Resistance of autotrophic and heterotrophic nitrifiers to prolonged soil Zn contamination

Heavy metal pollution negatively impacts soil microbiomes, but microbial communities can adapt to contamination over long-term. Even nitrifiers, often used as bioindicators of environmental pollution, can adapt, but the exact mechanisms of community adaptation remain unknown. Our aim was to study changes of autotrophic and heterotrophic nitrifier communities and their functions in soils with extremely high long-term pollution. The content of mobile forms of Zn, Cu and Pb in contaminated soils was 2000, 17 and 14 times higher than in uncontaminated soils. The results reveal that the autotrophic nitrification activity was 0.8 μg N g^-1 h^-1, only two times lower than in uncontaminated soils. High nitrification activity in contaminated soils is achieved due to the restructuring of the nitrifier community. Comammox bacteria Nitrospirota dominated in contaminated soils, while archaeal Nitrososphaera was most abundant in the uncontaminated soils. The genes of ammonium monooxygenase, nitrite oxidoreductase and heavy metal resistance genes were found in the genomes of Nitrospirota. Heavy metal resistance genes determined Zn resistance and comammox dominance in contaminated soils. Among genes associated with heterotrophic nitrification, those for nitroalkane oxidase and pyruvic oxime dioxygenase were widely present. The activity of the latter was highest in contaminated soils and was carried out by Burkholderiales. The activity of nitroalkane oxidase was lower in contaminated soils and was mainly performed by bacteria, whereas in uncontaminated soils it was probably carried out by fungi. In long-term contaminated soils, both autotrophic and heterotrophic nitrification bacteria developed resistance to high levels of heavy metals using efflux systems.