Evidence for high-temperature in situ nifH transcription in an alkaline hot spring of Lower Geyser Basin, Yellowstone National Park

Environmental Microbiology

Volumn 14, Issue 5, 2012, Pages 1272-1283

  Loiacono, Sara T ^a   Meyer Dombard, D'Arcy R ^a   Havig, Jeff R ^b   Poret Peterson, Amisha T ^b   Hartnett, Hilairy E ^b,c   Shock, Everett L ^b,c  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b ARIZONA STATE UNIVERSITY   (United States)

^c ARIZONA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NITROGEN; NITROGENASE REDUCTASE; OXIDOREDUCTASE;

ARTICLE; BACTERIUM; BIOFILM; ENVIRONMENT; GENETIC VARIABILITY; GENETICS; HEAT; METABOLISM; MICROBIOLOGY; NITROGEN FIXATION; PH; PHYLOGENY; SEDIMENT; THERMAL SPRING; UNITED STATES;

BACTERIA; BIOFILMS; ENVIRONMENT; GENETIC VARIATION; GEOLOGIC SEDIMENTS; HOT SPRINGS; HOT TEMPERATURE; HYDROGEN-ION CONCENTRATION; NITROGEN FIXATION; NITROGEN ISOTOPES; OXIDOREDUCTASES; PHYLOGENY; WYOMING;

EID: 84859975517     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2012.02710.x     Document Type: Article

References (40)

1. Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
2. Bishop, P.E., Jarlenski, D.M.L., and Hetherington, D.R. (1982) Expression of an alternative nitrogen fixation system in Azotobacter vinelandii. J Bacteriol 150: 1244-1251.
3. Brigle, K.E., Newton, W.E., and Dean, D.R. (1985) Complete nucleotide-sequence of the Azotobacter vinelandii nitrogenase structural gene cluster. Gene 37: 37-44.
4. Bürgmann, H., Widmer, F., Sigler, W.V., and Zeyer, J. (2003) mRNA extraction and reverse transcription-PCR protocol for detection of nifH gene expression by Azotobacter vinelandii in soil. Appl Environ Microbiol 69: 1928-1935.
5. Burr, M.D., Botero, L.M., Young, M.J., Inskeep, W.P., and McDermott, T.R. (2005) Observations concerning nitrogen cycling in a Yellowstone thermal soil environment. In Geothermal Biology and Geochemistry in Yellowstone National Park. Inskeep, W.P., and McDermott, T.R. (eds). Bozeman, USA: Thermal Biology Institute, Montana State University, pp. 171-182.
6. Delwiche, C.C., and Steyn, P.L. (1970) Nitrogen isotope fractionation in soils and microbial reactions. Environ Sci Technol 4: 929-935.
7. Dixon, R., and Kahn, D. (2004) Genetic regulation of biological nitrogen fixation. Nat Rev Microbiol 2: 621-631.
8. 2 regulate nitrogenase activity in cell extracts of Methanococcus maripaludis. Mol Microbiol 56: 1527-1538.
9. Fournier, R.O. (2005) Geochemistry and dynamics of the Yellowstone National Park hydrothermal system. In Geothermal Biology and Geochemistry in Yellowstone National Park. Inskeep, W.P., and McDermott, T.R. (eds). Bozeman, USA: Thermal Biology Institute, Montana State University, pp. 3-30.
10. Gallon, J.R. (1981) The oxygen sensitivity of nitrogenase: a problem for biochemists and micro-organisms. Trends Biochem Sci 6: 19-23.
11. Halbleib, C.M., and Ludden, P.W. (2000) Regulation of biological nitrogen fixation. J Nutr 130: 1081-1084.
12. Hall, J.R., Mitchell, K.R., Jackson-Weaver, O., Kooser, A.S., Cron, B.R., Crossey, L.J., and Takacs-Vesbach, C.D. (2008) Molecular characterization of the diversity and distribution of a thermal spring microbial community by using rRNA and metabolic genes. Appl Environ Microbiol 74: 4910-4922.
13. Hamilton, T.L., Boyd, E.S., and Peters, J.W. (2011a) Environmental constraints underpin the distribution and phylogenetic diversity of nifH in the Yellowstone geothermal complex. Microbiol Ecol 61: 860-870.
14. Hamilton, T.L., Lange, R.K., Boyd, E.S., and Peters, J.W. (2011b) Biological nitrogen fixation in acidic high-temperature geothermal springs in Yellowstone National Park, Wyoming. Environ Microbiol 13: 2204-2215.
15. Havig, J.R., Raymond, J., Meyer-Dombard, D.R., Zolotova, N., and Shock, E.L. (2011) Merging isotopes and community genomics in a siliceous sinter-depositing hot spring. J Geophys Res 116: G001005.
16. Holl, C.M., and Montoya, J.P. (2005) Interactions between nitrate uptake and nitrogen fixation in continuous cultures of the marine diazotroph Trichodesmium (Cyanobacteria). J Phycol 41: 1178-1183.
17. Hoover, T. (2000) Control of nitrogen fixation genes in Klebsiella pneumonia. In Prokaryotic Nitrogen Fixation. Triplett, E.W. (ed.). Norfolk, UK: Horizon Scientific Press, pp. 131-147.
18. Huber, T., Faulkner, G., and Hugenholtz, P. (2004) Bellerophon: a program to detect chimeric sequences in multiple sequence alignments. Bioinformatics 20: 2317-2319.
19. Lane, D.J. (1991) 16S/23S rRNA sequencing. In Nucleic Acid Techniques in Bacterial Systematics. Stackebrandt, E., and Goodfellow, M. (eds). Chichester, UK: John Wiley and Sons, pp. 115-175.
20. Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., etal. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
21. Lotta, M., Beatriz, D., Ingvild, W., Zheng, W.W., El-Shehawy, R., and Rasmussen, U. (2009) Diazotrophic diversity, nifH gene expression and nitrogenase activity in a rice paddy field in Fujian, China. Plant Soil 325: 207-218.
22. Macko, S.A., Fogel, M.L., Hare, P.E., and Hoering, T.C. (1987) Isotopic fractionation of nitrogen and carbon in the synthesis of amino acids by microorganisms. Chem Geol 65: 79-92.
23. Mariotti, A., Germon, J.C., Hubert, P., Kaiser, P., Letolle, R., Tardieux, A., and Tardieux, P. (1981) Experimental determination of nitrogen kinetic isotope fractionation: some principles; illustration for the denitrification and nitrification processes. Plant Soil 62: 413-430.
24. Mehta, M.P., and Baross, J.A. (2006) Nitrogen fixation at 92°C by a hydrothermal vent archaeon. Science 314: 1783-1786.
25. Mehta, M.P., Butterfield, D.A., and Baross, J.A. (2003) Phylogenetic diversity of nitrogenase (nifH) genes in deep-sea and hydrothermal vent environments of the Juan de Fuca ridge. Appl Environ Microbiol 69: 960-970.
26. Meyer-Dombard, D.R., Shock, E.L., and Amend, J.P. (2005) Archaeal and bacterial communities in geochemically diverse hot springs of Yellowstone National Park, USA. Geobiology 3: 211-227.
27. Meyer-Dombard, D.R., Swingley, W., Raymond, J., Havig, J., Shock, E.L., and Summons, R.E. (2011) Hydrothermal ecotones and streamer biofilm communities in the Lower Geyser Basin, Yellowstone National Park. Environ Microbiol 13: 2216-2231.
28. Mulholland, M.R., Ohki, K., and Capone, D.G. (2001) Nutrient controls on nitrogen uptake and metabolism by natural populations and cultures of Trichodesmium (Cyanobacteria). J Phycol 37: 1001-1009.
29. Normand, P., and Bousquet, J. (1989) Phylogeny of nitrogenase sequences in Frankia and other nitrogen-fixing microorganisms. J Mol Evol 29: 436-447.
30. Poly, F., Monrozier, L.J., and Bally, R. (2001) Improvement in the RFLP procedure for studying the diversity of nifH genes in communities of nitrogen fixers in soil. Res Microbiol 152: 95-103.
31. Rabouille, S., Staal, M., Stal, L.J., and Soetaert, K. (2006) Modeling the dynamic regulation of nitrogen fixation in the cyanobacterium Trichodesmium sp. Appl Environ Microbiol 72: 3217-3227.
32. Rosado, A.S., Duarte, G.F., Seldin, L., and van Elsas, 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.
33. Severin, I., and Stal, L.J. (2010) NifH expression by five groups of phototrophs compared with nitrogenase activity in coastal microbial mats. FEMS Microbiol Ecol 73: 55-67.
34. Shock, E.L., Holland, M., Meyer-Dombard, D.R., and Amend, J.P. (2005) Geochemical sources of energy for microbial metabolism in hydrothermal ecosystems: Obsidian Pool, Yellowstone National Park. In Geothermal Biology and Geochemistry in Yellowstone National Park. Inskeep, W.P., and McDermott, T.R. (eds). Bozeman, USA: Thermal Biology Institute, Montana State University, pp. 95-109.
35. Shock, E.L., Holland, M., Meyer-Dombard, D., Amend, J.P., Osburn, G.R., and Fischer, T.P. (2010) Quantifying inorganic sources of geochemical energy in hydrothermal ecosystems, Yellowstone National Park, USA. Geochim Cosmochim Acta 74: 4005-4043.
36. Steunou, A.S., Bhaya, D., Bateson, M.M., Melendrez, M.C., Ward, D.M., Brecht, E., etal. (2006) In situ analysis of nitrogen fixation and metabolic switching in unicellular thermophilic cyanobacteria inhabiting hot spring microbial mats. Proc Natl Acad Sci USA 103: 2398-2403.
37. 2 fixation over the diel cycle in a hot spring microbial mat. ISME J 2: 364-378.
38. 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 by reverse transcriptase PCR. Appl Environ Microbiol 66: 3119-3124.
39. Zehr, J.P., and McReynolds, L.A. (1989) Use of degenerate oligonucleotides for amplification of the nifH gene from the marine cyanobacterium Trichodesmium thiebautii. Appl Environ Microbiol 55: 2522-2526.
40. Zehr, J.P., Jenkins, B.D., Short, S.M., and Steward, G.F. (2003) Nitrogenase gene diversity and microbial community structure: a cross-system comparison. Environ Microbiol 5: 539-554.