Quantitative and phylogenetic study of the Deep Sea Archaeal Group in sediments of the Arctic mid-ocean spreading ridge

Abstract

In marine sediments archaea often constitute a considerable part of the microbial community, of which the Deep Sea Archaeal Group (DSAG) is one of the most predominant. Despite their high abundance no members from this archaeal group have so far been characterized and thus their metabolism is unknown. Here we show that the relative abundance of DSAG marker genes can be correlated with geochemical parameters, allowing prediction of both the potential electron donors and acceptors of these organisms. We estimated the abundance of 16S rRNA genes from Archaea, Bacteria, and DSAG in 52 sediment horizons from two cores collected at the slow-spreading Arctic Mid-Ocean Ridge, using qPCR. The results indicate that members of the DSAG make up the entire archaeal population in certain horizons and constitute up to ~50% of the total microbial community. The quantitative data were correlated to 30 different geophysical and geochemical parameters obtained from the same sediment horizons. We observed a significant correlation between the relative abundance of DSAG 16S rRNA genes and the content of organic carbon (p < 0.0001). Further, significant co-variation with iron oxide, and dissolved iron and manganese (all p < 0.0000), indicated a direct or indirect link to iron and manganese cycling. Neither of these parameters correlated with the relative abundance of archaeal or bacterial 16S rRNA genes, nor did any other major electron donor or acceptor measured. Phylogenetic analysis of DSAG 16S rRNA gene sequences reveals three monophyletic lineages with no apparent habitat-specific distribution. In this study we support the hypothesis that members of the DSAG are tightly linked to the content of organic carbon and directly or indirectly involved in the cycling of iron and/or manganese compounds. Further, we provide a molecular tool to assess their abundance in environmental samples and enrichment cultures.

Geochemical controls on the distribution and composition of biogenic and sedimentary carbon

“…Typified by slow sedimentation rates and sparse inputs of organic carbon, these environments nonetheless sustain active microbial communities Kallmeyer et al, 2012;Jørgensen et al, 2013; at depths of up to ~2.5 km below seafloor utilizing a range of adaptations to garner energy from the environment (Lever et al, 2015). Oxygenated sediments comprise 9-37% of the global seafloor and likewise contain active microbial communities that couple aerobic respiration to oxidation of organic matter, despite its scarcity in those environments (Archer et al, 2002;.…”

“…A range of mechanisms, however, likely contribute to decreased reactivity, from recalcitrance to preservation of otherwise more "labile" OC due to association with mineral surfaces or electron acceptor limitation. Indeed, sediment geochemical parameters structure the microbial communities present with lithology, redox, and OC all appearing to play major roles (Parkes et al, 2005;Durbin & Teske, 2011;Picard & Ferdelman, 2011;Jorgensen et al, 2012;Jørgensen et al, 2013). Whether this correlation is due to changes in chemical potential, geochemistry-induced shifts in compound bioavailability (e.g.…”

“…In work on sediments from the South Pacific Gyre, Fischer et al (2009) water geochemistry have been linked to variations in community structure (Picard & Ferdelman, 2011;Jorgensen et al, 2012;Jørgensen et al, 2013). Likewise, find that up to 20% of OC over a range of sedimentary environments is associated with iron oxide minerals and that associated OC is enriched in δ 13 C, suggesting that the abundance of specific mineral classes could affect both the content and composition of OC.…”

“…These organisms survive at the limits of life, at depths of up to ~2.5 km below seafloor using a diverse range of metabolisms and adaptations to garner energy from the environment (Jørgensen and Marshall 2016;Lever et al 2015). Heterotrophic metabolisms are active in the deep subsurface Jørgensen et al 2013;, sustained by buried organic carbon and electron acceptors from the photosynthetic surface environment . Oxygenated sediments comprise 9-37% of the global seafloor and likewise contain active microbial communities that couple aerobic respiration to oxidation of organic matter, despite its scarcity in those environments (Archer et al, 2002;.…”

“…Low sedimentation rates generate old, carbon-starved sediments with organisms utilizing an array of metabolisms and adaptations to garner energy from the environment (Lever et al, 2015;Jørgensen & Marshall, 2016) and partitioning into niches along gradients in organic carbon concentrations Jørgensen et al, 2013). This biomass turns over on extremely long time scales and may primarily be dormant or engaging in cell repair but not division Lever et al, 2015).…”