Phylogenomics reveals the dynamic evolution of fungal nitric oxide reductases and their relationship to secondary metabolism
Abstract
Fungi expressing P450nor, an unconventional nitric oxide (NO) reducing cytochrome P450, are considered significant contributors to environmental nitrous oxide (N2O) emissions. Despite extensive efforts, fungal contributions to N2O emissions remain uncertain. For example, the majority of N2O emitted from antibiotic-amended soil microcosms is attributed to fungal activity, yet axenic fungal cultures do not couple N-oxyanion respiration to growth and these fungi produce only minor quantities of N2O. To assist in reconciling these conflicting observations and produce a benchmark genomic analysis of fungal denitrifiers, genes underlying denitrification were examined in > 700 fungal genomes. Of 167 p450nor–containing genomes identified, 0, 30, and 48 also harbored the denitrification genes narG, napA or nirK, respectively. Compared to napA and nirK, p450nor was twice as abundant and exhibited two to five-fold more gene duplications, losses, and transfers, indicating a disconnect between p450nor presence and denitrification potential. Furthermore, co-occurrence of p450nor with genes encoding NO-detoxifying flavohemoglobins (Spearman r = 0.87, p = 1.6e–10) confounds hypotheses regarding P450nor’s primary role in NO detoxification. Instead, ancestral state reconstruction united P450nor with actinobacterial cytochrome P450s (CYP105) involved in secondary metabolism (SM) and 19 (11%) p450nor-containing genomic regions were predicted to be SM clusters. Another 40 (24%) genomes harboredmore »
- Authors:
-
[1];
[1]
- Univ. of Tennessee, Knoxville, TN (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
- Univ. of Tennessee, Knoxville, TN (United States)
- Publication Date:
- Research Org.:
- Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1468244
- Grant/Contract Number:
- AC05-00OR22725
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Genome Biology and Evolution
- Additional Journal Information:
- Journal Volume: 8; Journal ID: ISSN 1759-6653
- Publisher:
- Society for Molecular Biology and Evolution
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; P450nor; fungi; nitrous oxide; secondary metabolism; nitrogen cycle; horizontal gene transfer
Citation Formats
Higgins, Steven A., Schadt, Christopher Warren, Matheny, Patrick B., and Löffler, Frank E. Phylogenomics reveals the dynamic evolution of fungal nitric oxide reductases and their relationship to secondary metabolism. United States: N. p., 2018.
Web. doi:10.1093/gbe/evy187.
Higgins, Steven A., Schadt, Christopher Warren, Matheny, Patrick B., & Löffler, Frank E. Phylogenomics reveals the dynamic evolution of fungal nitric oxide reductases and their relationship to secondary metabolism. United States. https://doi.org/10.1093/gbe/evy187
Higgins, Steven A., Schadt, Christopher Warren, Matheny, Patrick B., and Löffler, Frank E. Wed .
"Phylogenomics reveals the dynamic evolution of fungal nitric oxide reductases and their relationship to secondary metabolism". United States. https://doi.org/10.1093/gbe/evy187. https://www.osti.gov/servlets/purl/1468244.
@article{osti_1468244,
title = {Phylogenomics reveals the dynamic evolution of fungal nitric oxide reductases and their relationship to secondary metabolism},
author = {Higgins, Steven A. and Schadt, Christopher Warren and Matheny, Patrick B. and Löffler, Frank E.},
abstractNote = {Fungi expressing P450nor, an unconventional nitric oxide (NO) reducing cytochrome P450, are considered significant contributors to environmental nitrous oxide (N2O) emissions. Despite extensive efforts, fungal contributions to N2O emissions remain uncertain. For example, the majority of N2O emitted from antibiotic-amended soil microcosms is attributed to fungal activity, yet axenic fungal cultures do not couple N-oxyanion respiration to growth and these fungi produce only minor quantities of N2O. To assist in reconciling these conflicting observations and produce a benchmark genomic analysis of fungal denitrifiers, genes underlying denitrification were examined in > 700 fungal genomes. Of 167 p450nor–containing genomes identified, 0, 30, and 48 also harbored the denitrification genes narG, napA or nirK, respectively. Compared to napA and nirK, p450nor was twice as abundant and exhibited two to five-fold more gene duplications, losses, and transfers, indicating a disconnect between p450nor presence and denitrification potential. Furthermore, co-occurrence of p450nor with genes encoding NO-detoxifying flavohemoglobins (Spearman r = 0.87, p = 1.6e–10) confounds hypotheses regarding P450nor’s primary role in NO detoxification. Instead, ancestral state reconstruction united P450nor with actinobacterial cytochrome P450s (CYP105) involved in secondary metabolism (SM) and 19 (11%) p450nor-containing genomic regions were predicted to be SM clusters. Another 40 (24%) genomes harbored genes nearby p450nor predicted to encode hallmark SM functions, providing additional contextual evidence linking p450nor to SM. Furthermore these findings underscore the potential physiological implications of widespread p450nor gene transfer, support the undiscovered affiliation of p450nor with fungal SM, and challenge the hypothesis of p450nor’s primary role in denitrification.},
doi = {10.1093/gbe/evy187},
journal = {Genome Biology and Evolution},
number = ,
volume = 8,
place = {United States},
year = {Wed Aug 29 00:00:00 EDT 2018},
month = {Wed Aug 29 00:00:00 EDT 2018}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 30 works
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Dual isotope and isotopomer signatures of nitrous oxide from fungal denitrification - a pure culture study: Isotopomer signatures of N
journal, August 2014
- Rohe, Lena; Anderson, Traute-Heidi; Braker, Gesche
- Rapid Communications in Mass Spectrometry, Vol. 28, Issue 17
Dynamic Evolution of Nitric Oxide Detoxifying Flavohemoglobins, a Family of Single-Protein Metabolic Modules in Bacteria and Eukaryotes
journal, April 2016
- Wisecaver, Jennifer H.; Alexander, William G.; King, Sean B.
