Fungal denitrification and nitric oxide reductase cytochrome P450nor
Open accessAbstract
We have shown that many fungi (eukaryotes) exhibit distinct denitrifying activities, although occurrence of denitrification was previously thought to be restricted to bacteria (prokaryotes), and have characterized the fungal denitrification system. It comprises NirK (copper-containing nitrite reductase) and P450nor (a cytochrome P450 nitric oxide (NO) reductase (Nor)) to reduce nitrite to nitrous oxide (N(2)O). The system is localized in mitochondria functioning during anaerobic respiration. Some fungal systems further contain and use dissimilatory and assimilatory nitrate reductases to denitrify nitrate. Phylogenetic analysis of nirK genes showed that the fungal-denitrifying system has the same ancestor as the bacterial counterpart and suggested a possibility of its proto-mitochondrial origin. By contrast, fungi that have acquired a P450 from bacteria by horizontal transfer of the gene, modulated its function to give a Nor activity replacing the original Nor with P450nor. P450nor receives electrons directly from nicotinamide adenine dinucleotide to reduce NO to N(2)O. The mechanism of this unprecedented electron transfer has been extensively studied and thoroughly elucidated. Fungal denitrification is often accompanied by a unique phenomenon, co-denitrification, in which a hybrid N(2) or N(2)O species is formed upon the combination of nitrogen atoms of nitrite with a nitrogen donor (amines and imines). Possible involvement of NirK and P450nor is suggested.
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Multiple fungal species, including the ubiquitous Candida, contain a fungal nitrate reductase enzyme and are known nitrate-reducers in the environment.
“Importantly, multiple fungal species, including the ubiquitous Candida, contain a fungal nitrate reductase enzyme and are known nitrate-reducers in the environment[229,230].”
From Enterosalivary nitrate metabolism and the microbiome: Intersection of microbial metabolism, nitric oxide and diet in cardiac and pulmonary vascular health (2017) · cites this paper as [230]
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Cites
Cell biology and molecular basis of denitrification
Zumft, W. G. (1997) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.61.4.533-616.1997 · Cited by 3,483 · see citing works
Missing lithotroph identified as new planctomycete
Strous, M., Fuerst, J. A., Kramer, E. H. M., Logemann, S., Gerard Muyzer, C., van de Pas-Schoonen, K. T., Webb, R. I., Kuenen, J. G., & Jetten, M. S. M. (1999) · Nature · doi:10.1038/22749 · Cited by 1,578 · see citing works
Berks, B. C., Ferguson, S. J., Moir, J. W. B., & Richardson, D. J. (1995) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/0005-2728(95)00092-5 · Cited by 596 · see citing works
Dissimilatory Nitrite and Nitric Oxide Reductases
Averill, B. A. (1996) · Chemical Reviews · doi:10.1021/cr950056p · Cited by 545 · see citing works
Evidence for Fungal Dominance of Denitrification and Codenitrification in a Grassland Soil
Laughlin, R. J., & Stevens, R. J. (2002) · Soil Science Society of America Journal · doi:10.2136/sssaj2002.1540 · Cited by 425 · see citing works
Shoun, H., Kim, D., Uchiyama, H., & Sugiyama, J. (1992) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.1992.tb05331.x · Cited by 422 · see citing works
Mitochondria as we don't know them
Tielens, A. G. M., Rotte, C., van Hellemond, J. J., & Martin, W. F. (2002) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(02)02193-x · Cited by 375 · see citing works
Shoun, H., & Tanimoto, T. (1991) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)99130-1 · Cited by 257 · see citing works
Nakahara, K., Tanimoto, T., Hatano, K., Usuda, K., & Shoun, H. (1993) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)53102-1 · Cited by 249 · see citing works
Spectroscopic and Kinetic Studies on Reaction of Cytochrome P450nor with Nitric Oxide
Shiro, Y., Fujii, M., Iizuka, T., Adachi, S., Tsukamoto, K., Nakahara, K., & Shoun, H. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.4.1617 · Cited by 206 · see citing works
Crystal structure of nitric oxide reductase from denitrifying fungus Fusarium oxysporum
