Nitrogenase gene diversity and microbial community structure: A cross-system comparison

Environmental Microbiology

Volumn 5, Issue 7, 2003, Pages 539-554

  Zehr, Jonathan P ^a   Jenkins, Bethany D ^a   Short, Steven M ^a   Steward, Grieg F ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF HAWAII   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARCHAEA; BACTERIA; ECOSYSTEM; ENVIRONMENTAL MICROBIOLOGY; EURYARCHAEOTA; GENE TRANSFER, HORIZONTAL; GENES, ARCHAEAL; GENES, BACTERIAL; NITROGEN FIXATION; NITROGENASE; OXIDOREDUCTASES; PHYLOGENY; VARIATION (GENETICS);

ARCHAEA; ISOPTERA; PROKARYOTA;

EID: 0038234799     PISSN: 14622912     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1462-2920.2003.00451.x     Document Type: Short Survey

References (88)

1. Affourtit, J., Zehr, J.P., and Paerl, H.W. (2001) Distribution of nitrogen-fixing microorganisms along the Neuse River Estuary, North Carolina. Microb Ecol 41: 114-123.
2. Arp, D.J. (2000) The nitrogen cycle. In Prokaryotic Nitrogen Fixation. Triplett, E.W. (ed). Wymondham, Great Britain: Horizon Scientific Press, pp. 1-14.
3. Atlas, R.M., and Bartha, R. (1998) Microbial Ecology: Fundamentals and Applications. Menlo Park, California: Addison-Wesley Longman.
4. Auman, A.J., Speake, C.C., and Lidstrom, M.E. (2001) nifH sequences and nitrogen fixation in type I and type II methanotrophs. Appl Environ Microbiol 67: 4009-4016.
5. Bagwell, C.E., and Lovell, C.R. (2000) Persistence of selected Spartina alterniflora rhizoplane diazotrophs exposed to natural and manipulated environmental variability. Appl Environ Microbiol 66: 4625-4633.
6. Bagwell, C.E., Piceno, Y.M., Ashburne-Lucas, A., and Lovell, C.R. (1998) Physiological diversity of the rhizosphere diazotroph assemblages of selected salt marsh grasses. Appl Environ Microbiol 64: 4276-4282.
7. Barbour, W.M., Wang, S.-P., and Stacey, G. (1992) Molecular genetics of Bradyrhizobium symbioses. In Biological Nitrogen Fixation. Stacey, G., Evans, H.J., and Burris, R.H. (eds). New York: Chapman & Hall, pp. 43-86.
8. Beeson, K.E., Erdner, D.L., Bagwell, C.E., Lovell, C.R., and Sobecky, P.A. (2002) Differentiation of plasmids in marine diazotroph assemblages determined by randomly amplified polymorphic DNA analysis. Microbiology-Sgm 148: 179-189.
9. Bergholz, P.W., Bagwell, C.E., and Lovell, C.R. (2001) Physiological diversity of rhizoplane diazotrophs of the salt-meadow cordgrass, Spartina patens: Implications for host specific ecotypes. Microbial Ecol 42: 466-473.
10. Bishop, P.E., Premakumar, R., Dean, D.R., Jacobsen, M.R., Chisnell, J.R., Rizzo, T.M., and Kopczynski, J. (1985) Nitrogen fixation by Azotobacter vinelandii strains having deletions in structural genes for nitrogenase. Science: 92-94.
11. Braun, S., Proctor, L., Zani, S., Mellon, M.T., and Zehr, J.P. (1999) Molecular evidence for zooplankton-associated nitrogen-fixing anaerobes based on amplification of the nifH gene. FEMS Microbiol Ecol 28: 273-279.
12. Bull, A.T., Ward, A.C., and Goodfellow, M. (2000) Search and discovery strategies for biotechnology: The paradigm shift. Microbiol Mol Biol Rev 64: 573-606,CP573.
13. Burgess, B.K., and Lowe, D.J. (1996) Mechanism of molybdenum nitrogenase. Chem Rev 96: 2983-3011.
14. Burns, J.A., Zehr, J.P., and Capone, D.G. (2002) Nitrogen fixing phylotypes of Chesapeake Bay and Neuse River Estuary sediments. Microb Ecol 44: 336-343.