- Molecular Biology and Evolution, Vol. 33, Issue 8
SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny
journal, January 1996
- Galtier, N.; Gouy, M.; Gautier, C.
- Bioinformatics, Vol. 12, Issue 6
genBlastG: using BLAST searches to build homologous gene models
journal, June 2011
- She, Rong; Chu, Jeffrey Shih-Chieh; Uyar, Bora
- Bioinformatics, Vol. 27, Issue 15
Nitrate Reductase and Nitrous Oxide Production by Fusarium oxysporum 11dn1 Under Aerobic and Anaerobic Conditions
journal, August 2000
- Kurakov, Alexander V.; Nosikov, Alexander N.; Skrynnikova, Evdokiya V.
- Current Microbiology, Vol. 41, Issue 2
Shifting the genomic gold standard for the prokaryotic species definition
journal, October 2009
- Richter, Michael; Rosselló-Móra, Ramon
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 45
Denitrification and aerobic respiration, hybrid electron transport chains and co-evolution
journal, February 2013
- Chen, Jianwei; Strous, Marc
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1827, Issue 2
Translating biosynthetic gene clusters into fungal armor and weaponry
journal, August 2015
- Keller, Nancy P.
- Nature Chemical Biology, Vol. 11, Issue 9
Nitrous Oxide Production by Organisms Other than Nitrifiers or Denitrifiers †
journal, January 1982
- Bleakley, Bruce H.; Tiedje, James M.
- Applied and Environmental Microbiology, Vol. 44, Issue 6
Coumarin formation in novobiocin biosynthesis: β-hydroxylation of the aminoacyl enzyme tyrosyl-S-NovH by a cytochrome P450 NovI
journal, April 2001
- Chen, Huawei; Walsh, Christopher T.
- Chemistry & Biology, Vol. 8, Issue 4
Microbial regulation of terrestrial nitrous oxide formation: understanding the biological pathways for prediction of emission rates
journal, April 2015
- Hu, Hang-Wei; Chen, Deli; He, Ji-Zheng
- FEMS Microbiology Reviews, Vol. 39, Issue 5
CONSEL: for assessing the confidence of phylogenetic tree selection
journal, December 2001
- Shimodaira, H.; Hasegawa, M.
- Bioinformatics, Vol. 17, Issue 12
RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models
journal, August 2006
- Stamatakis, Alexandros
- Bioinformatics, Vol. 22, Issue 21
Unusual Cytochrome P450 Enzymes and Reactions
journal, April 2013
- Guengerich, F. Peter; Munro, Andrew W.
- Journal of Biological Chemistry, Vol. 288, Issue 24
The Evolution and Future of Earth’s Nitrogen Cycle
journal, October 2010
- Canfield, Donald E.; Glazer, Alexander N.; Falkowski, Paul G.
- Science, Vol. 330, Issue 6001
Nitrous oxide emissions from soils: how well do we understand the processes and their controls?
journal, July 2013
- Butterbach-Bahl, Klaus; Baggs, Elizabeth M.; Dannenmann, Michael
- Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 368, Issue 1621
Fusarium wilt (Fusarium oxysporum f. sp. vasinfectum) genes expressed during infection of cotton (Gossypium hirsutum)+
journal, March 2006
- Mcfadden, Helen G.; Wilson, Iain W.; Chapple, Robin M.
- Molecular Plant Pathology, Vol. 7, Issue 2
Predicting active site residue annotations in the Pfam database
journal, August 2007
- Mistry, Jaina; Bateman, Alex; Finn, Robert D.
- BMC Bioinformatics, Vol. 8, Issue 1
Cytochrome P450–catalyzed L-tryptophan nitration in thaxtomin phytotoxin biosynthesis
journal, September 2012
- Barry, Sarah M.; Kers, Johan A.; Johnson, Evan G.
- Nature Chemical Biology, Vol. 8, Issue 10
A review of stable isotope techniques for N2O source partitioning in soils: recent progress, remaining challenges and future considerations
journal, January 2008
- Baggs, E. M.
- Rapid Communications in Mass Spectrometry, Vol. 22, Issue 11
CYP105-diverse structures, functions and roles in an intriguing family of enzymes in Streptomyces
journal, November 2014
- Moody, Suzy C.; Loveridge, E. Joel
- Journal of Applied Microbiology, Vol. 117, Issue 6
FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments
journal, March 2010
- Price, Morgan N.; Dehal, Paramvir S.; Arkin, Adam P.
