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

by Steven A Higgins, Christopher W Schadt, Brandon Matheny, Frank E Loeffler
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Genome Biology and Evolution
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Fungi expressing P450nor, an unconventional nitric oxide (NO) reducing cytochrome P450, are thought to be significant contributors to soil nitrous oxide (N2O) emissions. However, conflicting evidence of fungal N2O production engenders uncertainty in fungal contributions to N2O emissions. N2O emitted from antibiotic-amended soil microcosms is attributed to fungal activity, yet fungal isolates examined in pure culture exhibit low N2O-producing activity. To assist in reconciling these conflicting observations and produce a benchmark genomic analysis of fungal denitrifiers, genes underlying fungal denitrification were examined in >700 fungal genomes. Of 167 p450nor–containing genomes identified, 0, 18, and 29 % 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) suggests P450nor’s primary role is not 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. These findings underscore the potential physiological implications of widespread p450nor gene transfer, support the novel affiliation of p450nor with SM, and challenge the hypothesis of p450nor’s primary role in denitrification.