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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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“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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“However, since P450nor usually receives electrons from NADH to detoxify NO, it cannot act as a functional enzyme in the respiratory chain (Nakahara et al., 1993; Shoun et al., 2012).”
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“While some fungi also have dissimilatory nitrate reduc-tases (Shoun et al. 2012) and were found to play a role early in the fermentation of tobacco (Di Giacomo et al. 2007), fungal populations have not been studied as extensively as the bacterial populations and may only be present in low…”
BackgroundNomura, 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
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
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
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
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 40
“duction of nitric oxide (NO) into nitrous oxide (N2O) using NADH as an electron donor (2NO+NADH+H→N2O+NAD+H2O) [91].”
MethodIkeda‐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
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 38
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
“electron transport system (redox partner).(38) This fact suggested that the function of P450nor is”
BackgroundDawar, 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
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
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
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
“NOR has been reported to supply an enzyme bound nitrosating agent made of iron (ferrous)-nitrosyl or copper (cuprous)nitrosyl complexes which could act appropriately as nitrosating agents during denitrification (Shoun et al., 2012).”
BackgroundTemperature 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
“Denitrification by heterotrophic bacteria to N2O and N2 has been well studied, yet fungal archaean denitrification pathways also lead to production of N2O and/or N2 (Shoun et al. 2012; Long et al. 2013).”
BackgroundAl-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
“Results of previous studies support those found here, suggesting the existence of NO-related biosynthesis genes in fungi such as Magnaporthe oryzae (Samalova et al. 2013), Cylindrocarpon tonkinense, and Fusarium solani (Shoun et al. 2012).”
ResultZilli, 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
“In particular, this ability has been demonstrated for fungi of the order Hypocreales (such as genenera Fusarium and Trichoderma) (Maeda et al. 2015; Shoun et al. 2012).”
BackgroundWijeratne, 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
Wang, W., Cao, L., Tan, H., & Zhang, R. (2016) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-016-7800-5 · Cited by 33
“The result was likely attributed to the incomplete denitrifying system of actinomycete strains (Kumon et al. 2002; Shoun et al. 2012).”
BackgroundMcLean, K. J., Leys, D., & Munro, A. W. (2015) · Springer eBooks · doi:10.1007/978-3-319-12108-6_6 · Cited by 36
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 33
Chen, H., Fang-Bo, Y., & Shi, W. (2016) · Fungal Biology · doi:10.1016/j.funbio.2016.07.012 · Cited by 32
“…bacteria are lacking the g netic ability of synthesizing N2O reductase 63 M AN US CR IP T AC CE PT ED and thus mediate a truncated pathway of denitrificat on with N2O as the end product, almost all 64 the denitrifying fungi do not have this enzyme synthesis ability (Zumft 1997; Shoun et al., 2012).”
BackgroundResultInfluentialMaeda, K., Toyoda, S., Hanajima, D., & Yoshida, N. (2013) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2013.01.041 · Cited by 31
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
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
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 30
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
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
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
Metadata
- 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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