- PLoS ONE, Vol. 5, Issue 3
Chrysamides A–C, Three Dimeric Nitrophenyl trans -Epoxyamides Produced by the Deep-Sea-Derived Fungus Penicillium chrysogenum SCSIO41001
journal, July 2016
- Chen, Shengtian; Wang, Junfeng; Lin, Xiuping
- Organic Letters, Vol. 18, Issue 15
CASSIS and SMIPS: promoter-based prediction of secondary metabolite gene clusters in eukaryotic genomes
journal, December 2015
- Wolf, Thomas; Shelest, Vladimir; Nath, Neetika
- Bioinformatics, Vol. 32, Issue 8
Inferring duplications, losses, transfers and incomplete lineage sorting with nonbinary species trees.
text, January 2012
- Stolzer, Maureen; Lai, Han; Xu, Minli
- Carnegie Mellon University
Evaluation of antibacterial and antifungal compounds for selective inhibition of denitrification in soils
journal, January 2016
- Ladan, Shiva; Jacinthe, Pierre-André
- Environmental Science: Processes & Impacts, Vol. 18, Issue 12
Improved Culturability of Soil Bacteria and Isolation in Pure Culture of Novel Members of the Divisions Acidobacteria, Actinobacteria, Proteobacteria, and Verrucomicrobia
journal, May 2002
- Janssen, P. H.; Yates, P. S.; Grinton, B. E.
- Applied and Environmental Microbiology, Vol. 68, Issue 5
Nitric oxide generated by the rice blast fungus Magnaporthe oryzae drives plant infection
journal, October 2012
- Samalova, Marketa; Johnson, Jasper; Illes, Mary
- New Phytologist, Vol. 197, Issue 1
Denitrifying genes in bacterial and Archaeal genomes
journal, September 2002
- Philippot, Laurent
- Biochimica et Biophysica Acta (BBA) - Gene Structure and Expression, Vol. 1577, Issue 3
The biosynthesis of nitrous oxide in the green alga Chlamydomonas reinhardtii
journal, May 2017
- Plouviez, Maxence; Wheeler, David; Shilton, Andy
- The Plant Journal, Vol. 91, Issue 1
Dissimilatory nitrate reduction by Aspergillus terreus isolated from the seasonal oxygen minimum zone in the Arabian Sea
journal, January 2014
- Stief, Peter; Fuchs-Ocklenburg, Silvia; Kamp, Anja
- BMC Microbiology, Vol. 14, Issue 1
Fungal denitrification and nitric oxide reductase cytochrome P450nor
journal, May 2012
- Shoun, Hirofumi; Fushinobu, Shinya; Jiang, Li
- Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 367, Issue 1593
Comprehensive annotation of secondary metabolite biosynthetic genes and gene clusters of Aspergillus nidulans, A. fumigatus, A. niger and A. oryzae
journal, January 2013
- Inglis, Diane O.; Binkley, Jonathan; Skrzypek, Marek S.
- BMC Microbiology, Vol. 13, Issue 1
The Pfam protein families database
journal, November 2009
- Finn, Robert D.; Mistry, Jaina; Tate, John
- Nucleic Acids Research, Vol. 38, Issue suppl_1
Uncovering the Genome-Wide Transcriptional Responses of the Filamentous Fungus Aspergillus niger to Lignocellulose Using RNA Sequencing
journal, August 2012
- Delmas, Stéphane; Pullan, Steven T.; Gaddipati, Sanyasi
- PLoS Genetics, Vol. 8, Issue 8
The significant contribution of fungi to soil N2O production across diverse ecosystems
journal, January 2014
- Chen, Huaihai; Mothapo, Nape V.; Shi, Wei
- Applied Soil Ecology, Vol. 73
Nitric-oxide Dioxygenase Activity and Function of Flavohemoglobins: SENSITIVITY TO NITRIC OXIDE AND CARBON MONOXIDE INHIBITION
journal, August 2000
- Gardner, Paul R.; Gardner, Anne M.; Martin, Lori A.
- Journal of Biological Chemistry, Vol. 275, Issue 41
Nitrous oxide producing activity of diverse fungi from distinct agroecosystems
journal, November 2013
- Mothapo, Nape V.; Chen, Huaihai; Cubeta, Marc A.
- Soil Biology and Biochemistry, Vol. 66
Criteria and methodology for identifying respiratory denitrifiers.
journal, January 1995
- Mahne, I.; Tiedje, J. M.
- Applied and environmental microbiology, Vol. 61, Issue 3
Phenotypic and genotypic heterogeneity among closely related soil-borne N2- and N2O-producing Bacillus isolates harboring the nosZ gene: Genotype and phenotype of N2/N2O-producing soil Bacillus spp.
journal, March 2011
- Jones, Christopher M.; Welsh, Allana; Throbäck, Ingela N.
- FEMS Microbiology Ecology, Vol. 76, Issue 3
NCBI Reference Sequence (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins
journal, December 2004
- Pruitt, K. D.
- Nucleic Acids Research, Vol. 33, Issue Database issue
Transformation of the Nitrogen Cycle: Recent Trends, Questions, and Potential Solutions
journal, May 2008
- Galloway, J. N.; Townsend, A. R.; Erisman, J. W.
- Science, Vol. 320, Issue 5878
Transformation of the Nitrogen Cycle: Recent Trends, Questions, and Potential Solutions
journal, May 2008
- Galloway, J. N.; Townsend, A. R.; Erisman, J. W.
- Science, Vol. 320, Issue 5878
Nitric oxide reductases of prokaryotes with emphasis on the respiratory, heme?copper oxidase type
journal, January 2005
- Zumft, W.
- Journal of Inorganic Biochemistry, Vol. 99, Issue 1
Isotopic Fractionation by a Fungal P450 Nitric Oxide Reductase during the Production of N 2 O
journal, August 2014
- Yang, Hui; Gandhi, Hasand; Ostrom, Nathaniel E.
