High prokaryotic biodiversity associated with gut contents of the holothurian Molpadia musculus from the Nazaré Canyon (NE Atlantic)

Abstract

Sediments in the Nazaré Canyon (NE Atlantic) are inhabited by unexpectedly high abundances of the deposit-feeding holothurian Molpadia musculus. The energetic demand of such a large megafaunal biomass is presumably high and requires the efficient exploitation of the food inputs coming from the photic zone. We hypothesise the existence of cooperative interactions between these deep-sea holothurians and prokaryotes in their guts. To investigate these interactions, sediment samples and holothurians were collected at ca. 3500m depth using a Remote Operated Vehicle (ROV) and an incubation chamber used to “harvest” faeces from the holothurian. In all of these samples (ingested sediment from different sectors of the holothurian gut content, faeces and sediments) we determined total prokaryotic abundance, the relative abundance of Bacteria and Archaea (by means of Catalysed Reporter Deposition-Fluorescence in situ Hybridisation) and bacterial diversity (by means of fingerprinting techniques: ARISA and T-RFLP). Prokaryotic abundances and bacterial diversity in the holothurian gut were very high (up to 105 bacterial Operational Taxonomic Units) and significantly greater than in surrounding bottom sediments. Archaea represented a key component within the gut of the holothurians and in certain tracts dominated the prokaryotic assemblage. We also found that ca. 40% of bacterial OTUs were associated uniquely with the gut contents (i.e., absent in surrounding sediments). These findings suggest the occurrence of wide and highly diversified interactions between prokaryotes and deep-sea holothurians. Results presented here provide new insights into the potential relationships between deep-sea holothurians and specific associations of Archaea and Bacteria within their guts. The work opens new perspectives for investigating the diversity of prokaryotes associated to deep-sea megafauna.