Distribution and environmental drivers of fungal denitrifiers in global soils

Abstract

The microbial process denitrification is the primary source of the greenhouse gas nitrous oxide (N2O) from terrestrial ecosystems. Fungal denitrifiers, unlike many bacteria, lack the N2O reductase and are potential sources of N2O. Still, their diversity, distribution, and environmental determinants in terrestrial ecosystems remain unresolved. We used a phylogenetically informed approach to screen 1 980 soil and rhizosphere metagenomes representing 608 globally distributed sampling sites for the denitrification marker gene nirK, coding for nitrite reductase. We show that fungal denitrifiers are sparse, yet cosmopolitan and dominated by saprotrophs and opportunistic plant pathogens. Few showed biome-specific distribution patterns. However, members of the Fusarium oxysporum species complex, known to produce substantial amounts of N2O, were proportionally more abundant and diverse in the rhizosphere than in other biomes. Fungal denitrifiers were most frequently detected in croplands but were most abundant in forest soils. The overall low abundance of fungal relative to bacterial and archaeal denitrifiers suggests that their role in denitrification and contribution to soil N2O emissions may be less important than previously suggested. Nevertheless, in relative terms, they could play a role in soils characterized by high carbon to nitrogen ratio and low pH, especially in tundra and boreal and temperate coniferous forests. Our results further indicate that plant-pathogen interactions may favor fungal denitrifiers. Thus, increasing global warming with predicted proliferation of pathogens and the fact that many of the fungi with nirK detected in the metagenomes are stress-tolerant cosmopolitans suggest that fungal denitrifier abundance may increase in terrestrial ecosystems.