- Environmental Science & Technology, Vol. 48, Issue 18
Comparison of Expression of Secondary Metabolite Biosynthesis Cluster Genes in Aspergillus flavus, A. parasiticus, and A. oryzae
journal, June 2014
- Ehrlich, Kenneth; Mack, Brian
- Toxins, Vol. 6, Issue 6
Structural, Functional, and Spectroscopic Characterization of the Substrate Scope of the Novel Nitrating Cytochrome P450 TxtE
journal, September 2014
- Dodani, Sheel C.; Cahn, Jackson K. B.; Heinisch, Tillmann
- ChemBioChem, Vol. 15, Issue 15
Regulation and Role of Fungal Secondary Metabolites
journal, November 2016
- Macheleidt, Juliane; Mattern, Derek J.; Fischer, Juliane
- Annual Review of Genetics, Vol. 50, Issue 1
Nitric oxide reductases of prokaryotes with emphasis on the respiratory, heme?copper oxidase type
journal, January 2005
- Zumft, W.
- Journal of Inorganic Biochemistry, Vol. 99, Issue 1
Comprehensive annotation of secondary metabolite biosynthetic genes and gene clusters of Aspergillus nidulans, A. fumigatus, A. niger and A. oryzae
journal, January 2013
- Inglis, Diane O.; Binkley, Jonathan; Skrzypek, Marek S.
- BMC Microbiology, Vol. 13, Issue 1
N2O Evolution by Green Algae
journal, January 1984
- Weathers, Pamela J.
- Applied and Environmental Microbiology, Vol. 48, Issue 6
Novel P450nor Gene Detection Assay Used To Characterize the Prevalence and Diversity of Soil Fungal Denitrifiers
journal, May 2016
- Novinscak, Amy; Goyer, Claudia; Zebarth, Bernie J.
- Applied and Environmental Microbiology, Vol. 82, Issue 15
Anaerobic denitrification in fungi from the coastal marine sediments off Goa, India
journal, January 2009
- Cathrine, Sumathi J.; Raghukumar, Chandralata
- Mycological Research, Vol. 113, Issue 1
Bayesian Estimation of Ancestral Character States on Phylogenies
journal, October 2004
- Pagel, Mark; Meade, Andrew; Barker, Daniel
- Systematic Biology, Vol. 53, Issue 5
Oxygen requirement for denitrification by the fungus Fusarium oxysporum
journal, January 2001
- Zhou, Zhemin; Takaya, Naoki; Sakairi, Maria Antonina C.
- Archives of Microbiology, Vol. 175, Issue 1
Inferring duplications, losses, transfers and incomplete lineage sorting with nonbinary species trees.
text, January 2012
- Stolzer, Maureen; Lai, Han; Xu, Minli
- Carnegie Mellon University
Basic local alignment search tool
journal, October 1990
- Altschul, Stephen F.; Gish, Warren; Miller, Webb
- Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410
Denitrification by fungi
journal, July 1992
- Shoun, Hirofumi; Kim, Du-Hyun; Uchiyama, Hiroo
- FEMS Microbiology Letters, Vol. 94, Issue 3
eggNOG v3.0: orthologous groups covering 1133 organisms at 41 different taxonomic ranges
journal, November 2011
- Powell, S.; Szklarczyk, D.; Trachana, K.
- Nucleic Acids Research, Vol. 40, Issue D1
MrBayes 3.2: Efficient Bayesian Phylogenetic Inference and Model Choice Across a Large Model Space
journal, February 2012
- Ronquist, Fredrik; Teslenko, Maxim; van der Mark, Paul
- Systematic Biology, Vol. 61, Issue 3
NOTUNG: a program for dating gene duplications and optimizing gene family trees.
text, January 2018
- Chen, Kevin; Durand, Dannie; Farach-Colton, Martin
- Figshare
Predicting active site residue annotations in the Pfam database
journal, August 2007
- Mistry, Jaina; Bateman, Alex; Finn, Robert D.
- BMC Bioinformatics, Vol. 8, Issue 1
Inferring duplications, losses, transfers and incomplete lineage sorting with nonbinary species trees
journal, September 2012
- Stolzer, Maureen; Lai, Han; Xu, Minli
- Bioinformatics, Vol. 28, Issue 18
Pathogenicity associated genes in Fusarium oxysporum f. sp. cubense race 4
journal, January 2013
- Sutherland, René; Viljoen, Altus; Myburg, Alexander A.
- South African Journal of Science, Vol. 109, Issue 5/6
Systematic and searchable classification of cytochrome P450 proteins encoded by fungal and oomycete genomes
journal, January 2012
- Moktali, Venkatesh; Park, Jongsun; Fedorova-Abrams, Natalie D.
- BMC Genomics, Vol. 13, Issue 1
The Pfam protein families database
journal, November 2009
- Finn, Robert D.; Mistry, Jaina; Tate, John
- Nucleic Acids Research, Vol. 38, Issue suppl_1
The EMBL-EBI bioinformatics web and programmatic tools framework
journal, April 2015
- Li, Weizhong; Cowley, Andrew; Uludag, Mahmut
- Nucleic Acids Research, Vol. 43, Issue W1
Cytochrome P450–catalyzed L-tryptophan nitration in thaxtomin phytotoxin biosynthesis
journal, September 2012
- Barry, Sarah M.; Kers, Johan A.; Johnson, Evan G.
- Nature Chemical Biology, Vol. 8, Issue 10
Matplotlib: A 2D Graphics Environment
journal, January 2007
- Hunter, John D.