Park, S., Shimizu, H., Adachi, S., Nakagawa, A., Tanaka, I., Nakahara, K., Shoun, H., OBAYASHI, E., Nakamura, H., lizuka, T., et al. (1997) · Nature Structural Biology · doi:10.1038/nsb1097-827 · Cited by 187 · see citing works
Isotopologue fractionation during N 2 O production by fungal denitrification
Sutka, R. L., Adams, G. C., Ostrom, N. E., & Ostrom, P. H. (2008) · Rapid Communications in Mass Spectrometry · doi:10.1002/rcm.3820 · Cited by 184 · see citing works
Denitrification, a Novel Type of Respiratory Metabolism in Fungal Mitochondrion
Kobayashi, M., Matsuo, Y., Takimoto, A., Suzuki, S., Maruo, F., & Shoun, H. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.27.16263 · Cited by 184 · see citing works
Ferguson, S. J. (1998) · Current Opinion in Chemical Biology · doi:10.1016/s1367-5931(98)80059-8 · Cited by 177 · see citing works
Ammonia Fermentation, a Novel Anoxic Metabolism of Nitrate by Fungi
Zhou, Z., Takaya, N., Nakamura, A., Yamaguchi, M., Takeo, K., & Shoun, H. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m109096200 · Cited by 149 · see citing works
Lehnert, N., Praneeth, V. K. K., & Paulat, F. (2006) · Journal of Computational Chemistry · doi:10.1002/jcc.20400 · Cited by 121 · see citing works
Kizawa, H., Tomura, D., Oda, M., Fukamizu, A., Hoshino, T., Gotoh, O., Yasui, T., & Shoun, H. (1991) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)99270-7 · Cited by 121 · see citing works
Anaerobic denitrification in fungi from the coastal marine sediments off Goa, India
Manohar, C. S., & Raghukumar, C. (2008) · Mycological Research · doi:10.1016/j.mycres.2008.08.009 · Cited by 114 · see citing works
Structural diversity of cytochrome P450 enzyme system
Omura, T. (2010) · The Journal of Biochemistry · doi:10.1093/jb/mvq001 · Cited by 112 · see citing works
Usuda, K., Toritsuka, N., Matsuo, Y., Kim, D. H., & Shoun, H. (1995) · Applied and Environmental Microbiology · doi:10.1128/aem.61.3.883-889.1995 · Cited by 107 · see citing works
Proton Delivery in NO Reduction by Fungal Nitric-oxide Reductase
Shimizu, H., OBAYASHI, E., Gomi, Y., Arakawa, H., Park, S., Nakamura, H., Adachi, S., Shoun, H., & Shiro, Y. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.7.4816 · Cited by 107 · see citing works
Kobayashi, M., & Shoun, H. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.8.4146 · Cited by 94 · see citing works
Co-denitrification by the denitrifying system of the fungusFusarium oxysporum
Tanimoto, T., Hatano, K.-I., Kim, D.-H., Uchiyama, H., & Shoun, H. (1992) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.1992.tb05086.x · Cited by 90 · see citing works
Isotope effects and intermediates in the reduction of NO by P450NOR
Daiber, A., Nauser, T., Takaya, N., Kudo, T., Weber, P. B., Hultschig, C., Shoun, H., & Ullrich, V. (2002) · Journal of Inorganic Biochemistry · doi:10.1016/s0162-0134(01)00386-5 · Cited by 90 · see citing works
Uchimura, H., Enjoji, H., Seki, T., Taguchi, A., Tsakaya, N., & Shoun, H. (2002) · The Journal of Biochemistry · doi:10.1093/oxfordjournals.jbchem.a003137 · Cited by 84 · see citing works
Structural Evidence for Direct Hydride Transfer from NADH to Cytochrome P450nor
Oshima, R., Fushinobu, S., Su, F., Li, Z., Takaya, N., & Shoun, H. (2004) · Journal of Molecular Biology · doi:10.1016/j.jmb.2004.07.009 · Cited by 83 · see citing works
Identification ofHistoplasma capsulatumTranscripts Induced in Response to Reactive Nitrogen Species
Nittler, M. P., Murray, D. H., Foo, C. K., & Sil, A. (2005) · Molecular Biology of the Cell · doi:10.1091/mbc.e05-05-0434 · Cited by 80 · see citing works
Kumon, Y., Sasaki, Y., Kato, I., Takaya, N., Shoun, H., & Beppu, T. (2002) · Journal of Bacteriology · doi:10.1128/jb.184.11.2963-2968.2002 · Cited by 70 · see citing works
Takaya, N., Suzuki, S., Kuwazaki, S., Shoun, H., Maruo, F., Yamaguchi, M., & Takeo, K. (1999) · Archives of Biochemistry and Biophysics · doi:10.1006/abbi.1999.1499 · Cited by 69 · see citing works
Denitrification by yeasts and occurrence of cytochrome P450nor in Trichosporon cutaneum
Tsuruta, S., Takaya, N., Zhang, L., Shoun, H., Kimura, K., Hamamoto, M., & Nakase, T. (1998) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.1998.tb13262.x · Cited by 69 · see citing works
