Phylogenomics reveals the dynamic evolution of fungal nitric oxide reductases and their relationship to secondary metabolism

Higgins, Steven A.; Schadt, Christopher Warren; Matheny, Patrick B.; Löffler, Frank E.

doi:10.1093/gbe/evy187

Title: Phylogenomics reveals the dynamic evolution of fungal nitric oxide reductases and their relationship to secondary metabolism

Journal Article · Wed Aug 29 00:00:00 EDT 2018 · Genome Biology and Evolution

DOI:https://doi.org/10.1093/gbe/evy187· OSTI ID:1468244

Higgins, Steven A. ^[1];

^[1]; Matheny, Patrick B. ^[2];

^[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)

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.

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Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1468244

Journal Information:: Genome Biology and Evolution, Vol. 8; ISSN 1759-6653

Publisher:: Society for Molecular Biology and EvolutionCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 30 works

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Genome-scale phylogeny and contrasting modes of genome evolution in the fungal phylum Ascomycota Shen, Xing-Xing; Steenwyk, Jacob L.; LaBella, Abigail L. Science Advances, Vol. 6, Issue 45 https://doi.org/10.1126/sciadv.abd0079	journal	November 2020
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Characterization of Fungal nirK-Containing Communities and N2O Emission From Fungal Denitrification in Arable Soils Xu, Huifang; Sheng, Rong; Xing, Xiaoyi Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.00117	journal	February 2019
Combined Use of Vinasse and Nitrogen as Fertilizers Affects Nitrification, Ammonification, and Denitrification by Prokaryotes de Chaves, Miriam Gonçalves; Venturini, Andressa Monteiro; Merloti, Luis Fernando Frontiers in Soil Science, Vol. 1 https://doi.org/10.3389/fsoil.2021.746745	journal	November 2021

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