- Computing in Science & Engineering, Vol. 9, Issue 3
FunGene: the functional gene pipeline and repository
journal, January 2013
- Fish, Jordan A.; Chai, Benli; Wang, Qiong
- Frontiers in Microbiology, Vol. 4
A new fluorescence biosensor for nitric oxide detection based on cytochrome P450 55B1
journal, July 2016
- Li, Yong; Liu, Qian; Liang, Xiaosheng
- Sensors and Actuators B: Chemical, Vol. 230
Crystal structure of cytochrome P450 MoxA from Nonomuraea recticatena (CYP105)
journal, October 2007
- Yasutake, Yoshiaki; Imoto, Noriko; Fujii, Yoshikazu
- Biochemical and Biophysical Research Communications, Vol. 361, Issue 4
eggNOG v3.0: orthologous groups covering 1133 organisms at 41 different taxonomic ranges
text, January 2012
- Powell, S.; Szklarczyk, D.; Trachana, K.
- Oxford University Press
A scalable platform to identify fungal secondary metabolites and their gene clusters
journal, June 2017
- Clevenger, Kenneth D.; Bok, Jin Woo; Ye, Rosa
- Nature Chemical Biology, Vol. 13, Issue 8
Microbial regulation of terrestrial nitrous oxide formation: understanding the biological pathways for prediction of emission rates
journal, April 2015
- Hu, Hang-Wei; Chen, Deli; He, Ji-Zheng
- FEMS Microbiology Reviews, Vol. 39, Issue 5
Diversity and evolution of bioenergetic systems involved in microbial nitrogen compound transformations
journal, February 2013
- Simon, Jörg; Klotz, Martin G.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1827, Issue 2
RNA-sequencing reveals the complexities of the transcriptional response to lignocellulosic biofuel substrates in Aspergillus niger
journal, November 2014
- Pullan, Steven T.; Daly, Paul; Delmas, Stéphane
- Fungal Biology and Biotechnology, Vol. 1, Issue 1
Occurrence and biological function of cytochrome P450 monooxygenases in the actinomycetes
journal, September 1991
- O'Keefe, D. P.; Harder, P. A.
- Molecular Microbiology, Vol. 5, Issue 9
Dynamic Evolution of Nitric Oxide Detoxifying Flavohemoglobins, a Family of Single-Protein Metabolic Modules in Bacteria and Eukaryotes
journal, April 2016
- Wisecaver, Jennifer H.; Alexander, William G.; King, Sean B.
- Molecular Biology and Evolution, Vol. 33, Issue 8
Nitrite reduction to nitrous oxide by propionibacteria: Detoxication mechanism
journal, January 1982
- Kaspar, Heinrich F.
- Archives of Microbiology, Vol. 133, Issue 2
Versatile and open software for comparing large genomes
journal, January 2004
- Kurtz, Stefan; Phillippy, Adam; Delcher, Arthur L.
- Genome Biology, Vol. 5, Issue 2, R12
Phylogenetic, taxonomic and functional diversity of fungal denitrifiers and associated N2O production efficacy
journal, April 2015
- Mothapo, Nape; Chen, Huaihai; Cubeta, Marc A.
- Soil Biology and Biochemistry, Vol. 83
How reliable is the intramolecular distribution of 15N in N2O to source partition N2O emitted from soil?
journal, October 2013
- Decock, Charlotte; Six, Johan
- Soil Biology and Biochemistry, Vol. 65
genBlastG: using BLAST searches to build homologous gene models
journal, June 2011
- She, Rong; Chu, Jeffrey Shih-Chieh; Uyar, Bora
- Bioinformatics, Vol. 27, Issue 15
The biosynthesis of nitrous oxide in the green alga Chlamydomonas reinhardtii
journal, May 2017
- Plouviez, Maxence; Wheeler, David; Shilton, Andy
- The Plant Journal, Vol. 91, Issue 1
CONSEL: for assessing the confidence of phylogenetic tree selection
journal, December 2001
- Shimodaira, H.; Hasegawa, M.
- Bioinformatics, Vol. 17, Issue 12
Intergenomic Comparisons Highlight Modularity of the Denitrification Pathway and Underpin the Importance of Community Structure for N2O Emissions
journal, December 2014
- Graf, Daniel R. H.; Jones, Christopher M.; Hallin, Sara
- PLoS ONE, Vol. 9, Issue 12
Nitrate Reductase and Nitrous Oxide Production by Fusarium oxysporum 11dn1 Under Aerobic and Anaerobic Conditions
journal, August 2000
- Kurakov, Alexander V.; Nosikov, Alexander N.; Skrynnikova, Evdokiya V.
- Current Microbiology, Vol. 41, Issue 2
Shifting the genomic gold standard for the prokaryotic species definition
journal, October 2009
- Richter, Michael; Rosselló-Móra, Ramon
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 45
Cell biology and molecular basis of denitrification.
journal, January 1997
- Zumft, W. G.
- Microbiology and molecular biology reviews : MMBR, Vol. 61, Issue 4
Detection and Diversity of Fungal Nitric Oxide Reductase Genes ( p450nor ) in Agricultural Soils
journal, March 2016
- Higgins, Steven A.; Welsh, Allana; Orellana, Luis H.
- Applied and Environmental Microbiology, Vol. 82, Issue 10
Translating biosynthetic gene clusters into fungal armor and weaponry
journal, August 2015
- Keller, Nancy P.
