Decoupled Spatial Distribution of PAHs Degraders Determined by Taxonomic 16S rRNA and Degrading Genes Across Chinese Forest Soils

Abstract

Knowing the structure and distribution of microbial communities and the underlying mechanisms shaping microbial geographic patterns is crucial for soil ecology and biogeochemical cycles of elements. Studies have explored the diversity, composition, and distribution of whole microbial communities based on taxonomic (16S rRNA) genes in many habitats. However, it is unclear whether the active microbes characterized by other genetic elements are driven by the same environmental variables and follow similar distribution patterns owing to technical limits on identifying the active functional genes in complex communities. Here, we employed ubiquitous phenanthrene as a model compound and applied DNA-stable isotope probing to investigate the active phenanthrene degraders by 16S rRNA genes and phenanthrene-degrading genes in forest soils. The effects of environmental variables and geographic distance on the diversity and composition of both genetic elements were examined. The diversity and similarity of whole microbial communities was closely linked with the total phenanthrene-degrading genes. However, the abundance and diversity of the active phenanthrene-degrading genes mismatched those of the active 16S rRNA genes, suggesting their distinct responses to environment variables and geographic distance. Geographic distance had a strong effect on the active phenanthrene-degrading community identified by taxonomic genes but not the active phenanthrene-degrading genes. Dispersal and mutation might explain the decoupled biogeographic patterns between the active taxonomic 16S rRNA and phenanthrene-degrading genes. This study provides new insights into the different driving forces for the active functional microbes characterized by various genetic elements, implying the diverse evolutionary mechanisms between functional genetic elements and 16S rRNA genes. Plain Language Summary As the most abundant organisms on Earth, microbes play important roles in ecosystem and biogeochemical cycles of elements. However, the information about the active functional microbes is limited due to deficient approaches to identify the active ones. Here we give a multiangle view about the active functional microbes by analyzing the two different genetic elements with the aid of stable isotope probing for the first time. A huge diversity of functional microbes characterized by taxonomic 16S rRNA and PAH-RHDα genes were identified from eight Chinese forest soils. We observed the uncoupling distribution between 16S rRNA and PAH-RHDα genes, and the inconsistent responses of whole microbial communities, functional microbes, and the functional genes to environmental changes, suggesting both active taxonomic and active functional genes of microbial communities should be considered in future studies. This work expands our knowledge on the diversity and environmental behavior of specific functional microbes in the environment and provides some clues on the mechanisms underlying the geographic distribution patterns of soil microbes.