Microbial diversity drives pyrene dissipation in soil

Abstract

Soil microbial diversity is an essential driver of multiple ecosystem functions and services. However, the role and mechanisms of microbial diversity in the dissipation of persistent organic pollutants in soil are largely unexplored. Here, a gradient of soil microbial diversity was constructed artificially by a dilution-to-extinction approach to assess the role of soil microbial diversity in the dissipation of pyrene, a high molecular weight polycyclic aromatic hydrocarbon (PAH), in a 42-day microcosm experiment. The results showed that pyrene dissipation (98.1%) and the abundances of pyrene degradation genes (the pyrene dioxygenase gene nidA and the gram-positive PAH-ring hydroxylating dioxygenase gene PAH-RHDα GP) were highest in soils with high microbial diversity. Random-forest machine learning was combined with linear regression analysis to identify a range of keystone taxa (order level) associated with pyrene dissipation, including Sphingobacteriales, Vampirovibrionales, Blastocatellales, Myxococcales, Micrococcales and Rhodobacterales. The diversity of these keystone taxa was significantly and positively correlated with the abundance of pyrene degradation genes and the removal rate of pyrene. According to (partial) Mantel tests, keystone taxa diversity was the dominant factor determining pyrene dissipation compared with total microbial diversity. Moreover, co-occurrence network analysis revealed that diverse keystone taxa may drive pyrene dissipation via more positive interactions between keystone species and with other species in soil. Taken together, these findings provide new insights on the regulation of keystone taxa diversity to promote the dissipation of PAH in soil.