- Nature Chemical Biology, Vol. 11, Issue 9
Denitrification by Actinomycetes and Purification of Dissimilatory Nitrite Reductase and Azurin fromStreptomyces thioluteus
journal, September 1998
- Shoun, Hirofumi; Kano, Mitsuyoshi; Baba, Ikuko
- Journal of Bacteriology, Vol. 180, Issue 17
Nitroaromatic compounds: Environmental toxicity, carcinogenicity, mutagenicity, therapy and mechanism: Nitro aromatic pollutants
journal, February 2014
- Kovacic, Peter; Somanathan, Ratnasamy
- Journal of Applied Toxicology, Vol. 34, Issue 8
Dissimilatory nitrate reduction by Aspergillus terreus isolated from the seasonal oxygen minimum zone in the Arabian Sea
journal, January 2014
- Stief, Peter; Fuchs-Ocklenburg, Silvia; Kamp, Anja
- BMC Microbiology, Vol. 14, Issue 1
A review of stable isotope techniques for N2O source partitioning in soils: recent progress, remaining challenges and future considerations
journal, January 2008
- Baggs, E. M.
- Rapid Communications in Mass Spectrometry, Vol. 22, Issue 11
Chemical formation of hybrid di-nitrogen calls fungal codenitrification into question
journal, December 2016
- Phillips, Rebecca L.; Song, Bongkeun; McMillan, Andrew M. S.
- Scientific Reports, Vol. 6, Issue 1
BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs
journal, June 2015
- Simão, Felipe A.; Waterhouse, Robert M.; Ioannidis, Panagiotis
- Bioinformatics, Vol. 31, Issue 19
NCBI reference sequences (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins
journal, January 2007
- Pruitt, K. D.; Tatusova, T.; Maglott, D. R.
- Nucleic Acids Research, Vol. 35, Issue Database
ASTRAL-II: coalescent-based species tree estimation with many hundreds of taxa and thousands of genes
journal, June 2015
- Mirarab, Siavash; Warnow, Tandy
- Bioinformatics, Vol. 31, Issue 12
Occurrence and biological function of cytochrome P450 monooxygenases in the actinomycetes
journal, September 1991
- O'Keefe, D. P.; Harder, P. A.
- Molecular Microbiology, Vol. 5, Issue 9
Hybrid Respiration in the Denitrifying Mitochondria of Fusarium oxysporum
journal, April 2003
- Takaya, N.
- Journal of Biochemistry, Vol. 133, Issue 4
RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models
journal, August 2006
- Stamatakis, Alexandros
- Bioinformatics, Vol. 22, Issue 21
Jalview Version 2--a multiple sequence alignment editor and analysis workbench
journal, January 2009
- Waterhouse, A. M.; Procter, J. B.; Martin, D. M. A.
- Bioinformatics, Vol. 25, Issue 9
Indications for the Occurrence of Nitric Oxide Synthases in Fungi and Plants and the Involvement in Photoconidiation of Neurospora crassa
journal, August 1996
- Ninnemann, Helga; Maier, Josef
- Photochemistry and Photobiology, Vol. 64, Issue 2
Denitrification and aerobic respiration, hybrid electron transport chains and co-evolution
journal, February 2013
- Chen, Jianwei; Strous, Marc
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1827, Issue 2
Fungal and bacterial denitrification are differently affected by long-term pH amendment and cultivation of arable soil
journal, November 2012
- Herold, Miriam B.; Baggs, Elizabeth M.; Daniell, Tim J.
- Soil Biology and Biochemistry, Vol. 54
Oxygen requirement for denitrification by the fungus Fusarium oxysporum
journal, January 2001
- Zhou, Zhemin; Takaya, Naoki; Sakairi, Maria Antonina C.
- Archives of Microbiology, Vol. 175, Issue 1
Codenitrification and Denitrification Are Dual Metabolic Pathways through Which Dinitrogen Evolves from Nitrate in Streptomyces antibioticus
journal, June 2002
- Kumon, Yasuyuki; Sasaki, Yasuyuki; Kato, Isao
- Journal of Bacteriology, Vol. 184, Issue 11
NOTUNG: A Program for Dating Gene Duplications and Optimizing Gene Family Trees
journal, August 2000
- Chen, Kevin; Durand, Dannie; Farach-Colton, Martin
- Journal of Computational Biology, Vol. 7, Issue 3-4
Regulation and Role of Fungal Secondary Metabolites
journal, November 2016
- Macheleidt, Juliane; Mattern, Derek J.; Fischer, Juliane
- Annual Review of Genetics, Vol. 50, Issue 1
X-ray structure of nitric oxide reductase (cytochrome P450nor) at atomic resolution
journal, December 2001
- Shimizu, Hideaki; Park, Sam-Yong; Shiro, Yoshitsugu
- Acta Crystallographica Section D Biological Crystallography, Vol. 58, Issue 1
Isotopic Fractionation by a Fungal P450 Nitric Oxide Reductase during the Production of N 2 O
journal, August 2014
- Yang, Hui; Gandhi, Hasand; Ostrom, Nathaniel E.