15. Cavalier-Smith, T. (2002) The neomuran origin of archaebacteria, the negibacterial root of the universal tree and bacterial megaclassification. Int J Syst Evol Microbiol 52: 7-76.
16. Chen, Y.-B., Dominic, B., Mellon, M.T., and Zehr, J.P. (1998) Circadian rhythm of nitrogenase gene expression in the diazotrophic filamentous nonheterocystous cyanobacterium Trichodesmium sp. Strain IMS 101. J Bacteriol 180: 3598-3605.
17. Chien, Y.-T., and Zinder, S.H. (1996) Cloning, functional organization, transcript studies, and phylogenetic analysis of the complete nitrogenase structural genes (nifHDK2) and associated genes in the archaeon Methanosarcina barkeri 227. J Bacteriol 178: 143-148.
18. Chien, Y.T., Auerbuch, V., Brabban, A.D., and Zinder, S.H. (2000) Analysis of genes encoding an alternative nitrogenase in the archaeon Methanosarcina barkeri 227. J Bacteriol 182: 3247-3253.
19. Cho, J.C., and Tiedje, J.M. (2000) Biogeography and degree of endemicity of fluorescent Pseudomonas strains in soil. Appl Environ Microbiol 66: 5448-5456.
20. Des Marais, D.J., and Walter, M.R. (1999) Astrobiology: Exploring the origins, evolution, and distribution of life in the Universe. Ann Rev Ecol Syst 30: 397-420.
21. Dicker, H., and Smith, D. (1980) Acetylene reduction (nitrogen fixation) in a Delaware, USA salt marsh. Mar Biol 57: 241-250.
22. Dominic, B., Zani, S., Chen, Y.-B., Mellon, M.T., and Zehr, J.P. (2000) Organization of the nif genes of the nonheterocystous cyanobacterium Trichodesmium sp. IMS101. J Phycol 36: 693-701.
23. Doolittle, W.F. (1999) Lateral genomics. Trends Biochem Sci 24: M5-M8.
24. Dyble, J., Paerl, H.W., and Neilan, B.A. (2002) Genetic characterization of Cylindrospermopsis raciborskii (Cyanobacteria) isolates from diverse geographic origins based on nifH and cpcBA-IGS nucleotide sequence analysis. Appl Environ Microbiol 68: 2567-2571.
25. Eady, R.R. (1996) Structure-function relationships of alternative nitrogenases. Chem Rev 96: 3013-3030.
26. Egener, T., Hurek, T., and Reinhold-Hurek, B. (1998) Use of green fluorescent protein to detect expression of nif genes of Azoarcus sp. BH72, a grass-associated diazotroph, on rice roots. Mol Plant-Microbe Interacts 11: 71-75.
27. Egener, T., Hurek, T., and Reinhold-Hurek, B. (1999) Endophytic expression of nif genes of Azoarcus sp strain BH72 in rice roots. Mol Plant-Microbe Interacts 12: 813-819.
28. Hamelin, J., Fromin, N., Tarnawski, S., Teyssier-Cuvelle, S., and Aragno, M. (2002) nifH gene diversity in the bacterial community associated with the rhizosphere of Molinia coerulea, an oligonitrophilic perennial grass. Environ Microbiol 4: 477-481.
29. Hirsch, AM., McKhann, H.I., Reddy, A., Liao, J., Fang, Y., and Marshall, C.R. (1995) Assessing horizontal transfer of nifHDK genes in eubacteria: Nucleotide sequence of nifK from Frankia Strain HFPCcl3. Mol Biol Evol 12: 16-27.
30. Hoover, T. (2000) Control of nitrogen fixation genes in Klebsiella pneumoniae. In Prokaryotic Nitrogen Fixation. Triplett, E.W. (ed). Norfolk, England: Horizon Scientific Press, pp. 131-147.
31. Howard, J.B., and Rees, D.C. (1996) Structural basis of biological nitrogen fixation. Chem Rev 96: 2965-2982.
32. Howarth, R.W., and Marino, R. (1988) Nitrogen fixation in freshwater, estuarine, and marine ecosystems. 2. Biogeochemical controls. Limnol Oceanogr 33: 688-701.
