Regulation of nif gene expression and the energetics of N2 fixation over the diel cycle in a hot spring microbial mat
Tóm tắt
Nitrogen fixation, a prokaryotic, O2-inhibited process that reduces N2 gas to biomass, is of paramount importance in biogeochemical cycling of nitrogen. We analyzed the levels of nif transcripts of Synechococcus ecotypes, NifH subunit and nitrogenase activity over the diel cycle in the microbial mat of an alkaline hot spring in Yellowstone National Park. The results showed a rise in nif transcripts in the evening, with a subsequent decline over the course of the night. In contrast, immunological data demonstrated that the level of the NifH polypeptide remained stable during the night, and only declined when the mat became oxic in the morning. Nitrogenase activity was low throughout the night; however, it exhibited two peaks, a small one in the evening and a large one in the early morning, when light began to stimulate cyanobacterial photosynthetic activity, but O2 consumption by respiration still exceeded the rate of O2 evolution. Once the irradiance increased to the point at which the mat became oxic, the nitrogenase activity was strongly inhibited. Transcripts for proteins associated with energy-producing metabolisms in the cell also followed diel patterns, with fermentation-related transcripts accumulating at night, photosynthesis- and respiration-related transcripts accumulating during the day and late afternoon, respectively. These results are discussed with respect to the energetics and regulation of N2 fixation in hot spring mats and factors that can markedly influence the extent of N2 fixation over the diel cycle.
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Allewalt, 2006, Effect of temperature and light on growth of and photosynthesis by Synechococcus isolates typical of those predominating in the octopus spring microbial mat community of Yellowstone National Park, Appl Environ Microbiol, 72, 544, 10.1128/AEM.72.1.544-550.2006
Anderson, 1987, Formation and fate of fermentation products in hot spring cyanobacterial mats, Appl Environ Microbiol, 53, 2343, 10.1128/aem.53.10.2343-2352.1987
Bebout, 1993, Identification of the sources of energy for nitrogen fixation and physiological characterization of nitrogen-fixing members of a marine microbial mat community, Appl Environ Microbiol, 59, 1495, 10.1128/aem.59.5.1495-1503.1993
Bell-Pedersen, 2005, Circadian rhythms from multiple oscillators: lessons from diverse organisms, Nat Rev Genet, 6, 544, 10.1038/nrg1633
Berman-Frank, 2001, Segregation of nitrogen fixation and oxygenic photosynthesis in the marine cyanobacterium Trichodesmium, Science, 294, 1534, 10.1126/science.1064082
Bhaya, 2008, Population level functional diversity in a microbial community revealed by comparative genomic and metagenomic analyses, ISMEJ, 100, 207
Boomer, 2002, Molecular characterization of novel red green nonsulfur bacteria from five distinct hot spring communities in Yellowstone National Park, Appl Environ Microbiol, 68, 346, 10.1128/AEM.68.1.346-355.2002
Cady, 1996, Fossilization processes in siliceous thermal springs: trends in preservation along the thermal gradient, Ciba Found Symp, 202, 150
Canfield, 1993, Biogeochemical cycles of carbon, sulfur, and free oxygen in a microbial mat, Geochim Cosmochim Acta, 57, 3971, 10.1016/0016-7037(93)90347-Y
Carpenter, 1976, Marine Oscillatoria (Trichodesmium): explanation for aerobic nitrogen fixation without heterocysts, Science, 191, 1278, 10.1126/science.1257749
Des Marais, 2003, Biogeochemistry of hypersaline microbial mats illustrates the dynamics of modern microbial ecosystems and the early evolution of the biosphere, Biol Bull, 204, 160, 10.2307/1543552