- Environmental Science & Technology, Vol. 48, Issue 18
Comparison of Expression of Secondary Metabolite Biosynthesis Cluster Genes in Aspergillus flavus, A. parasiticus, and A. oryzae
journal, June 2014
- Ehrlich, Kenneth; Mack, Brian
- Toxins, Vol. 6, Issue 6
Denitrification by yeasts and occurrence of cytochrome P450nor in Trichosporon cutaneum
journal, November 1998
- Tsuruta, Sayuri; Takaya, Naoki; Zhang, Li
- FEMS Microbiology Letters, Vol. 168, Issue 1
Denitrification in pathogenic bacteria: for better or worst?
journal, May 2005
- Philippot, Laurent
- Trends in Microbiology, Vol. 13, Issue 5
FunGene: the functional gene pipeline and repository
journal, January 2013
- Fish, Jordan A.; Chai, Benli; Wang, Qiong
- Frontiers in Microbiology, Vol. 4
Denitrification in pathogenic bacteria: for better or worst?
journal, May 2005
- Philippot, Laurent
- Trends in Microbiology, Vol. 13, Issue 5
N2O production, a widespread trait in fungi
journal, April 2015
- Maeda, Koki; Spor, Aymé; Edel-Hermann, Véronique
- Scientific Reports, Vol. 5, Issue 1
Nitric oxide generated by the rice blast fungus Magnaporthe oryzae drives plant infection
journal, October 2012
- Samalova, Marketa; Johnson, Jasper; Illes, Mary
- New Phytologist, Vol. 197, Issue 1
The EMBL-EBI bioinformatics web and programmatic tools framework
journal, April 2015
- Li, Weizhong; Cowley, Andrew; Uludag, Mahmut
- Nucleic Acids Research, Vol. 43, Issue W1
RNA-sequencing reveals the complexities of the transcriptional response to lignocellulosic biofuel substrates in Aspergillus niger
journal, November 2014
- Pullan, Steven T.; Daly, Paul; Delmas, Stéphane
- Fungal Biology and Biotechnology, Vol. 1, Issue 1
Diversity and evolution of bioenergetic systems involved in microbial nitrogen compound transformations
journal, February 2013
- Simon, Jörg; Klotz, Martin G.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1827, Issue 2
Dissimilatory nitrate reduction in fungi under conditions of hypoxia and anoxia: A review
journal, September 2007
- Morozkina, E. V.; Kurakov, A. V.
- Applied Biochemistry and Microbiology, Vol. 43, Issue 5
Denitrification by yeasts and occurrence of cytochrome P450nor in Trichosporon cutaneum
journal, November 1998
- Tsuruta, Sayuri; Takaya, Naoki; Zhang, Li
- FEMS Microbiology Letters, Vol. 168, Issue 1
Indications for the Occurrence of Nitric Oxide Synthases in Fungi and Plants and the Involvement in Photoconidiation of Neurospora crassa
journal, August 1996
- Ninnemann, Helga; Maier, Josef
- Photochemistry and Photobiology, Vol. 64, Issue 2
Fungal Denitrification and Cytochrome P-450.
journal, January 1992
- Shoun, Hirofumi
- Journal of the agricultural chemical society of Japan, Vol. 66, Issue 2
Contrasting Short-Term Antibiotic Effects on Respiration and Bacterial Growth Compromises the Validity of the Selective Respiratory Inhibition Technique to Distinguish Fungi and Bacteria
journal, September 2008
- Rousk, Johannes; Demoling, Louise Aldén; Bååth, Erland
- Microbial Ecology, Vol. 58, Issue 1
New functions for the ancient globin family: bacterial responses to nitric oxide and nitrosative stress. MicroReview
journal, May 2000
- Poole, Robert K.; Hughes, Martin N.
- Molecular Microbiology, Vol. 36, Issue 4
Inferring duplications, losses, transfers and incomplete lineage sorting with nonbinary species trees.
text, January 2012
- Stolzer, Maureen; Lai, Han; Xu, Minli
- Carnegie Mellon University
A scalable platform to identify fungal secondary metabolites and their gene clusters
journal, June 2017
- Clevenger, Kenneth D.; Bok, Jin Woo; Ye, Rosa
- Nature Chemical Biology, Vol. 13, Issue 8
Fungal denitrification and nitric oxide reductase cytochrome P450nor
journal, May 2012
- Shoun, Hirofumi; Fushinobu, Shinya; Jiang, Li
- Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 367, Issue 1593
Cell biology and molecular basis of denitrification
journal, December 1997
- Zumft, W. G.
- Microbiology and Molecular Biology Reviews, Vol. 61, Issue 4
eggNOG v3.0: orthologous groups covering 1133 organisms at 41 different taxonomic ranges
journal, November 2011
- Powell, S.; Szklarczyk, D.; Trachana, K.
- Nucleic Acids Research, Vol. 40, Issue D1
MrBayes 3.2: Efficient Bayesian Phylogenetic Inference and Model Choice Across a Large Model Space
journal, February 2012
- Ronquist, Fredrik; Teslenko, Maxim; van der Mark, Paul
- Systematic Biology, Vol. 61, Issue 3
BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs
journal, June 2015
- Simão, Felipe A.; Waterhouse, Robert M.; Ioannidis, Panagiotis
- Bioinformatics, Vol. 31, Issue 19
Isotopocule analysis of biologically produced nitrous oxide in various environments: ISOTOPOCULE ANALYSIS OF BIOLOGICAL N
journal, April 2015
- Toyoda, Sakae; Yoshida, Naohiro; Koba, Keisuke
- Mass Spectrometry Reviews, Vol. 36, Issue 2
Uncovering the Genome-Wide Transcriptional Responses of the Filamentous Fungus Aspergillus niger to Lignocellulose Using RNA Sequencing
journal, August 2012
- Delmas, Stéphane; Pullan, Steven T.; Gaddipati, Sanyasi
- PLoS Genetics, Vol. 8, Issue 8
Bayesian Estimation of Ancestral Character States on Phylogenies
journal, October 2004
- Pagel, Mark; Meade, Andrew; Barker, Daniel
- Systematic Biology, Vol. 53, Issue 5
Fungal Cytochrome P450 Monooxygenases: Their Distribution, Structure, Functions, Family Expansion, and Evolutionary Origin
journal, June 2014
- Chen, Wanping; Lee, Mi-Kyung; Jefcoate, Colin
- Genome Biology and Evolution, Vol. 6, Issue 7
ASTRAL-II: coalescent-based species tree estimation with many hundreds of taxa and thousands of genes
journal, June 2015
- Mirarab, Siavash; Warnow, Tandy
- Bioinformatics, Vol. 31, Issue 12
A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data
journal, September 2016
- Spatafora, Joseph W.; Chang, Ying; Benny, Gerald L.
