. 1995, 177:6881-6893.
22. Khamis A., Colson P., Raoult D., Scola B.L. Usefulness of rpoB gene sequencing for identification of Afipia and Bosea species, including a strategy for choosing discriminative partial sequences. Appl. Environ. Microbiol. 2003, 69:6740-6749.
23. Kompantseva E.I., Imhoff J.F., Thiemann B., Panteleeva E.E., Akimov V.N. Comparative study of the fatty acid composition of some groups of purple nonsulfur bacteria. Microbiology 2007, 76:541-551.
24. Kumar S., Nei M., Dudley J., Tamura K. MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform. 2008.
25. Kuykendall L.D., Roy M.A., O'neill J.J., Devine T.E. Fatty acids, antibiotic resistance, and deoxyribonucleic acid homology groups of Bradyrhizobium japonicum. Int. J. Syst. Evol. Microbiol. 1988, 38:358-361.
26. La Duc M.T., Nicholson W., Kern R., Venkateswaran K. Microbial characterization of the Mars Odyssey spacecraft and its encapsulation facility. Environ. Microbiol. 2003, 5:977-985.
27. Laguerre G., Bardin M., Amarger N. Isolation from soil of symbiotic and non-symbiotic Rhizobium leguminosarum by DNA hybridization. Can. J. Microbiol./Rev. Can. Microbiol. 1993, 39:1142-1149.
28. Lane D.J., Pace B., Olsen G.J., Stahl D.A., Sogin M.L., Pace N.R. Rapid determination of 16S ribosomal RNA sequences for phylogenetic analyses. Proc. Natl. Acad. Sci. U.S.A. 1985, 82:6955-6959.
29. Lorquin J., Molouba F., Dreyfus B. Identification of the carotenoid pigment canthaxanthin from photosynthetic Bradyrhizobium strains. Appl. Environ. Microbiol. 1997, 63:1151-1154.
30. Manassila M., Nuntagij A., Kotepong S., Boonkerd N., Teaumroong N. Characterization and monitoring of selected rhizobial strains isolated from tree legumes in Thailand. Afr. J. Biotechnol. 2007, 6:1393-1402.
31. 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.
32. 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.
33. 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. Evol. Microbiol. 1989, 39:159-167.
34. Miller L.T. Single derivatization method for routine analysis of bacterial whole-cell fatty acid methyl esters, including hydroxy acids. J. Clin. Microbiol. 1982, 16:584-586.
35. Moulin L., Munive A., Dreyfus B., Boivin-Masson C. Nodulation of legumes by members of the beta-subclass of Proteobacteria. Nature 2001, 411:948-950.
36. Parker M.A. rRNA and dnaK relationships of Bradyrhizobium sp. nodule bacteria from four papilionoid legume trees in Costa Rica. Syst. Appl. Microbiol. 2004, 27:334-342.
37. Pfennig N., Truper H.G. Type and neotype strains of the species of phototrophic bacteria maintained in pure culture. Int. J. Syst. Evol. Microbiol. 1971, 21:19-24.
38. Pongsilp N., Teaumroong N., Nuntagij A., Boonkerd N., Sadowsky M. Genetic structure of indigenous non-nodulating and nodulation populations of Bradyrhizobia in soil from Thailand. Symbiosis 2002, 33:39-58.
39. Rao J.R., Cooper J.E. Rhizobia catabolize nod gene-inducing flavonoids via C-ring fission mechanisms. J. Bacteriol. 1994, 176:5409-5413.
40. Rivas R., Martens M., de Lajudie P., Willems A. Multilocus sequence analysis of the genus Bradyrhizobium. Syst. Appl. Microbiol. 2009, 32:101-110.
41. Roca A., Cox M. RecA protein: structure, function, and role in recombinational DNA repair. Prog. Nucleic Acid Res. Mol. Biol. 1997, 56:129-224.
42. 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.
43. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 1987, 4:406-425.
44. Sameshima R., Isawa T., Sadowsky M.J., Hamada T., Kasai H., Shutsrirung A., Mitsui H., Minamisawa K. Phylogeny and distribution of extra-slow-growing Bradyrhizobium japonicum harboring high copy numbers of RS[alpha], RS[beta] and IS1631. FEMS Microbiol. Ecol. 2003, 44:191-202.
45. Sasser, M. (1990) Identification of bacteria by gas chromatography of cellular fatty acids, in, MIDI Technical Note.
46. Sawada H., Kuykendall L., Young J. Changing concepts in the systematics of bacterial nitrogen-fixing legume symbionts. J. Gen. Appl. Microbiol. 2003, 49:155-179.
47. Seewaldt E., Schleifer K.H., Bock E., Stackebrandt E. The close phylogenetic relationship of Nitrobacter and Rhodopseudomonas palustris. Arch. Microbiol. 1982, 131:287-290.
48. Segovia L., Pinero D., Palacios R., Martinez-Romero E. Genetic structure of a soil population of non-symbiotic Rhizobium leguminosarum. Appl. Environ. Microbiol. 1991, 57:426-433.
49. Soberon-Chavez G., Najera R. Isolation from soil of Rhizobium leguminosarum lacking symbiotic information. Can. J. Microbiol. 1989, 35:464-468.
50. Somasegaran P., Hoben H.J. Handbook for Rhizobia: Methods in Legume-rhizobium Technology 1994, Springer-Verlag, Heidelberg, Germany.
