skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: 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 (N 2O) emissions. Despite extensive efforts, fungal contributions to N 2O emissions remain uncertain. For example, the majority of N 2O 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 N 2O. 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.more » 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.« less

Authors:
 [1]; ORCiD logo [1];  [2]; ORCiD logo [1]
  1. Univ. of Tennessee, Knoxville, TN (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  2. Univ. of Tennessee, Knoxville, TN (United States)
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1468244
DOE Contract Number:  
AC05-00OR22725
Resource Type:
Journal Article
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. doi:10.1093/gbe/evy187.
Higgins, Steven A., Schadt, Christopher Warren, Matheny, Patrick B., and Löffler, Frank E. Sat . "Phylogenomics reveals the dynamic evolution of fungal nitric oxide reductases and their relationship to secondary metabolism". United States. doi: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},
issn = {1759-6653},
number = ,
volume = 8,
place = {United States},
year = {2018},
month = {8}
}