Change in Land Use Alters the Diversity and Composition of Bradyrhizobium Communities and Led to the Introduction of Rhizobium etli into the Tropical Rain Forest of Los Tuxtlas (Mexico)

Microbial Ecology

Volumn 63, Issue 4, 2012, Pages 822-834

  Ormeño Orrillo, Ernesto ^a,b   Rogel Hernández, Marco A ^b   Lloret, Lourdes ^b   López López, Aline ^b   Martínez, Julio ^b   Barois, Isabelle ^a   Martínez Romero, Esperanza ^b  

^a INSTITUTO DE ECOLOGÍA   (Mexico)

^b INSTITUTO DE CIENCIAS FÍSICAS   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; RAIN; RIBOSOME DNA; RNA 16S;

AGRICULTURE; ARTICLE; BRADYRHIZOBIUM; CLASSIFICATION; DNA SEQUENCE; ECOSYSTEM; FORESTRY; GENETICS; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; MEXICO; MICROBIOLOGY; PHYLOGENY; RHIZOBIUM ETLI; SYMBIOSIS; TREE; TROPIC CLIMATE;

AGRICULTURE; BACTERIAL PROTEINS; BRADYRHIZOBIUM; DNA, RIBOSOMAL; ECOSYSTEM; FORESTRY; MEXICO; PHYLOGENY; RAIN; RHIZOBIUM ETLI; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SOIL MICROBIOLOGY; SYMBIOSIS; TREES; TROPICAL CLIMATE;

BACTERIA (MICROORGANISMS); BRADYRHIZOBIACEAE; BRADYRHIZOBIUM; PHASEOLUS VULGARIS; RHIZOBIACEAE; RHIZOBIUM ETLI; ZEA MAYS;

EID: 84864316880     PISSN: 00953628     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00248-011-9974-9     Document Type: Article

References (89)