51. Stackebrandt E., Frederiksen W., Garrity G.M., Grimont P.A.D., Kampfer P., Maiden M.C.J., Nesme X., Rossello-Mora R., Swings J., Truper H.G. Report of the ad hoc committee for the re-evaluation of the species definition in bacteriology. Int. J. Syst. Evol. Microbiol. 2002, 52:1043-1047.
52. Stackebrandt E., Goebel B.M. Taxonomic note: a place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int. J. Syst. Evol. Microbiol. 1994, 44:846-849.
53. Sullivan J.T., Eardly B.D., van Berkum P., Ronson C.W. Four unnamed species of non-symbiotic rhizobia isolated from the rhizosphere of Lotus corniculatus. Appl. Environ. Microbiol. 1996, 62:2818-2825.
54. Sullivan J.T., Patrick H.N., Lowther W.L., Scott D.B., Ronson C.W. Nodulating strains of Rhizobium loti arise through chromosomal symbiotic gene transfer in the environment. Proc. Natl. Acad. Sci. U.S.A. 1995, 92:8985-8989.
55. Tighe S.W., de Lajudie P., Dipietro K., Lindstrom K., Nick G., Jarvis B.D.W. Analysis of cellular fatty acids and phenotypic relationships of Agrobacterium, Bradyrhizobium, Mesorhizobium, Rhizobium and Sinorhizobium species using the Sherlock Microbial Identification System. Int. J. Syst. Evol. Microbiol. 2000, 50:787-801.
56. Tong Z., Sadowsky M.J. A Selective medium for the isolation and quantification of Bradyrhizobium japonicum and Bradyrhizobium elkanii strains from soils and inoculants. Appl. Environ. Microbiol. 1994, 60:581-586.
57. van Berkum P., Elia P., Eardly B.D. Multilocus sequence typing as an approach for population analysis of Medicago-nodulating rhizobia. J. Bacteriol. 2006, 188:5570-5577.
58. van Niel C.B. The culture, general physiology, morphology, and classification of the non-sulfur purple and brown bacteria. Bacteriol. Rev. 1944, 8:1-118.
59. Vinuesa P., Rademaker J.L., de Bruijn F.J., Werner D. Genotypic characterization of Bradyrhizobium strains nodulating endemic woody legumes of the Canary Islands by PCR-restriction fragment length polymorphism analysis of genes encoding 16S rRNA (16S rDNA) and 16S-23S rDNA intergenic spacers, repetitive extragenic palindromic PCR genomic fingerprinting, and partial 16S rDNA sequencing. Appl. Environ. Microbiol. 1998, 64:2096-2104.
60. Vinuesa P., Rojas-Jimenez K., Contreras-Moreira B., Mahna S.K., Prasad B.N., Moe H., Selvaraju S.B., Thierfelder H., Werner D. Multilocus sequence analysis for assessment of the biogeography and evolutionary genetics of four Bradyrhizobium species that nodulate soybeans on the Asiatic continent. Appl. Environ. Microbiol. 2008, 74:6987-6996.
61. Vinuesa P., Silva C., Werner D., Martinez-Romero E. Population genetics and phylogenetic inference in bacterial molecular systematics: the roles of migration and recombination in Bradyrhizobium species cohesion and delineation. Mol. Phylogenet. Evol. 2005, 34:29-54.
62. West N.J., Obernosterer I., Zemb O., Lebaron P. Major differences of bacterial diversity and activity inside and outside of a natural iron-fertilized phytoplankton bloom in the Southern Ocean. Environ. Microbiol. 2008, 10:738-756.
63. Willems A., Collins M.D. Evidence for a close genealogical relationship between Afipia (the causal organism of cat scratch disease), Bradyrhizobium japonicum and Blastobacter denitrificans. FEMS Microbiol. Lett. 1992, 96:241-246.
64. Willems A., Doignon-Bourcier F., Goris J., Coopman R., De Lajudie P., De Vos P., Gillis M. DNA-DNA hybridization study of Bradyrhizobium strains. Int. J. Syst. Evol. Microbiol. 2001, 51:1315-1322.
65. Woese C.R., Stackebrandt E., Weisburg W.G., Paster B.J., Madigan M.T., Fowler V.J., Hahn C.M., Blanz P., Gupta R., Nealson K.H. The phylogeny of purple bacteria: the alpha subdivision. Syst. Appl. Microbiol. 1984, 5:315-326.
66. Wolde-meskel E., Terefework Z., Lindstrom K., Frostegard A. Metabolic and genomic diversity of rhizobia isolated from field standing native and exotic woody legumes in southern Ethiopia. Syst. Appl. Microbiol. 2004, 27:603-611.
67. Wong F.Y.K., Stackebrandt E., Ladha J.K., Fleischman D.E., Date R.A., Fuerst J.A. Phylogenetic analysis of Bradyrhizobium japonicum and photosynthetic stem-nodulating bacteria from Aeschynomene species grown in separated geographical regions. Appl. Environ. Microbiol. 1994, 60:940-946.
68. Young J.P., Downer H.L., Eardly B.D. Phylogeny of the phototrophic Rhizobium strain BTAi1 by polymerase chain reaction-based sequencing of a 16S rRNA gene segment. J. Bacteriol. 1991, 173:2271-2277.
69. Yutin N., Suzuki M.T., Rosenberg M., Rotem D., Madigan M.T., Süling J., Imhoff J.F., Béjà O. BchY-based degenerate primers target all types of anoxygenic photosynthetic bacteria in a single PCR. Appl. Environ. Microbiol. 2009, 75:7556-7559.