- Mycologia, Vol. 108, Issue 5
Structural, Functional, and Spectroscopic Characterization of the Substrate Scope of the Novel Nitrating Cytochrome P450 TxtE
journal, September 2014
- Dodani, Sheel C.; Cahn, Jackson K. B.; Heinisch, Tillmann
- ChemBioChem, Vol. 15, Issue 15
Nucleotide sequence of the unique nitrate/nitrite-inducible cytochrome P-450 cDNA from Fusarium oxysporum
journal, June 1991
- Kizawa, H.; Tomura, D.; Oda, M.
- Journal of Biological Chemistry, Vol. 266, Issue 16
Draft Genome Sequence of Medusavirus Stheno, Isolated from the Tatakai River of Uji, Japan
journal, January 2021
- Yoshida, Koki; Zhang, Ruixuan; Garcia, Kimberly G.
- Microbiology Resource Announcements, Vol. 10, Issue 1
Nitrous Oxide (N2O) production in axenic Chlorella vulgaris microalgae cultures: evidence, putative pathways, and potential environmental impacts
journal, January 2013
- Guieysse, B.; Plouviez, M.; Coilhac, M.
- Biogeosciences, Vol. 10, Issue 10
Phylogenetic, taxonomic and functional diversity of fungal denitrifiers and associated N2O production efficacy
journal, April 2015
- Mothapo, Nape; Chen, Huaihai; Cubeta, Marc A.
- Soil Biology and Biochemistry, Vol. 83
Spectroscopic and Kinetic Studies on Reaction of Cytochrome P450nor with Nitric Oxide: IMPLICATION FOR ITS NITRIC OXIDE REDUCTION MECHANISM
journal, January 1995
- Shiro, Yoshitsugu; Fujii, Motoyasu; Iizuka, Tetsutaro
- Journal of Biological Chemistry, Vol. 270, Issue 4
FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments
journal, March 2010
- Price, Morgan N.; Dehal, Paramvir S.; Arkin, Adam P.
- PLoS ONE, Vol. 5, Issue 3
Chrysamides A–C, Three Dimeric Nitrophenyl trans -Epoxyamides Produced by the Deep-Sea-Derived Fungus Penicillium chrysogenum SCSIO41001
journal, July 2016
- Chen, Shengtian; Wang, Junfeng; Lin, Xiuping
- Organic Letters, Vol. 18, Issue 15
Cytochrome P-450 55A1 (P-450dNIR) acts as nitric oxide reductase employing NADH as the direct electron donor.
journal, April 1993
- Nakahara, K.; Tanimoto, T.; Hatano, K.
- Journal of Biological Chemistry, Vol. 268, Issue 11
Denitrification by the fungus Fusarium oxysporum and involvement of cytochrome P-450 in the respiratory nitrite reduction
journal, June 1991
- Shoun, H.; Tanimoto, T.
- Journal of Biological Chemistry, Vol. 266, Issue 17
Works referencing / citing this record:
Ecological and physiological implications of nitrogen oxide reduction pathways on greenhouse gas emissions in agroecosystems
journal, May 2019
- Yoon, Sukhwan; Song, Bongkeun; Phillips, Rebecca L.
- FEMS Microbiology Ecology, Vol. 95, Issue 6
Genome-scale phylogeny and contrasting modes of genome evolution in the fungal phylum Ascomycota
journal, November 2020
- Shen, Xing-Xing; Steenwyk, Jacob L.; LaBella, Abigail L.
- Science Advances, Vol. 6, Issue 45
Nitric oxide as a developmental and metabolic signal in filamentous fungi
journal, February 2020
- Zhao, Yanxia; Lim, Jieyin; Xu, Jianyang
- Molecular Microbiology, Vol. 113, Issue 5
Algal photosynthesis converts nitric oxide into nitrous oxide
journal, January 2020
- Burlacot, Adrien; Richaud, Pierre; Gosset, Arthur
- Proceedings of the National Academy of Sciences, Vol. 117, Issue 5
Characterization of Fungal nirK-Containing Communities and N2O Emission From Fungal Denitrification in Arable Soils
journal, February 2019
- Xu, Huifang; Sheng, Rong; Xing, Xiaoyi
- Frontiers in Microbiology, Vol. 10
Combined Use of Vinasse and Nitrogen as Fertilizers Affects Nitrification, Ammonification, and Denitrification by Prokaryotes
journal, November 2021
- de Chaves, Miriam Gonçalves; Venturini, Andressa Monteiro; Merloti, Luis Fernando
- Frontiers in Soil Science, Vol. 1