1. Giller KE, Cadisch G (1995) Future benefits from biological nitrogen fixation: an ecological approach to agriculture. Plant Soil 174: 255-277.
2. Giller KE (2001) Nitrogen fixation in tropical cropping systems. CABI, Wallington.
3. Crews TE (1999) The presence of nitrogen fixing legumes in terrestrial communities: evolutionary vs ecological considerations. Biogeochemistry 46: 233-246.
4. Sprent J (2005) West African legumes: the role of nodulation and nitrogen fixation. New Phytol 167: 326-330.
5. Willems A (2006) The taxonomy of rhizobia: an overview. Plant Soil 287: 3-14.
6. Chen WM, Laevens S, Lee TM, Coenye T, De Vos P, Mergeay M, Vandamme P (2001) Ralstonia taiwanensis sp. nov., isolated from root nodules of Mimosa species and sputum of a cystic fibrosis patient. Int J Syst Evol Microbiol 51: 1729-1735.
7. Moulin L, Munive A, Dreyfus B, Boivin-Masson C (2001) Nodulation of legumes by members of the beta-subclass of Proteobacteria. Nature 411: 948-950.
8. Parker MA (2008) Symbiotic relationships of legumes and nodule bacteria on Barro Colorado Island, Panama: a review. Microb Ecol 55: 662-672.
9. Parker MA (2004) rRNA and dnaK relationships of Bradyrhizobium sp. nodule bacteria from four papilionoid legume trees in Costa Rica. Syst Appl Microbiol 27: 334-342.
10. Koponen P, Nygren P, Domenach AM, Le Roux C, Saur E, Roggy JC (2003) Nodulation and dinitrogen fixation of legume trees in a tropical freshwater swamp forest in French Guiana. J Trop Ecol 19: 655-666.
11. Moreira FM, Haukka K, Young JP (1998) Biodiversity of rhizobia isolated from a wide range of forest legumes in Brazil. Mol Ecol 7: 889-895.
12. Guevara S, Laborde J, Sánchez-Ríos G (2004) Los Tuxtlas. El Paisaje de la Sierra. Instituto de Ecología, A. C, Xalapa.
13. Martínez-Romero E (2003) Diversity of Rhizobium-Phaseolus vulgaris symbiosis: overview and perspectives. Plant Soil 252: 11-23.
14. Strobel G, Daisy B (2003) Bioprospecting for microbial endophytes and their natural products. Microbiol Mol Biol Rev 67: 491-502.
15. Borneman J, Triplett E (1997) Molecular microbial diversity in soils from eastern Amazonia: evidence for unusual microorganisms and microbial population shifts associated with deforestation. Appl Environ Microbiol 63: 2647-2653.
16. Upchurch R, Chiu C-Y, Everett K, Dyszynski G, Coleman DC, Whitman WB (2008) Differences in the composition and diversity of bacterial communities from agricultural and forest soils. Soil Biol Biochem 40: 1294-1305.
17. Chim Chan O, Casper P, Sha LQ, Feng ZL, Fu Y, Yang XD, Ulrich A, Zou XM (2008) Vegetation cover of forest, shrub and pasture strongly influences soil bacterial community structure as revealed by 16S rRNA gene T-RFLP analysis. FEMS Microbiol Ecol 64: 449-458.
18. Jangid K, Williams MA, Franzluebbers AJ, Sanderlin JS, Reeves JH, Jenkins MB, Endale DM, Coleman DC, Whitman WB (2008) Relative impacts of land-use, management intensity and fertilization upon soil microbial community structure in agricultural systems. Soil Biol Biochem 40: 2843-2853.
19. Hartmann M, Lee S, Hallam SJ, Mohn WW (2009) Bacterial, archaeal and eukaryal community structures throughout soil horizons of harvested and naturally disturbed forest stands. Environ Microbiol 11: 3045-3062.
20. da C Jesus E, Marsh TL, Tiedje JM, de S Moreira FM (2009) Changes in land use alter the structure of bacterial communities in Western Amazon soils. ISME J 3: 1004-1011.
21. Faoro H, Alves AC, Souza EM, Rigo LU, Cruz LM, Al-Janabi SM, Monteiro RA, Baura VA, Pedrosa FO (2010) Influence of soil characteristics on the diversity of bacteria in the Southern Brazilian Atlantic Forest. Appl Environ Microbiol 76: 4744-4749.
22. Nusslein K, Tiedje JM (1999) Soil bacterial community shift correlated with change from forest to pasture vegetation in a tropical soil. Appl Environ Microbiol 65: 3622-3626.