Kim, S.-W., Fushinobu, S., Zhou, S., Wakagi, T., & Shoun, H. (2009) · Applied and Environmental Microbiology · doi:10.1128/aem.02536-08 · Cited by 64 · see citing works
Purification and Properties of a Cyotchrome P-450 of a Fungus, Fusarium oxysporum
Shoun, H., Sudo, Y., Seto, Y., & Beppu, T. (1983) · The Journal of Biochemistry · doi:10.1093/oxfordjournals.jbchem.a134467 · Cited by 63 · see citing works
Kudo, T., Tomura, D., Liu, D. L., Dai, X. Q., & Shoun, H. (1996) · Biochimie · doi:10.1016/s0300-9084(97)82538-2 · Cited by 51 · see citing works
Soluble, nitrate/nitrite‐inducible cytochrome P‐450 of the fungus, Fusarium oxysporum
Shoun, H., Suyama, W., & Yasui, T. (1989) · FEBS Letters · doi:10.1016/0014-5793(89)81151-2 · Cited by 49 · see citing works
Takaya, N., & Shoun, H. (2000) · Molecular and General Genetics MGG · doi:10.1007/s004380051177 · Cited by 49 · see citing works
Hybrid Respiration in the Denitrifying Mitochondria of Fusarium oxysporum
Takaya, N. (2003) · The Journal of Biochemistry · doi:10.1093/jb/mvg060 · Cited by 47 · see citing works
Soil Formate Regulates the Fungal Nitrous Oxide Emission Pathway
K., W., Farrell, R. E., & Siciliano, S. D. (2008) · Applied and Environmental Microbiology · doi:10.1128/aem.00797-08 · Cited by 45 · see citing works
Kudo, T., Takaya, N., Park, S., Shiro, Y., & Shoun, H. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m007244200 · Cited by 43 · see citing works
Nakahara, K., & Shoun, H. (1996) · The Journal of Biochemistry · doi:10.1093/oxfordjournals.jbchem.a021525 · Cited by 38 · see citing works
Denitrification of Nitrate by the FungusCylindrocarpon tonkinense
Watsuji, T., Takaya, N., Nakamura, A., & Shoun, H. (2003) · Bioscience Biotechnology and Biochemistry · doi:10.1271/bbb.67.1115 · Cited by 35 · see citing works
Multi-Energy Metabolic Mechanisms of the FungusFusarium oxysporumin Low Oxygen Environments
Zhou, Z., Takaya, N., & Shoun, H. (2010) · Bioscience Biotechnology and Biochemistry · doi:10.1271/bbb.100482 · Cited by 33 · see citing works
Nitrous Oxide-forming Codenitrification Catalyzed by Cytochrome P450nor
Su, F., Takaya, N., & Shoun, H. (2004) · Bioscience Biotechnology and Biochemistry · doi:10.1271/bbb.68.473 · Cited by 30 · see citing works
The B′ Helix Determines Cytochrome P450nor Specificity for the Electron Donors NADH and NADPH
Li, Z., Kudo, T., Takaya, N., & Shoun, H. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m203923200 · Cited by 30 · see citing works
Sang-Wan, K. I. M., Fushinobu, S., Zhou, S., Wakagi, T., & Shoun, H. (2010) · Bioscience Biotechnology and Biochemistry · doi:10.1271/bbb.100071 · Cited by 21 · see citing works
Umemura, M., Su, F., Takaya, N., Shiro, Y., & Shoun, H. (2004) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.2004.04206.x · Cited by 15 · see citing works
Formate-forming Fungal Catabolic Pathway to Supply Electrons to Nitrate Respiration
Kuwazaki, S., Takaya, N., Nakamura, A., & Shoun, H. (2003) · Bioscience Biotechnology and Biochemistry · doi:10.1271/bbb.67.937 · Cited by 15 · see citing works
Co-denitrification by the denitrifying system of the fungus Fusarium oxysporum
Tanimoto, T. (1992) · FEMS Microbiology Letters · doi:10.1016/0378-1097(92)90525-s · Cited by 12 · see citing works
Watsuji, T., Takaya, N., Nakamura, A., & Shoun, H. (2003) · Bioscience Biotechnology and Biochemistry · doi:10.1271/bbb.67.1109 · Cited by 11 · see citing works
Involvement of a Glu71–Arg64 Couple in the Access Channel for NADH in Cytochrome P450nor
Su, F., Fushinobu, S., Takaya, N., & Shoun, H. (2004) · Bioscience Biotechnology and Biochemistry · doi:10.1271/bbb.68.1156 · Cited by 8 · see citing works
Kubota, Y., Takaya, N., & Shoun, H. (1999) · Archives of Microbiology · doi:10.1007/s002030050701 · Cited by 7 · see citing works
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The microbial nitrogen-cycling network
Kuypers, M. M. M., Marchant, H. K., & Kartal, B. (2018) · Nature Reviews Microbiology · doi:10.1038/nrmicro.2018.9 · Cited by 4,490 · see citing works
Hu, H., Chen, D., & He, J. (2015) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuv021 · Cited by 806 · see citing works
Genomics and Ecology of Novel N2O-Reducing Microorganisms.