Dillon, 2007, High rates of sulfate reduction in a low-sulfate hot spring microbial mat are driven by a low level of diversity of sulfate-respiring microorganisms, Appl Environ Microbiol, 73, 5218, 10.1128/AEM.00357-07
Elsen, 2000, Expression of uptake hydrogenase and molybdenum nitrogenase in Rhodobacter capsulatus is coregulated by the RegB-RegA two-component regulatory system, J Bacteriol, 182, 2831, 10.1128/JB.182.10.2831-2837.2000
Elsen, 2004, RegB/RegA, a highly conserved redox-responding global two-component regulatory system, Microbiol Mol Biol Rev, 68, 263, 10.1128/MMBR.68.2.263-279.2004
Farmer, 1997, Fossilization of coniform (Phormidium) stromatolites in siliceous thermal springs, Yellowstone National Park, GSA (abs), 29, 295
Fay, 1992, Oxygen relations of nitrogen fixation in cyanobacteria, Microbiol Rev, 56, 340, 10.1128/mr.56.2.340-373.1992
Ferris, 1997, Seasonal distributions of dominant 16S rRNA-defined populations in a hot spring microbial mat examined by denaturing gradient gel electrophoresis, Appl Environ Microbiol, 63, 1375, 10.1128/aem.63.4.1375-1381.1997
Ghirardi, 2007, Hydrogenases and hydrogen photoproduction in oxygenic photosynthetic organisms, Annu Rev Plant Biol, 58, 71, 10.1146/annurev.arplant.58.032806.103848
Golden, 2003, Heterocyst development in Anabaena, Curr Opin Microbiol, 6, 557, 10.1016/j.mib.2003.10.004
Han, 1996, Temperature dependence of oxygen diffusion in H2O and D2O, J Phys Chem, 100, 5597, 10.1021/jp952903y
Hanada, 1997, Porphyrobacter tepidarius sp. nov., a moderately thermophilic aerobic photosynthetic bacterium isolated from a hot spring, Int J Syst Bacteriol, 47, 408, 10.1099/00207713-47-2-408
Hanada, 2002, Roseiflexus castenholzii gen. nov., sp. nov., a thermophilic, filamentous, photosynthetic bacterium that lacks chlorosomes, Int J Syst Evol Microbiol, 52, 187, 10.1099/00207713-52-1-187
Hoehler, 2001, The role of microbial mats in the production of reduced gases on the early Earth, Nature, 412, 324, 10.1038/35085554
Hu, 2004, Characterization of Azotobacter vinelandii nifZ deletion strains. Indication of stepwise MoFe protein assembly, J Biol Chem, 279, 54963, 10.1074/jbc.M408983200
Huang, 1999, Organization and expression of nitrogen-fixation genes in the aerobic nitrogen-fixing unicellular cyanobacterium Synechococcus sp. strain RF-1, Microbiology, 145, 743, 10.1099/13500872-145-3-743
Jacobson, 1989, Biochemical and genetic analysis of the nifUSVWZM cluster from Azotobacter vinelandii, Mol Gen Genet, 219, 49, 10.1007/BF00261156
Joshi, 1996, A global two component signal transduction system that integrates the control of photosynthesis, carbon dioxide assimilation, and nitrogen fixation, Proc Natl Acad Sci USA, 93, 14515, 10.1073/pnas.93.25.14515
Kehoe, 2006, Responding to color: the regulation of complementary chromatic adaptation, Annu Rev Plant Biol, 57, 127, 10.1146/annurev.arplant.57.032905.105215
Kim, 1996, Evidence for the direct interaction of the nifW gene product with the MoFe protein, J Biol Chem, 271, 9764, 10.1074/jbc.271.16.9764
Klatt, 2007, Comparative genomics provides evidence for the 3-hydroxypropionate autotrophic pathway in filamentous anoxygenic phototrophic bacteria and in hot spring microbial mats, Environ Microbiol, 9, 2067, 10.1111/j.1462-2920.2007.01323.x
Kühl, 1992, Microsensor measurements of sulfate reduction and sulfide oxidation in compact microbial communities of aerobic biofilms, Appl Environ Microbiol, 58, 1164, 10.1128/aem.58.4.1164-1174.1992
Lau, 2005, Molecular diversity of cyanobacteria inhabiting coniform structures and surrounding mat in a Yellowstone hot spring, Astrobiology, 5, 83, 10.1089/ast.2005.5.83
Lee, 1998, Genetic analysis on the NifW by utilizing the yeast two-hybrid system revealed that the NifW of Azotobacter vinelandii interacts with the NifZ to form higher-order complexes, Biochem Biophys Res Commun, 244, 498, 10.1006/bbrc.1998.8119