23. Carney KM, Matson PA, Bohannan BJM (2004) Diversity and composition of tropical soil nitrifiers across a plant diversity gradient and among land-use types. Ecol Lett 7: 684-694.
24. Knief C, Vanitchung S, Harvey NW, Conrad R, Dunfield PF, Chidthaisong A (2005) Diversity of methanotrophic bacteria in tropical upland soils under different land uses. Appl Environ Microbiol 71: 3826-3831.
25. Bala A, Giller KE (2001) Symbiotic specificity of tropical tree rhizobia for host legumes. New Phytol 149: 495-507.
26. Thies JE, Bohlool BB, Singleton PW (1991) Subgroups of the cowpea miscellany: symbiotic specificity within Bradyrhizobium spp. for Vigna unguiculata, Phaseolus lunatus, Arachis hypogaea, and Macroptilium atropurpureum. Appl Environ Microbiol 57: 1540-1545.
27. Lewin A, Rosenberg C, Meyer ZAH, Wong CH, Nelson L, Manen JF, Stanley J, Dowling DN, Denarie J, Broughton WJ (1987) Multiple host-specificity loci of the broad host-range Rhizobium sp. NGR234 selected using the widely compatible legume Vigna unguiculata. Plant Mol Biol 8: 447-459.
28. Vincent JM (1970) A manual for the practical study of root nodule bacteria. Blackwell, Oxford.
29. Fahraeus G (1957) The infection of clover root hairs by nodule bacteria studied by a simple glass slide technique. J Gen Microbiol 16: 374-381.
30. Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173: 697-703.
31. Versalovic J, Schneider M, De Bruijn FJ, Lupski JR (1994) Genomic fingerprinting of bacteria using repetitive sequence-based polymerase chain reaction. Methods Mol Cell Biol 5: 25-40.
32. Haukka K, Lindstrom K, Young JP (1998) 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 64: 419-426.
33. Eardly BD, Young JP, Selander RK (1992) Phylogenetic position of Rhizobium sp. strain Or 191, a symbiont of both Medicago sativa and Phaseolus vulgaris, based on partial sequences of the 16S rRNA and nifH genes. Appl Environ Microbiol 58: 1809-1815.
34. Hollis AB, Kloos WE, Elkan GH (1981) DNA: DNA hybridization studies of Rhizobiurn japonicum and related Rhizobiaceae. J Gen Microbiol 123: 215-222.
35. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2. 0. Bioinformatics 23: 2947-2948.
36. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41: 95-98.
37. 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.
38. Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3. 0. Syst Biol 59: 307-321.
39. Desper R, Gascuel O (2002) Fast and accurate phylogeny reconstruction algorithms based on the minimum-evolution principle. J Comput Biol 9: 687-705.
40. Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25: 1253-1256.
41. Willems A, Munive A, de Lajudie P, Gillis M (2003) In most Bradyrhizobium groups sequence comparison of 16S-23S rDNA internal transcribed spacer regions corroborates DNA-DNA hybridizations. Syst Appl Microbiol 26: 203-210.
42. Willems A, Coopman R, Gillis M (2001) Phylogenetic and DNA-DNA hybridization analyses of Bradyrhizobium species. Int J Syst Evol Microbiol 51: 111-117.
43. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75: 7537-7541.
44. Rivas R, Martens M, de Lajudie P, Willems A (2009) Multilocus sequence analysis of the genus Bradyrhizobium. Syst Appl Microbiol 32: 101-110.
45. Ribeiro RA, Rogel MA, Lopez-Lopez A, Ormeno-Orrillo E, Gomes Barcellos F, Martinez J, Lopes Thompson F, Martinez-Romero E, Hungria M (2011) Reclassification of Rhizobium tropici type A strains as Rhizobium leucaenae sp. nov. Int J Syst Evol Microbiol In Press.
46. Good IL (1953) The population frequencies of species and the estimation of population parameters. Biometrika 80: 193-201.
47. Chao A (1987) Estimating the population size for capture-recapture data with unequal catchability. Biometrics 43: 783-791.
48. Chao A, Lee S-M (1992) Estimating the number of classes via sample coverage. J Am Stat Assoc 87: 210-217.
