Microbial community structure in hadal sediments: high similarity along trench axes and strong changes along redox gradients

Abstract

Hadal trench sediments are hotspots of biogeochemical activity in the deep sea, but the biogeochemical and ecological factors that shape benthic hadal microbial communities remain unknown. Here, we sampled ten hadal sites from two trench regions with a vertical resolution of down to 1 cm. We sequenced 16S rRNA gene amplicons using universal and archaea-specific primer sets and compared the results to biogeochemical parameters. Despite bathymetric and depositional heterogeneity we found a high similarity of microbial communities within each of the two trench axes, while composition at the phylum level varied strongly with sediment depth in conjunction with the redox stratification into oxic, nitrogenous, and ferruginous zones. As a result, communities of a given sediment horizon were more similar to each other across a distance of hundreds of kilometers within each trench, than to those of adjacent horizons from the same sites separated only by centimeters. Total organic carbon content statistically only explained a small part of the variation within and between trenches, and did not explain the community differences observed between the hadal and adjacent shallower sites. Anaerobic taxa increased in abundance at the top of the ferruginous zone, seeded by organisms deposited at the sediment surface and surviving burial through the upper redox zones. While an influence of other potential factors such as geographic isolation, hydrostatic pressure, and non-steady state depositional regimes could not be discerned, redox stratification and diagenesis appear to be the main selective forces that structure community composition in hadal sediments.

Anammox bacteria drive fixed nitrogen loss in hadal trench sediments

“…While further tests are required to validate in situ metabolic rates from the lander incubations, the consistency between the two types of incubation again suggests that the activity of N 2 production was not heavily affected by recovery. The apparent lack of sensitivity to hydrostatic pressure, in conjunction with the close affiliation of hadal anammox bacteria to organisms from shallow waters, lends support to a recent hypothesis that due to continuous burial, obligate anaerobes in hadal sediments have little chance to diversify and thereby to establish specific adaptations such as piezophily (44). Instead, strains are selected from the seed stock that deposits from above and is buried through the oxic zone.…”

“…Biomolecular analysis of the abundance and phylogeny of anammox bacteria in the sediments conducted in subsamples of the sediment used for incubations included qPCR of anammox 16S rRNA genes and amplicon sequencing of the anammox-specific hzsA gene. Furthermore, a deeply sequenced 16S rRNA gene amplicon dataset obtained with "universal" primers from separate sediment cores (44) was mined for anammox bacterial sequence variants. For qPCR and hzsA sequencing, ∼1 cm 3 of sediment was sampled while setting up incubations and frozen at À80 °C.…”

“…In parallel, 16S rRNA gene data of anammox bacteria were extracted from the dataset of ref. 44 as amplicons classified either broadly in the candidate order Brocadiales or specifically in the candidate genera Anammoxoglobus, Brocadia, Jettenia, Kuenenia, or Scalindua. For phylogenetic analysis, reference sequences of anammox bacterial 16S rRNA and hzsA genes were mined from publicly available metagenomic datasets stored in the Integrated Microbial Genomes databases and the National Center for Biotechnology Information.…”

Culture Enrichment Combined With Long-Read Sequencing Facilitates Genomic Understanding of Hadal Sediment Microbes

“…In organic-rich sediments, microbial respiration depletes oxygen and nitrate within a few centimeters below the sediment surface, and makes subsurface sediments entirely dominated by anaerobic carbon remineralization processes (Durbin and Teske, 2011). Hadal sediments are usually considered as anaerobic environments, which are inhabited by a number of anaerobes (Schauberger et al, 2021). Thus, we cultured the sampled hadal sediments in a flask with anaerobic headspace to mimic the in situ environment.…”

“…In past decades, DNA cloning library and amplification of small subunit (SSU) rRNA genes are widely used to study the composition of hadal microbial community (Eloe et al, 2011;Ahmad et al, 2020;Schauberger et al, 2021). However, due to the problems relevant to sequencing depth and primer preference, microbial groups of low abundance are difficult to detect from original environmental samples.…”