Lindell, 2001, Ecological aspects of ntcA gene expression and its use as an indicator of the nitrogen status of marine Synechococcus spp, Appl Environ Microbiol, 67, 3340, 10.1128/AEM.67.8.3340-3349.2001
Lohr, 2005, Genome-based examination of chlorophyll and carotenoid biosynthesis in Chlamydomonas reinhardtii, Plant Physiol, 138, 490, 10.1104/pp.104.056069
Ludwig, 2006, Occurrence of hydrogenases in cyanobacteria and anoxygenic photosynthetic bacteria: implications for the phylogenetic origin of cyanobacterial and algal hydrogenases, J Mol Evol, 63, 758, 10.1007/s00239-006-0001-6
Luque, 1994, Molecular mechanism for the operation of nitrogen control in cyanobacteria, EMBO J, 13, 2862, 10.1002/j.1460-2075.1994.tb06580.x
Martinez-Argudo, 2004, The NifL-NifA System: a multidomain transcriptional regulatory complex that integrates environmental signals, J Bacteriol, 186, 601, 10.1128/JB.186.3.601-610.2004
Murry, 1989, Evidence that the barrier to the penetration of oxygen into heterocysts depends upon two layers of the cell envelope, Arch Microbiol, 151, 469, 10.1007/BF00454860
Namsaraev, 2003, The structure and biogeochemical activity of the phototrophic communities from the Bol'sherechenskii alkaline hot spring, Mikrobiologiia, 72, 228
Nold, 1996, Photosynthate partitioning and fermentation in hot spring microbial mat communities, Appl Environ Microbiol, 62, 4598, 10.1128/aem.62.12.4598-4607.1996
Nübel, 2002, Microscopic examination of distribution and phenotypic properties of phylogenetically diverse chloroflexaceae-related bacteria in hot spring microbial mats, Appl Environ Microbiol, 68, 4593, 10.1128/AEM.68.9.4593-4603.2002
Omoregie, 2004, Determination of nitrogen-fixing phylotypes in Lyngbya sp. and Microcoleus chthonoplastes cyanobacterial mats from Guerrero Negro, Baja California, Mexico, Appl Environ Microbiol, 70, 2119, 10.1128/AEM.70.4.2119-2128.2004
Paerl, 1996, Seasonal nitrogen fixation dynamics in a marine microbial mat: potential roles of cyanobacteria and microheterotrophs, Limnol Oceanogr, 41, 419, 10.4319/lo.1996.41.3.0419
Pearson, 1979, Aerobic nitrogenase activity associated with a non-heterocystous filamentous cyanobacterium, FEMS Microbiol Lett, 5, 163, 10.1111/j.1574-6968.1979.tb03271.x
Peterson, 1976, Conversion of acetylene reduction rates to nitrogen fixation rates in natural populations of blue-green algae, Anal Biochem, 73, 404, 10.1016/0003-2697(76)90187-1
Pierson, 2001, O phototroph, o chemotroph, where art thou?, Trends Microbiol, 9, 259, 10.1016/S0966-842X(01)02008-X
Pierson, 1984, Physiological ecology of a gliding bacterium containing bacteriochlorophyll a, Appl Environ Microbiol, 47, 576, 10.1128/aem.47.3.576-584.1984
Pierson, 1985, Heliothrix oregonensis, gen. nov., sp. nov., a phototrophic filamentous gliding bacterium containing bacteriochlorophyll a, Arch Microbiol, 142, 164, 10.1007/BF00447061
Pinckney, 1997, Anoxygenic photosynthesis and nitrogen fixation by a microbial mat community in a Bahamian hypersaline lagoon, Appl Environ Microbiol, 63, 420, 10.1128/aem.63.2.420-426.1997
Rabouille, 2006, Modeling the dynamic regulation of nitrogen fixation in the cyanobacterium Trichodesmium sp, Appl Environ Microbiol, 72, 3217, 10.1128/AEM.72.5.3217-3227.2006
Ramsing, 2000, Highly ordered vertical structure of Synechococcus populations within the one-millimeter-thick photic zone of a hot spring cyanobacterial mat, Appl Environ Microbiol, 66, 1038, 10.1128/AEM.66.3.1038-1049.2000
Rangaraj, 2002, Accumulation of 99Mo-containing iron-molybdenum cofactor precursors of nitrogenase on NifNE, NifH, and NifX of Azotobacter vinelandii, J Biol Chem, 277, 40106, 10.1074/jbc.M204581200
Reddy, 1993, Unicellular, aerobic nitrogen-fixing cyanobacteria of the genus Cyanothece, J Bacteriol, 175, 1284, 10.1128/jb.175.5.1284-1292.1993