Hallin, S., Philippot, L., Löffler, F., Sanford, R., & Jones, C. M. (2018) · Trends in Microbiology · doi:10.1016/j.tim.2017.07.003 · Cited by 546 · see citing works
Fungal traits that drive ecosystem dynamics on land
Treseder, K. K., & Lennon, J. T. (2015) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00001-15 · Cited by 625 · see citing works
Role of organic amendment application on greenhouse gas emission from soil
Thangarajan, R., Bolan, N. S., Tian, G., Naidu, R., & Kunhikrishnan, A. (2013) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2013.01.031 · Cited by 533 · see citing works
Biological sources and sinks of nitrous oxide and strategies to mitigate emissions
THOMSON, A. J., Giannopoulos, G., Pretty, J., Baggs, E. M., & Richardson, D. J. (2012) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2011.0415 · Cited by 512 · see citing works
The role of nitrifier denitrification in the production of nitrous oxide revisited
Wrage, N., Horn, M. A., Well, R., Müller, C., Velthof, G. L., & Oenema, O. (2018) · Soil Biology and Biochemistry · doi:10.1016/j.soilbio.2018.03.020 · Cited by 511 · see citing works
Maia, L. B., & Moura, J. J. G. (2014) · Chemical Reviews · doi:10.1021/cr400518y · Cited by 401 · see citing works
Lehnert, N., Dong, H. T., Harland, J. B., Hunt, A. P., & White, C. J. (2018) · Nature Reviews Chemistry · doi:10.1038/s41570-018-0041-7 · Cited by 279 · see citing works
Structure and function of haemoglobins
Gell, D. A. (2017) · Blood Cells Molecules and Diseases · doi:10.1016/j.bcmd.2017.10.006 · Cited by 277 · see citing works
Estuarine plastisphere as an overlooked source of N2O production
Su, X., Yang, L., Yang, K., Tang, Y., Wen, T., Wang, Y., Rillig, M. C., Rohe, L., Pan, J., Li, H., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-31584-x · Cited by 239 · see citing works
Applications of microbial cytochrome P450 enzymes in biotechnology and synthetic biology
Girvan, H. M., & Munro, A. W. (2016) · Current Opinion in Chemical Biology · doi:10.1016/j.cbpa.2016.02.018 · Cited by 238 · see citing works
N2O production, a widespread trait in fungi
Maeda, K., Spor, A., Edel‐Hermann, V., Heraud, C., Breuil, M., Bizouard, F., Toyoda, S., Yoshida, N., Steinberg, C., & Philippot, L. (2015) · Scientific Reports · doi:10.1038/srep09697 · Cited by 232 · see citing works
Medinets, S., Skiba, U., Rennenberg, H., & Butterbach‐Bahl, K. (2014) · Soil Biology and Biochemistry · doi:10.1016/j.soilbio.2014.09.025 · Cited by 219 · see citing works
Munro, A. W., Girvan, H. M., Mason, A. E., Dunford, A. J., & McLean, K. J. (2013) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2012.11.006 · Cited by 191 · see citing works
Koch, C. D., Gladwin, M. T., Freeman, B. A., Lundberg, J. O., Weitzberg, E., & Morris, A. (2017) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2016.12.015 · Cited by 186 · see citing works
Nitrate Storage and Dissimilatory Nitrate Reduction by Eukaryotic Microbes
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Evidence for fungal and chemodenitrification based N2O flux from nitrogen impacted coastal sediments
Wankel, S. D., Ziebis, W., Buchwald, C., Charoenpong, C., de Beer, D., Dentinger, J. E., Xu, Z. Z., & Zengler, K. (2017) · Nature Communications · doi:10.1038/ncomms15595 · Cited by 165 · see citing works
Fungal Cytochrome P450s and the P450 Complement (CYPome) of Fusarium graminearum
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Functions of elements in soil microorganisms
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Mothapo, N. V., Chen, H., Cubeta, M. A., Grossman, J., Fuller, F., & Shi, W. (2015) · Soil Biology and Biochemistry · doi:10.1016/j.soilbio.2015.02.001 · Cited by 153 · see citing works
