Abstract
Nitrous oxide (N2O) is a potent greenhouse gas and the predominant ozone depleting substance. The only enzyme known to reduce N2O is the nitrous oxide reductase, encoded by the nosZ gene, which is present among bacteria and archaea capable of either complete denitrification or only N2O reduction to di-nitrogen gas. To determine whether the occurrence of nosZ, being a proxy for the trait N2O reduction, differed among taxonomic groups, preferred habitats or organisms having either NirK or NirS nitrite reductases encoded by the nirK and nirS genes, respectively, 652 microbial genomes across 18 phyla were compared. Furthermore, the association of different co-occurrence patterns with enzymes reducing nitric oxide to N2O encoded by nor genes was examined. We observed that co-occurrence patterns of denitrification genes were not randomly distributed across taxa, as specific patterns were found to be more dominant or absent than expected within different taxonomic groups. The nosZ gene had a significantly higher frequency of co-occurrence with nirS than with nirK and the presence or absence of a nor gene largely explained this pattern, as nirS almost always co-occurred with nor. This suggests that nirS type denitrifiers are more likely to be capable of complete denitrification and thus contribute less to N2O emissions than nirK type denitrifiers under favorable environmental conditions. Comparative phylogenetic analysis indicated a greater degree of shared evolutionary history between nosZ and nirS. However 30% of the organisms with nosZ did not possess either nir gene, with several of these also lacking nor, suggesting a potentially important role in N2O reduction. Co-occurrence patterns were also non-randomly distributed amongst preferred habitat categories, with several habitats showing significant differences in the frequencies of nirS and nirK type denitrifiers. These results demonstrate that the denitrification pathway is highly modular, thus underpinning the importance of community structure for N2O emissions.
Highlights
Managing nitrogen (N) is one of the major environmental challenges for the 21st century [1,2]
The aim of our study was to determine whether patterns of co-occurrence of nosZ, being a proxy for the trait N2O reduction, differed among nirK and nirS type denitrifiers, how this relates to taxonomic affiliation, and whether these patterns could be explained by the presence of a nor gene encoding one of the canonical nitric oxide (NO) reductases or the p450nor variant for fungal denitrifiers
The amino acid sequence for the P450-type nitric oxide reductase (P450nor) from Fusarium oxysporum [35] was used as a query for TBLASTN searches of each fungal genome, and the resulting hits were aligned to the query sequence to both correctly identify P450nor based on previously described conserved amino acid positions [28], as well as to aid in assembly of exons
Summary
Managing nitrogen (N) is one of the major environmental challenges for the 21st century [1,2]. The only known sink for N2O in Earth’s troposphere is microbial reduction to di-nitrogen (N2), catalyzed by the N2O reductase encoded by the nosZ gene. This unique enzyme is found among a wide range of bacterial and archaeal taxa capable of complete denitrification, an anaerobic respiratory process in which soluble nitrate (NO32) or nitrite (NO22) is reduced to the gases nitric oxide (NO), N2O and N2 via a series of enzymatic steps. It was recently shown that manipulation of the proportion of denitrifiers with the nosZ gene in soil microcosms significantly affected the ratio of N2O:N2 production, establishing a causal link between denitrifier community composition and potential N2O emissions [15]. The regulation of N2O emissions has a genetic basis
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