Metagenomics reveals the high polycyclic aromatic hydrocarbon-degradation potential of abundant uncultured bacteria from chronically polluted subantarctic and temperate coastal marine environments

Abstract

Aims: To investigate the potential to degrade polycyclic aromatic hydrocarbons (PAHs) of yet-to-be-cultured bacterial populations from chronically polluted intertidal sediments.

Methods and results: A gene variant encoding the alpha subunit of the catalytic component of an aromatic-ring-hydroxylating oxygenase (RHO) was abundant in intertidal sediments from chronically polluted subantarctic and temperate coastal environments, and its abundance increased after PAH amendment. Conversely, this marker gene was not detected in sediments from a nonimpacted site, even after a short-term PAH exposure. A metagenomic fragment carrying this gene variant was identified in a fosmid library of subantarctic sediments. This fragment contained five pairs of alpha and beta subunit genes and a lone alpha subunit gene of oxygenases, classified as belonging to three different RHO functional classes. In silico structural analysis suggested that two of these oxygenases contain large substrate-binding pockets, capable of accepting high molecular weight PAHs.

Conclusions: The identified uncultured micro-organism presents the potential to degrade aromatic hydrocarbons with various chemical structures, and could represent an important member of the PAH-degrading community in these polluted coastal environments.

Significance and impact of the study: This work provides valuable information for the design of environmental molecular diagnostic tools and for the biotechnological application of RHO enzymes.

Keywords: intertidal sediments; metagenomic library; polycyclic aromatic hydrocarbons; protein modelling; quantitative PCR; ring-hydroxylating oxygenases.