Wu, D., Şenbayram, M., Well, R., Brüggemann, N., Pfeiffer, B., Loick, N., Stempfhuber, B., Dittert, K., & Bol, R. A. (2016) · Soil Biology and Biochemistry · doi:10.1016/j.soilbio.2016.10.022 · Cited by 144 · see citing works
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Fungal denitrification revisited – Recent advancements and future opportunities
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Tosha, T., Nomura, T., Nishida, T., Saeki, N., Okubayashi, K., Yamagiwa, R., Sugahara, M., Nakane, T., Yamashita, K., Hirata, K., et al. (2017) · Nature Communications · doi:10.1038/s41467-017-01702-1 · Cited by 108 · see citing works
Wei, W., Isobe, K., Shiratori, Y., Nishizawa, T., Ohte, N., Otsuka, S., & Senoo, K. (2013) · Soil Biology and Biochemistry · doi:10.1016/j.soilbio.2013.10.044 · Cited by 108 · see citing works
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Wu, D., Cardenas, L. M., Calvet, S., Brüggemann, N., Loick, N., Liu, S., & Bol, R. A. (2017) · Soil Biology and Biochemistry · doi:10.1016/j.soilbio.2017.06.007 · Cited by 100 · see citing works
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Rohe, L., Anderson, T., Braker, G., Flessa, H., Giesemann, A., Lewicka‐Szczebak, D., Wrage, N., & Well, R. (2014) · Rapid Communications in Mass Spectrometry · doi:10.1002/rcm.6975 · Cited by 94 · see citing works
Semedo, M., Song, B., Sparrer, T., & Phillips, R. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.02121 · Cited by 87 · see citing works
Su, X., Wen, T., Wang, Y., Xu, J., Li, C., Zhang, J., Xue, X., Ding, K., Tang, Y., & Zhu, Y. (2021) · Global Change Biology · doi:10.1111/gcb.15863 · Cited by 86 · see citing works
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Yoon, S., Song, B., Phillips, R., Chang, J., & Song, M. J. (2019) · FEMS Microbiology Ecology · doi:10.1093/femsec/fiz066 · Cited by 79 · see citing works
Marusenko, Y., Huber, D. P., & Hall, S. J. (2013) · Soil Biology and Biochemistry · doi:10.1016/j.soilbio.2013.03.018 · Cited by 78 · see citing works
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Soil aggregate size modifies the impacts of fertilization on microbial communities
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Lourenço, K. S., Costa, O. Y. A., Cantarella, H., & Kuramae, E. E. (2022) · Soil Biology and Biochemistry · doi:10.1016/j.soilbio.2022.108563 · Cited by 63 · see citing works
Detection and Diversity of Fungal Nitric Oxide Reductase Genes ( p450nor ) in Agricultural Soils
Higgins, S., Welsh, A. K., Orellana, L. H., Konstantinidis, K. T., Chee‐Sanford, J. C., Sanford, R. A., Schadt, C. W., & Löffler, F. E. (2016) · Applied and Environmental Microbiology · doi:10.1128/aem.00243-16 · Cited by 62 · see citing works
Li, X., Gao, D., Li, Y., Zheng, Y., Dong, H., Liang, X., Liu, M., & Hou, L. (2023) · Environmental Science & Technology · doi:10.1021/acs.est.2c06602 · Cited by 61 · see citing works
Reed, C. J., Lam, Q., Mirts, E. N., & Lu, Y. (2021) · Chemical Society Reviews · doi:10.1039/d0cs01297a · Cited by 61 · see citing works
Mosier, A. C., Miller, C. S., Frischkorn, K. R., Ohm, R. A., Li, Z., LaButti, K. M., Lapidus, A. L., Lipzen, A., Chen, C., Johnson, J., et al. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.00238 · Cited by 60 · see citing works
Chlamydomonas reinhardtii, an Algal Model in the Nitrogen Cycle
Bellido-Pedraza, C. M., Calatrava, V., Sanz‐Luque, E., Tejada‐Jiménez, M., Llamas, Á., Plouviez, M., Guieysse, B., Fernández, E. M., & Galván, A. (2020) · Plants · doi:10.3390/plants9070903 · Cited by 59 · see citing works
Taylor, D. L., & Sinsabaugh, R. L. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-415955-6.00004-9 · Cited by 58 · see citing works