33. Humayoun, S.B., Bano, N., and Hollibaugh, J.T. (2003) Depth distribution of microbial diversity in a meromictic lake; Mono Lake, California. Appl Environ Microbiol 69: 1030-1042.
34. Hurek, T., Egener, T., and Reinhold-Hurek, B. (1997) Divergence in nitrogenases of Azoarcus spp., Proteobacteria of the beta subclass. J Bacteriol 179: 4172-4178.
35. Hurek, T., Handley, L.L., Reinhold-Hurek, B., and Piche, Y. (2002) Azoarcus grass endophytes contribute fixed nitrogen to the plant in an unculturable state. Mol Plant-Microbe Interacts 15: 233-242.
36. Jellison, R., and Melack, J.M. (2001) Nitrogen limitation and particulate elemental ratios of seston in hypersaline Mono Lake, California, USA. Hydrobiologia 466: 1-12.
37. Karl, D.M., and Michaels, A.F. (1996) The Hawaiian Ocean Time-Series (Hot) and Bermuda Atlantic Time-Series Study (Bats) - Preface. Deep-Sea Res Part II-Top St Oce 43: 127-128.
38. Kent, H.M., Buck, M., and Evans, D.J. (1989) Cloning and sequencing of the nifH gene of Desulfovibrio gigas. FEMS Microbiol Lett 61: 73-78.
39. Kim, K., Zhang, Y.P., and Roberts, G.P. (1999) Correlation of activity regulation and substrate recognition of the ADP-ribosyltransferase that regulates nitrogenase activity in Rhodospirillum rubrum. J Bacteriol 181: 1698-1702.
40. Klein, M., Friedrich, M., Roger, A.J., Hugenholtz, P., Fishbain, S., Abicht, H., et al. (2001) Multiple lateral transfers of dissimilatory sulfite reductase genes between major lineages of sulfate-reducing prokaryotes. J Bacteriol 183: 6028-6035.
41. Lilburn, T.C., Kim, K.S., Ostrom, N.E., Byzek, K.R., Leadbetter, J.R., and Breznak, J.A. (2001) Nitrogen fixation by symbiotic and free-living spirochetes. Science 292: 2495-2498.
42. Loveless, T.M., and Bishop, P.E. (1999) Identification of genes unique to Mo-independent nitrogenase systems in diverse diazotrophs. Can J Microbiol 45: 312-317.
43. Lovell, C.R., Piceno, Y.M., Quattro, J.M., and Bagwell, C.E. (2000) Molecular analysis of diazotroph diversity in the rhizosphere of the smooth cordgrass, Spartina alterniflora. Appl Environ Microbiol 66: 3814-3822.
44. Lovell, C.R., Friez, M.J., Longshore, J.W., and Bagwell, C.E. (2001) Recovery and phylogenetic analysis of nifH sequences from diazotrophic bacteria associated with dead aboveground biomass of Spartina alterniflora. Appl Environ Microbiol 67: 5308-5314.
45. Madigan, M.T., Martinko, J.M., and Parker, J. (2000) Brock Biology of Microorganisms. Upper Saddle River, New Jersey: Prentice Hall.
46. Maidak, B.L., Cole, J.R., Lilburn, T.G., Parker, C.T.J.P., Farris, R.J. et al. (2001) The RDP-II (Ribosomal Database Project). Nucleic Acids Res 29: 173-174.
47. Methe, B.A., Hiorns, W.D., and Zehr, J.P. (1998) Contrasts between marine and freshwater bacterial community composition: analyses of communities in Lake George, New York and six other Adirondack lakes. Limnol Oceanogr 43: 368-374.
48. Mullins, T.D., Britschgi, T.B., Krest, R.L., and Giovannoni, S.J. (1995) Genetic comparisons reveal the same unknown bacterial lineages in Atlantic and Pacific bacterioplankton communities. Limnol Oceanogr 40: 148-158.