Revsbech, 1989, An oxygen microelectrode with a guard cathode, Limnol Oceanogr, 34, 474, 10.4319/lo.1989.34.2.0474
Revsbech, 1984, Microelectrode studies of interstitial water chemistry and photosynthetic activity in a hot spring microbial mat, Appl Environ Microbiol, 48, 270, 10.1128/aem.48.2.270-275.1984
Rubio, 2005, Maturation of nitrogenase: a biochemical puzzle, J Bacteriol, 187, 405, 10.1128/JB.187.2.405-414.2005
Scherer, 1988, Interaction of photosynthesis, respiration and nitrogen fixation in cyanobacteria, Photosynth Res, 15, 95, 10.1007/BF00035255
Schneegurt, 1994, Oscillating behavior of carbohydrate granule formation and dinitrogen fixation in the cyanobacterium Cyanothece sp. strain ATCC 51142, J Bacteriol, 176, 1586, 10.1128/jb.176.6.1586-1597.1994
Staal, 2007, On the role of oxygen for nitrogen fixation in the marine cyanobacterium Trichodesmium sp, Environ Microbiol, 9, 727, 10.1111/j.1462-2920.2006.01195.x
Stal, 1984, Nitrogen fixation associated with the cyanobacterial mat of a marine laminated microbial ecosystem, Mar Biol, 82, 217, 10.1007/BF00392402
Stal, 1985, Nitrogenase activity in the non-heterocystous cyanobacterium Oscillatoria sp. grown under alternating light–dark cycles, Archs Microbiol, 143, 67, 10.1007/BF00414770
Steunou, 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, 10.1073/pnas.0507513103
Tamagnini, 2002, Hydrogenases and hydrogen metabolism of cyanobacteria, Microbiol Mol Biol Rev, 66, 1, 10.1128/MMBR.66.1.1-20.2002
Tel-Or, 1977, Photosynthetic components and activities of nitrogen-fixing isolated heterocysts of Anabaena cylindrica, Proc R Soc London Ser B, 198, 61, 10.1098/rspb.1977.0086
Valladares, 2003, Cytochrome c oxidase genes required for nitrogenase activity and diazotrophic growth in Anabaena sp. PCC 7120, Mol Microbiol, 47, 1239, 10.1046/j.1365-2958.2003.03372.x
van der Meer, 2005, Diel variations in carbon metabolism by green nonsulfur-like bacteria in alkaline siliceous hot spring microbial mats from Yellowstone National Park, Appl Environ Microbiol, 71, 3978, 10.1128/AEM.71.7.3978-3986.2005
van der Meer, 2000, Autotrophy of green non-sulphur bacteria in hot spring microbial mats: biological explanations for isotopically heavy organic carbon in the geological record, Environ Microbiol, 2, 428, 10.1046/j.1462-2920.2000.00124.x
Villbrandt, 1990, Interactions between nitrogen fixation and oxygenic photosynthesis in a marine cyanobacterial mat, FEMS Microbiol Ecol, 74, 59, 10.1111/j.1574-6968.1990.tb04052.x
Walsby, 1985, The permeability of heterocysts to the gases nitrogen and oxygen, Proc R Soc Lond B, 226, 345, 10.1098/rspb.1985.0099
Wang, 1985, Complex formation and O2 sensitivity of Azotobacter vinelandii nitrogenase and its component proteins, Biochemistry, 24, 214, 10.1021/bi00322a031
Ward, 2006, Cyanobacterial ecotypes in the microbial mat community of Mushroom Spring (Yellowstone National Park, Wyoming) as species-like units linking microbial community composition, structure and function, Philos Trans R Soc Lond B Biol Sci, 361, 1997, 10.1098/rstb.2006.1919
Ward, 2000, Ecology of Cyanobacteria, 37
Ward, 2008, Genomics, environmental genomics and the issue of microbial species, Heredity, 100, 207, 10.1038/sj.hdy.6801011
Ward, 1998, A natural view of microbial biodiversity within hot spring cyanobacterial mat communities, Microbiol Mol Biol Rev, 62, 1353, 10.1128/MMBR.62.4.1353-1370.1998
Ward, 1997, Biodiversity within hot spring microbial mat communities: molecular monitoring of enrichment cultures, Antonie van Leeuwenhoek, 71, 143, 10.1023/A:1000131426164
Whelan, 2003, A method for the absolute quantification of cDNA using real-time PCR, J Immunol Methods, 278, 261, 10.1016/S0022-1759(03)00223-0
Wolk, 1994, The Molecular Biology of Cyanobacteria, 76