Indications for enzymatic denitrification to N2O at low pH in an ammonia-oxidizing archaeon
Jung, M., Gwak, J.-H., Rohe, L., Giesemann, A., Kim, J., Well, R., Madsen, E. L., Herbold, C. W., Wagner, M., & Rhee, S. (2019) · The ISME Journal · doi:10.1038/s41396-019-0460-6 · Cited by 58 · see citing works
Lourenço, K. S., Dimitrov, M. R., Pijl, A. S., Soares, J. R., do Carmo, J. B., van Veen, J. A., Cantarella, H., & Kuramae, E. E. (2018) · GCB Bioenergy · doi:10.1111/gcbb.12519 · Cited by 57 · see citing works
Zheng, N., Yu, Y., Wang, J., Chapman, S. J., Yao, H., & Zhang, Y. (2020) · Environmental Pollution · doi:10.1016/j.envpol.2020.115106 · Cited by 53 · see citing works
Yamamoto, A., Akiyama, H., Naokawa, T., Miyazaki, Y., Honda, Y., Sano, Y., Nakajima, Y., & Yagi, K. (2013) · Biology and Fertility of Soils · doi:10.1007/s00374-013-0830-6 · Cited by 53 · see citing works
Rational and semi-rational engineering of cytochrome P450s for biotechnological applications
Xu, L., & Du, Y. (2018) · Synthetic and Systems Biotechnology · doi:10.1016/j.synbio.2018.10.001 · Cited by 53 · see citing works
Effects of organic matter and low oxygen on the mycobenthos in a coastal lagoon
Ortega-Arbulú, A.-S., Pichler, M., Vuillemin, A., & Orsi, W. D. (2018) · Environmental Microbiology · doi:10.1111/1462-2920.14469 · Cited by 52 · see citing works
An electrogenic nitric oxide reductase
Al-Attar, S., & de Vries, S. (2015) · FEBS Letters · doi:10.1016/j.febslet.2015.06.033 · Cited by 51 · see citing works
Long, A., Song, B., Fridey, K., & Silva, A. (2014) · FEMS Microbiology Ecology · doi:10.1093/femsec/fiu004 · Cited by 49 · see citing works
Higgins, S., Schadt, C., Matheny, P. B., & Löffler, F. (2018) · Genome Biology and Evolution · doi:10.1093/gbe/evy187 · Cited by 45 · see citing works
Zhang, Y., Wang, W., & Yao, H. (2022) · Archives of Agronomy and Soil Science · doi:10.1080/03650340.2022.2025588 · Cited by 51 · see citing works
Agrawal, Y., Khatri, I., Subramanian, S., & Shenoy, B. D. (2015) · Genome Biology and Evolution · doi:10.1093/gbe/evv037 · Cited by 45 · see citing works
The biosynthesis of nitrous oxide in the green alga Chlamydomonas reinhardtii
Plouviez, M., Wheeler, D., Shilton, A. N., Packer, M. A., McLenachan, P. A., Sanz‐Luque, E., Ocaña‐Calahorro, F. J., Fernández, E. M., & Guieysse, B. (2017) · The Plant Journal · doi:10.1111/tpj.13544 · Cited by 46 · see citing works
Hong, P., Shu, Y., Wu, X., Wang, C., Tian, C., Wu, H., Donde, O. O., & Xiao, B. (2019) · Bioresource Technology · doi:10.1016/j.biortech.2019.122083 · Cited by 45 · see citing works
Maeda, K., Miyatake, F., Asano, R., Nakajima, K., Maeda, T., & Iwabuchi, K. (2018) · Chemosphere · doi:10.1016/j.chemosphere.2018.04.169 · Cited by 43 · see citing works
Xu, H., Sheng, R., Xing, X., Zhang, W., Hou, H., Liu, Y., Qin, H., Chen, C., & Wei, W. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.00117 · Cited by 43 · see citing works
Denitrification Aligns with N2 Fixation in Red Sea Corals
Tilstra, A., El-Khaled, Y. C., Roth, F., Rädecker, N., Pogoreutz, C., Voolstra, C. R., & Wild, C. (2019) · Scientific Reports · doi:10.1038/s41598-019-55408-z · Cited by 43 · see citing works
Han, H., Song, B., Song, M. J., & Yoon, S. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.01203 · Cited by 42 · see citing works
Li, L., Yang, M., Li, J., Bol, R. A., Du, Z., & Wu, D. (2022) · Journal of Cleaner Production · doi:10.1016/j.jclepro.2022.130451 · Cited by 42 · see citing works
Stanfill, S. B., Hecht, S. S., Joerger, A. C., González, P. J., Maia, L. B., Rivas, M. G., Moura, J. J. G., Gupta, A., Brun, N. E. L., Crack, J. C., et al. (2023) · Critical Reviews in Toxicology · doi:10.1080/10408444.2023.2264327 · Cited by 44 · see citing works