49. Nesbo, C.L., L'Haridon, S., Stetter, K.O., and Doolittle, W.F. (2001) Phylogenetic analyses of two 'Archaeal' genes in Thermotoga maritima reveal multiple transfers between Archaea and Bacteria. Mol Biol Evol 18: 362-375.
50. Noda, S., Ohkuma, M., Usami, R., Horikoshi, K., and Kudo, T. (1999) Culture-independent characterization of a gene responsible for nitrogen fixation in the symbiotic microbial community in the gut of the termite Neotermes koshunensis. Appl Environ Microbiol 65: 4935-4942.
51. Ohkuma, M., Noda, S., Usami, R., Horikoshi, K., and Kudo, T. (1996) Diversity of nitrogen fixation genes in the symbiotic intestinal microflora of the termite Reticulitermes speratus. Appl Environ Microbiol 62: 2747-2752.
52. Ohkuma, M., Noda, S., and Kudo, T. (1999) Phylogenetic diversity of nitrogen fixation genes in the symbiotic microbial community in the gut of diverse termites. Appl Environ Microbiol 65: 4926-4934.
53. Olson, J.B., Litaker, R.W., and Paerl, H.W. (1999) Ubiquity of heterotrophic diazotrophs in marine microbial mats. Aquat Micr Ecol 19: 29-36.
54. Pace, N.R. (1997) A molecular view of microbial diversity and the biosphere. Science 276: 734-740.
55. Paerl, H.W. (1988) Nuisance phytoplankton blooms in coastal, estuarine, and inland waters. Limnol Oceanogr 33: 823-847.
56. Piceno, Y.M., and Lovell, C.R. (2000a) Stability in natural bacterial communities. II. Plant resource allocation effects on rhizosphere diazotroph assemblage composition. Microb Ecol 39: 41-48.
57. Piceno, Y.M., and Lovell, C.R. (2000b) Stability in natural bacterial communities. I. Nutrient addition effects on rhizosphere diazotroph assemblage composition. Microb Ecol 39: 32-40.
58. Poly, F., Monrozier, L.J., and Bally, R. (2001a) Improvement in the RFLP procedure for studying the diversity of nifH genes in communities of nitrogen fixers in soil. Res Microbiol 152: 95-103.
59. Poly, F., Ranjard, L., Nazaret, S., Gourbiere, F., and Monrozier, L.J. (2001b) Comparison of nifH gene pools in soils and soil microenvironments with contrasting properties. Appl Environ Microbiol 67: 2255-2262.
60. Postgate, J.R., and Eady, R.R. (1988) The evolution of biological nitrogen fixation. In Nitrogen Fixation: Hundred Years After. Bothe, H., de Bruijn, F.J, and Newton, W.E. (eds). Stuttgart: Gustav Fischer, pp. 31-40.
61. Rappe, M.S., Connon, S.A., Vergin, K.L., and Giovannoni, S.J. (2002) Cultivation of the ubiquitous SAR11 marine bacterioplankton clade. Nature 418: 630-633.
62. Redfield, A.C. (1958) The biological control of chemical factors in the environment. Am Scientist 46: 205-222.
63. 2 by a molybdenum-CO dehydrogenase. J Biol Chem 272: 26627-26633.
64. Rosado, A.S., Duarte, G.F., Seldin, L., and VanElsas, J.D. (1998) Genetic diversity of nifH gene sequences in Paenibacillus azotofixans strains and soil samples analyzed by denaturing gradient gel electrophoresis of PCR-amplified gene fragments. Appl Environ Microbiol 64: 2770-2779.
65. 2 fixing bacteria in forests and clearcuts in western Oregon. Microb Ecol 39: 12-21.
66. Simonet, P., Grosjean, M.C., Misra, A.K., Nazaret, S., Cournoyer, B., and Normand, P. (1991) Frankia genus-specific characterization by polymerase chain reaction. Appl Environ Microbiol 57: 3278-3286.
67. 2 fixation by sulfate-reducing bacteria in a marine intertidal microbial mat. Aquat Micr Ecol 28: 1-12.
68. 2 fixation - A strategy for meeting nitrogen requirements of marine and terrestrial cyanobacterial mats. FEMS Microbiol Ecol 21: 149-156.