49. Magurran AE (1988) Ecological diversity and its measurement. Chapman, London.
50. Chao A, Chazdon RL, Colwell RK, Shen T-J (2005) A new statistical approach for assessing similarity of species composition with incidence and abundance data. Ecol Lett 8: 148-159.
51. Wolfe R, Hanley J (2002) If we're so different, why do we keep overlapping? When 1 plus 1 doesn't make 2. CMAJ 166: 65-66.
52. Jordan DC (1984) Family III. Rhizobiaceae Conn 1938. In: Krieg NR, Holt JG (eds) Bergey's manual of systematic bacteriology, vol 1. Williams & Wilkins, Baltimore, pp 234-235.
53. Grossman JM, Sheaffer C, Wyse D, Graham PH (2005) Characterization of slow-growing root nodule bacteria from Inga oerstediana in organic coffee agroecosystems in Chiapas, Mexico. Appl Soil Ecol 29: 236-251.
54. Hughes RF, Kauffman JB, Jaramillo VJ (1999) Biomass, carbon, and nutrient dynamics of secondary forests in a humid tropical region of Mexico. Ecology 80: 1892-1907.
55. Sprent JI (2007) Evolving ideas of legume evolution and diversity: a taxonomic perspective on the occurrence of nodulation. New Phytol 174: 11-25.
56. Sprent J (2005) Nodulated legume trees. In: Werner D, Newton W (eds) Nitrogen fixation in agriculture, forestry, ecology, and the environment, vol 4. Springer, Dordrecht, pp 113-141.
57. Sprent J (2001) Nodulation in legumes. Cromwell, Kew.
58. Bongers F, Popma J, del Castillo JM, Carabias J (1998) Structure and floristic composition of the lowland rain forest of Los Tuxtlas, Mexico. Vegetatio 74: 55-80.
59. Vázquez-Torres M, Onaindia M (2008) Tree canopy composition in the tropical mountain rain forest of Los Tuxtlas, Mexico. Rev Biol Trop 56: 1571-1579.
60. Parker MA (2003) Genetic markers for analysing symbiotic relationships and lateral gene transfer in neotropical bradyrhizobia. Mol Ecol 12: 2447-2455.
61. Ramirez-Bahena MH, Peix A, Rivas R, Camacho M, Rodriguez-Navarro DN, Mateos PF, Martinez-Molina E, Willems A, Velazquez E (2009) Bradyrhizobium pachyrhizi sp. nov. and Bradyrhizobium jicamae sp. nov., isolated from effective nodules of Pachyrhizus erosus. Int J Syst Evol Microbiol 59: 1929-1934.
62. Parker MA (2003) A widespread neotropical Bradyrhizobium lineage associated with Machaerium and Desmodium (Papilionoideae). Plant Soil 254: 263-268.
63. Menna P, Barcellos FG, Hungria M (2009) 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 59: 2934-2950.
64. Steenkamp ET, Stepkowski T, Przymusiak A, Botha WJ, Law IJ (2008) Cowpea and peanut in southern Africa are nodulated by diverse Bradyrhizobium strains harboring nodulation genes that belong to the large pantropical clade common in Africa. Mol Phylogenet Evol 48: 1131-1144.
65. Wang ET, Rogel MA, Garcia-de los Santos A, Martinez-Romero J, Cevallos MA, Martinez-Romero E (1999) Rhizobium etli bv. mimosae, a novel biovar isolated from Mimosa affinis. Int J Syst Bacteriol 49(Pt 4): 1479-1491.
66. Lira-Noriega A, Guevara S, Laborde J, Sánchez-Rios G (2007) Composición florística en potreros de Los Tuxtlas, Veracruz, México. Acta Botánica Mexicana 80: 59-87.
67. Gonzalez V, Acosta JL, Santamaria RI, Bustos P, Fernandez JL, Hernandez Gonzalez IL, Diaz R, Flores M, Palacios R, Mora J, Davila G (2010) Conserved symbiotic plasmid DNA sequences in the multireplicon pangenomic structure of Rhizobium etli. Appl Environ Microbiol 76: 1604-1614.
68. Ferreira MC, Andrade DS, Chueire LMO, Takemura SM, Hungria M (2000) Tillage method and crop rotation effects on the population sizes and diversity of bradyrhizobia nodulating soybean. Soil Biol Biochem 32: 627-637.
69. Caballero-Mellado J, Martinez-Romero E (1999) Soil fertilization limits the genetic diversity of Rhizobium in bean nodules. Symbiosis 26: 111-121.
70. Labes G, Ulrich A, Lentzsch P (1996) Influence of bovine slurry deposition on the structure of nodulating Rhizobium leguminosarum bv. viciae soil populations in a natural habitat. Appl Environ Microbiol 62: 1717-1722.