Nomura, T., Kimura, T., Kanematsu, Y., Yamada, D., Yamashita, K., Hirata, K., Ueno, G., Murakami, H., Hisano, T., Yamagiwa, R., et al. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2101481118 · Cited by 41 · see citing works
Keuschnig, C., Gorfer, M., Li, G., Mania, D., Frostegård, Å., Bakken, L. R., & Larose, C. (2020) · Environmental Microbiology · doi:10.1111/1462-2920.14980 · Cited by 40 · see citing works
A microbial eukaryote with a unique combination of purple bacteria and green algae as endosymbionts
Muñoz-Gómez, S. A., Kreutz, M., & Hess, S. (2021) · Science Advances · doi:10.1126/sciadv.abg4102 · Cited by 40 · see citing works
Şenbayram, M., Well, R., Shan, J., Bol, R. A., Burkart, S., Jones, D. L., & Wu, D. (2020) · Plant and Soil · doi:10.1007/s11104-020-04457-9 · Cited by 39 · see citing works
Time-resolved studies of metalloproteins using X-ray free electron laser radiation at SACLA
Suga, M., Shimada, A., Akita, F., Shen, J., Tosha, T., & Sugimoto, H. (2019) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2019.129466 · Cited by 38 · see citing works
Ikeda‐Ohtsubo, W., Miyahara, M., Kim, S.-W., Yamada, T., Matsuoka, M., Watanabe, A., Fushinobu, S., Wakagi, T., Shoun, H., Miyauchi, K., et al. (2012) · Journal of Bioscience and Bioengineering · doi:10.1016/j.jbiosc.2012.08.015 · Cited by 38 · see citing works
Li, J., Zhang, Q., Li, Y., Liu, J., Pan, H., Guan, X., Xu, X., Xu, J. M., & Di, H. (2016) · Journal of Soils and Sediments · doi:10.1007/s11368-016-1620-1 · Cited by 37 · see citing works
Matsuoka, M., Kumar, A., Muddassar, M., Matsuyama, A., Yoshida, M., & Zhang, K. Y. J. (2017) · Journal of Chemical Information and Modeling · doi:10.1021/acs.jcim.6b00649 · Cited by 37 · see citing works
Dawar, K. M., Khan, A., Kamil-Sardar, M., Fahad, S., Saud, S., Datta, R., & Danish, S. (2020) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2020.143739 · Cited by 37 · see citing works
RetractedBelowground Defence Strategies in Plants
Steinberg, C., Lecomte, C., Alabouvette, C., & Edel‐Hermann, V. (2016) · Signaling and communication in plants · doi:10.1007/978-3-319-42319-7 · Cited by 36 · see citing works
Glycerine as a carbon source in nitrite removal and sludge production
Bernat, K., Kulikowska, D., & Żuchniewski, K. (2015) · Chemical Engineering Journal · doi:10.1016/j.cej.2014.12.096 · Cited by 35 · see citing works
Biotic nitrosation of diclofenac in a soil aquifer system (Katari watershed, Bolivia)
Chirón, S., & Duwig, C. (2016) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2016.05.048 · Cited by 35 · see citing works
Temperature effects on N 2 O and N 2 denitrification end‐products for a New Zealand pasture soil
Phillips, R., McMillan, A. M. S., Palmada, T., Dando, J., & Giltrap, D. L. (2014) · New Zealand Journal of Agricultural Research · doi:10.1080/00288233.2014.969380 · Cited by 36 · see citing works
Al-Hosni, K., Shahzad, R., Khan, A. L., Imran, Q. M., Al‐Harrasi, A., Rawahi, A. A., Asaf, S., Kang, S., Yun, B., & Lee, I. (2018) · Journal of Plant Interactions · doi:10.1080/17429145.2018.1432773 · Cited by 34 · see citing works
Zilli, J. É., Alves, B. J. R., Rouws, L. F. M., Simões‐Araújo, J. L., Soares, L. H. D. B., Cassán, F., Castellanos, M. O., & O’Hara, G. W. (2019) · Plant and Soil · doi:10.1007/s11104-019-04187-7 · Cited by 33 · see citing works
Wijeratne, G. B., Bhadra, M., Siegler, M. A., & Karlin, K. D. (2019) · Journal of the American Chemical Society · doi:10.1021/jacs.9b07286 · Cited by 33 · see citing works
Wang, W., Cao, L., Tan, H., & Zhang, R. (2016) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-016-7800-5 · Cited by 33 · see citing works