69. Steppe, T.F., Pinckney, J.L., Dyble, J., and Paerl, H.W. (2001) Diazotrophy in modern marine Bahamian stromatolites. Microb Ecol 41: 36-44.
70. Strunk, O. and Ludwig, W. (1993) The ARB-Project: A software environment for sequence data (Munich, Germany). http://www.arb-home.de.
71. Tamas, I., Svircev, Z., and Andersson, S.G.E. (2000) Determinative value of a portion of the nifH sequence for the genera Nostoc and Anabaena (Cyanobacteria). Current Microbiol 41: 197-200.
72. Tan, Z.Y., Hurek, T., Vinuesa, P., Muller, P., Ladha, J.K., and Reinhold-Hurek, B. (2001) Specific detection of Bradyrhizobium and Rhizobium strains colonizing rice (Oryza sativa) roots by 16S-23S ribosomal DNA intergenic spacer-targeted PCR. Appl Environ Microbiol 67: 3655-3664.
73. Thiel, T. (1993) Characterization of genes for an alternative nitrogenase in the cyanobacterium Anabaena variabilis. J Bacteriol 175: 6276-6286.
74. Thiel, T., Lyons, E.M., Erker, J.C., and Ernst, A. (1995) A second nitrogenase in vegetative cells of a heterocyst-forming cyanobacterium. Proc Natl Acad Sci USA 92: 9358-9362.
75. 2 fixing bacterial diversity detected in rice roots by molecular evolutionary analysis of nifH gene sequences. J Bacteriol 177: 1414-1417.
76. 2 fixing bacteria associated with rice roots by molecular evolutionary analysis of a nifD library. Can J Microbiol 41: 235-240.
77. Vitousek, P.M. (1999) Nutrient limitation to nitrogen fixation in young volcanic sites. Ecosystems 2: 505-510.
78. Vitousek, P.M., and Howarth, R.W. (1991) Nitrogen limitation on land and in the sea: How can it occur? Biogeochemistry 13: 87-115.
79. Wang, S., Chen, J., and Johnson, J.L. (1988) The presence of five nifH-like sequences in Clostridium pasteurianum: sequence divergence and transcription properties. Nucleic Acids Res 16: 439-454.
80. Wu, J., Sunda, W., Boyle, E.A., and Karl, D.M. (2000) Phosphate depletion in the western North Atlantic Ocean. Science 289: 759-762.
81. Young, J.P.W. (1992) Phylogenetic classification of nitrogen-fixing organisms. In Biological Nitrogen Fixation. Stacey, G., Evans, H.J., and Burris, R.H. (eds). New York: Chapman & Hall, pp. 43-86.
82. Zani, S., Mellon, M.T., Collier, J.L., and Zehr, J.P. (2000) Expression of nifH genes in natural microbial assemblages in Lake George, New York detected with RT-PCR. Appl Environ Microbiol 66: 3119-3124.
83. Zehr, J.P., and Capone, D.G. (1996) Problems and promises of assaying the genetic potential for nitrogen fixation in the marine environment. Microb Ecol 32: 263-281.
84. Zehr, J.P., and McReynolds, L.A. (1989) Use of degenerate oligonucleotides for amplification of the nifH gene from the marine cyanobacterium Trichodesmium spp. Appl Environ Microbiol 55: 2522-2526.
85. Zehr, J.P., Mellon, M., Braun, S., Litaker, W., Steppe, T., and Paerl, H.W. (1995) Diversity of heterotrophic nitrogen fixation genes in a marine cyanobacterial mat. Appl Environ Microbiol 61: 2527-2532.
86. Zehr, J.P., Mellon, M.T., and Hiorns, W.D. (1997) Phylogeny of cyanobacterial nifH genes: evolutionary implications and potential applications to natural assemblages. Microbiology 143: 1443-1450.
87. Zehr, J.P., Mellon, M.T., and Zani, S. (1998) New nitrogen fixing microorganisms detected in oligotrophic oceans by the amplification of nitrogenase (nifH) genes. Appl Environ Microbiol 64: 3444-3450.
88. 2 in the subtropical North Pacific Ocean. Nature 412: 635-638.