Lack of evidence for the role of gut microbiota in PAH biodegradation by the polychaete Capitella teleta

Abstract

Capitella teleta is a marine sediment-feeding polychaete known to degrade various polycyclic aromatic hydrocarbons (PAHs) and reported to possess genes involved in PAH transformation, such as those in the P450 cytochrome superfamily. Previous research focusing on biodegradation of PAHs by C. teleta demonstrated that these worms are effective biodegraders, but overlooked the possible role of its gut microbiota in facilitating PAH metabolism. Recently, C. teleta's microbiome was characterized and found to contain several bacterial genera known to contain PAH-degrading members, including Acinetobacter, Thalassotalea, and Achromobacter. Despite this, however, no data have thus far been presented demonstrating the role of C. teleta's gut microbiota in PAH degradation. The present study was designed to more conclusively determine the presence of PAH-degrading bacteria in worm digestive tracts and to more clearly distinguish the relative roles of worm versus gut-microbial metabolism in the removal of PAH from sediment. To do this, we manipulated marine sediment microorganisms and worm gut microbiota by autoclaving and antibiotic treatment, respectively. Our results showed that no fluoranthene degradation occurred in microcosms in the absence of worms. More importantly, there was no significant difference in fluoranthene degradation between antibiotic-treated and non-treated worms. We also found no evidence of fluoranthene degradation using resting cells of gut microbes of C. teleta, and we were unable to isolate fluoranthene-degrading bacterial strains from enrichments of polychaete gut contents, despite multiple attempts. Gut microbiota in worms treated with antibiotics recovered, through bidirectional transfer, between worms and sediment after 2 weeks of microcosm incubation, and gut microbes appear to be required for the survival and growth of C. teleta. Our results build on previous studies suggesting that C. teleta itself is primarily responsible for the metabolism of fluoranthene in ingested sediment. We hypothesize that C. teleta's core microbiota, which includes members of Propionibacterium as the most abundant genus, likely aid worms in obtaining key nutrients (e.g., vitamins) from its sediment diet.