McLean, K. J., Leys, D., & Munro, A. W. (2015) · Springer eBooks · doi:10.1007/978-3-319-12108-6_6 · Cited by 35 · see citing works
Fungi in soil: a rich community with diverse functions
Taylor, D. L., & Bhatnagar, J. M. (2024) · Elsevier eBooks · doi:10.1016/b978-0-12-822941-5.00004-1 · Cited by 32 · see citing works
Chen, H., Fang-Bo, Y., & Shi, W. (2016) · Fungal Biology · doi:10.1016/j.funbio.2016.07.012 · Cited by 32 · see citing works
Maeda, K., Toyoda, S., Hanajima, D., & Yoshida, N. (2013) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2013.01.041 · Cited by 31 · see citing works
Nutrient Enrichment Alters Salt Marsh Fungal Communities and Promotes Putative Fungal Denitrifiers
Kearns, P. J., Bulseco, A., Hoyt, H., Angell, J. H., & Bowen, J. L. (2018) · Microbial Ecology · doi:10.1007/s00248-018-1223-z · Cited by 31 · see citing works
Microbial potential for denitrification in the hyperarid Atacama Desert soils
Wu, D., Şenbayram, M., Moradi, G., Mörchen, R., Knief, C., Klumpp, E., Jones, D. L., Well, R., Chen, R., & Bol, R. A. (2021) · Soil Biology and Biochemistry · doi:10.1016/j.soilbio.2021.108248 · Cited by 31 · see citing works
Su, X., Li, C., Tang, Y., Wen, T., Yang, K., Wang, Y., Zhang, J., Zhu, G., Yang, X., Hou, L., et al. (2022) · Environmental Science & Technology · doi:10.1021/acs.est.2c03550 · Cited by 31 · see citing works
Bösch, Y., Jones, C. M., Finlay, R. D., Karlsson, M., Larsbo, M., Keller, T., & Hallin, S. (2022) · Soil Biology and Biochemistry · doi:10.1016/j.soilbio.2022.108718 · Cited by 29 · see citing works
Chemical formation of hybrid di-nitrogen calls fungal codenitrification into question
Phillips, R., Song, B., McMillan, A. M. S., Grelet, G., Weir, B. S., Palmada, T., & Tobias, C. (2016) · Scientific Reports · doi:10.1038/srep39077 · Cited by 30 · see citing works
Rohe, L., Anderson, T., Flessa, H., Goeske, A., Lewicka‐Szczebak, D., Wrage, N., & Well, R. (2021) · Biogeosciences · doi:10.5194/bg-18-4629-2021 · Cited by 30 · see citing works
- Authors
- Shoun, H., Fushinobu, S., Jiang, L., Kim, S.-W., & Wakagi, T.
- Affiliations
- The University of Tokyo (JP)
- Department of Biotechnology, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Yayoi, Bunkyo-ku, Tokyo 113-8657, Japan
- Venue
- Philosophical Transactions of the Royal Society B Biological Sciences
- Publisher
- The Royal Society
- Published
- 2012-05-05
- Volume
- 367
- Issue
- 1593
- Pages
- 1186-1194
- ISSN
- 0962-8436 (ISSN-L)
- 1471-2970
- PMC
- PMC3306627
- OpenAlex
- W2127344845
- Cited by
- 256
- References
- 50
- Citations by year
- 2026: 17 · 2025: 14 · 2024: 22 · 2023: 20 · 2022: 20 · 2021: 24 · 2020: 17 · 2019: 23 · 2018: 19 · 2017: 14 · 2016: 26 · 2015: 15 · 2014: 10 · 2013: 13 · 2012: 2
- FWCI
- 1.14
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Philosophical Transactions of the Royal Society B Biological Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- University of Tokyo
- University of Tsukuba
- Chiba University
- Universität Konstanz
- Japan Society for the Promotion of Science (20248009)
- Topics
- Physical Sciences › Environmental Science › Pollution › Wastewater Treatment and Nitrogen Removal
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial metabolism and enzyme function
- Keywords
- fungal denitrification, nitric oxide reductase, nirK, nitrite reductase, nitrous oxide, anaerobic respiration, mitochondrial electron transport chain, horizontal gene transfer, phylogenetic analysis, nitrate reductase
- MeSH terms
- Cytochrome P-450 Enzyme System, Fungi, Models, Molecular, Nitric Oxide, Nitrite Reductases, Nitrous Oxide, Denitrification
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