71. Fox JE, Gulledge J, Engelhaupt E, Burow ME, McLachlan JA (2007) Pesticides reduce symbiotic efficiency of nitrogen-fixing rhizobia and host plants. Proc Natl Acad Sci 104: 10282-10287.
72. Ramos MLG, Ribeiro WQ (1993) Effect of fungicides on survival of Rhizobium on seeds and the nodulation of bean (Phaseolus vulgaris L.). Plant Soil 152: 145-150.
73. Ormeño-Orrillo E, Rosenblueth M, Luyten E, Vanderleyden J, Martínez-Romero E (2008) Mutations in lipopolysaccharide biosynthetic genes impair maize rhizosphere and root colonization of Rhizobium tropici CIAT899. Environ Microbiol 10: 1271-1284.
74. Mitchell R, Hester A, Campbell C, Chapman S, Cameron C, Hewison R, Potts J (2010) Is vegetation composition or soil chemistry the best predictor of the soil microbial community? Plant Soil 333: 417-430.
75. Guevara S, Laborde J, Sánchez-Rios G (2004) Rain forest regeneration beneath the canopy of fig trees isolated in pastures of Los Tuxtlas, Mexico. Biotropica 36: 99-108.
76. Purata SE (1986) Floristic and structural changes during old-field succession in the Mexican tropics in relation to site history and species availability. J Trop Ecol 2: 257-276.
77. Davidson EA, Reis De Carvalho CJ, Vieira ICG, Figueiredo RDO, Moutinho P, Ishida FY, Dos Santos MTP, Guerrero JB, Kalif K, Saba RT (2004) Nitrogen and phosphorus limitation of biomass growth in a tropical secondary forest. Ecol Appl 14: S150-S163.
78. Gehring C, Vlek PLG, De Souza LAG, Denich M (2005) Biological nitrogen fixation in secondary regrowth and mature rainforest of central Amazonia. Agric Ecosyst Environ 111: 237-252.
79. Postma J, Hok-A-Hin CH, van Veen JA (1990) Role of microniches in protecting introduced Rhizobium leguminosarum biovar trifolii against competition and predation in soil. Appl Environ Microbiol 56: 495-502.
80. Wang ET, Martínez-Romero J, Martínez-Romero E (1999) Genetic diversity of rhizobia from Leucaena leucocephala nodules in Mexican soils. Mol Ecol 8: 711-724.
81. Gutierrez-Zamora ML, Martínez-Romero E (2001) Natural endophytic association between Rhizobium etli and maize (Zea mays L.). J Biotechnol 91: 117-126.
82. Rosenblueth M, Martinez-Romero E (2004) Rhizobium etli maize populations and their competitiveness for root colonization. Arch Microbiol 181: 337-344.
83. Hallmann J, Quadt-Hallmann A, Miller WG, Sikora RA, Lindow SE (2001) Endophytic colonization of plants by the biocontrol agent Rhizobium etli G12 in relation to Meloidogyne incognita infection. Phytopathology 91: 415-422.
84. Hernández-Lucas I, Segovia L, Martínez-Romero E, Pueppke SG (1995) Phylogenetic relationships and host range of Rhizobium spp. that nodulate Phaseolus vulgaris L. Appl Environ Microbiol 61: 2775-2779.
85. Chen WX, Tan ZY, Gao JL, Li Y, Wang ET (1997) Rhizobium hainanense sp. nov., isolated from tropical legumes. Int J Syst Bacteriol 47: 870-873.
86. Elliott GN, Chen WM, Bontemps C, Chou JH, Young JP, Sprent JI, James EK (2007) Nodulation of Cyclopia spp. (Leguminosae, Papilionoideae) by Burkholderia tuberum. Ann Bot 100: 1403-1411.
87. Lopez-Lopez A, Rogel-Hernandez MA, Barois I, Ortiz Ceballos AI, Martinez J, Ormeno-Orrillo E, Martinez-Romero E (2011) Rhizobium grahamii sp. nov. from Dalea leporina, Leucaena leucocephala, Clitoria ternatea nodules, and Rhizobium mesoamericanum sp. nov. from Phaseolus vulgaris, siratro, cowpea and Mimosa pudica nodules. Int J Syst Evol Microbiol In Press.
88. Estrada A, Cammarano P, Coates-Estrada R (2000) Bird species richness in vegetation fences and in strips of residual rain forest vegetation at Los Tuxtlas, Mexico. Biodivers Conserv 9: 1399-1416.
89. Acosta-Durán C, Martínez-Romero E (2002) Diversity of rhizobia from nodules of the leguminous tree Gliricidia sepium, a natural host of Rhizobium tropici. Arch Microbiol 178: 161-164.