Xenobiotic metabolism activity of gut microbiota from six marine species: combined taxonomic, metagenomic, and in vitro transformation analysis

Abstract

The xenobiotic metabolism driven by the gut microbiota significantly regulates the bioavailability and toxic effects of environmental pollutants such as plasticizers on aquatic organisms. However, it is still unknown whether the gut microbiota can exhibit variable metabolic ability across host species and which functional bacteria and genes are involved in xenobiotic transformation. This study investigated the enriched gut microbiota community composition and diversity of in vitro enrichment cultures from 6 marine species, namely, yellowfin seabream (Acanthopagrus latus), thorn fish (Terapon jarbua), shortnose ponyfish (Leiognathus brevirostris), mussel (Perna viridis), prawn (Parapenaeopsis hungerfordi) and crab (Charybdis riversandersoni). Pseudomonadota, Bacteroidota and Bacillota were the dominant phyla and Enterobacter, Raoultella, Klebsiella, Dysgonomanas and Lactococcus were the dominant genera in the enriched flora according to 16S rRNA sequencing. Furthermore, the metagenomic results revealed that all enriched gut microbiota presented metabolic genes for carbohydrates, amino acids, lipids, and xenobiotics. In particular, the gut microbiota of yellowfin seabream had the highest abundance of glycoside hydrolase family genes and CYP450 enzyme genes. Klebsiella was identified as a common potential degrader of xenobiotic metabolism. In addition, the Biolog plate test system confirmed that the gut microbiota can metabolize various carbon sources and drive the xenobiotic transformation. According to AWCD analysis of community level physiological profiling (CLPP), yellowfin seabream >mussel >prawn >shortnose ponyfish >crab >thorn fish. The gut microbiota of yellowfin seabream presented a stronger metabolic profile of phthalates and bisphenol analogs which reflected by their AWCD results and concentration variations. Overall, our results demonstrated the diverse metabolic abilities of the gut microbiota from six marine organisms and their potential for altering of the fate of xenobiotics in the ecosystem on the basis of combined taxonomic, metagenomic, and in vitro transformation analysis.