Organic carbon in marine sediments is a critical component of the global carbon cycle, and its degradation influences a wide range of phenomena, including the magnitude of carbon sequestration over geologic timescales, the recycling of inorganic carbon and nutrients, the dissolution and precipitation of carbonates, the production of methane and the nature of the seafloor biosphere. Although much has been learned about the factors that promote and hinder rates of organic carbon degradation in natural systems, the controls on the distribution of organic carbon in modern and ancient sediments are still not fully understood. In this review, we summarize how recent findings are changing entrenched perspectives on organic matter degradation in marine sediments: a shift from a structurally-based chemical reactivity viewpoint towards an emerging acceptance of the role of the ecosystem in organic matter degradation rates. That is, organic carbon has a range of reactivities determined by not only the nature of the organic compounds, but by the biological, geochemical, and physical attributes of its environment. This shift in mindset has gradually come about due to a greater diversity of sample sites, the molecular revolution in biology, discoveries concerning the extent and limits of life, advances in quantitative modeling, investigations of ocean carbon cycling under a variety of extreme paleo-conditions (e.g. greenhouse environments, euxinic/anoxic oceans), the application of novel analytical techniques and interdisciplinary efforts. Adopting this view across scientific disciplines will enable additional progress in understanding how marine sediments influence the global carbon cycle.
Numerous archaeal lineages are known to inhabit marine subsurface sediments, although their distributions, metabolic capacities, and interspecies interactions are still not well understood. Abundant and diverse archaea were recently reported in Costa Rica (CR) margin subseafloor sediments recovered during IODP Expedition 334. Here, we recover metagenome-assembled genomes (MAGs) of archaea from the CR margin and compare them to their relatives from shallower settings. We describe 31 MAGs of six different archaeal lineages (Lokiarchaeota, Thorarchaeota, Heimdallarchaeota, Bathyarcheota, Thermoplasmatales, and Hadesarchaea) and thoroughly analyze representative MAGs from the phyla Lokiarchaeota and Bathyarchaeota. Our analysis suggests the potential capability of Lokiarchaeota members to anaerobically degrade aliphatic and aromatic hydrocarbons. We show it is genetically possible and energetically feasible for Lokiarchaeota to degrade benzoate if they associate with organisms using nitrate, nitrite, and sulfite as electron acceptors, which suggests a possibility of syntrophic relationships between Lokiarchaeota and nitrite and sulfite reducing bacteria. The novel Bathyarchaeota lineage possesses an incomplete methanogenesis pathway lacking the methyl coenzyme M reductase complex and encodes a noncanonical acetogenic pathway potentially coupling methylotrophy to acetogenesis via the methyl branch of Wood–Ljungdahl pathway. These metabolic characteristics suggest the potential of this Bathyarchaeota lineage to be a transition between methanogenic and acetogenic Bathyarchaeota lineages. This work expands our knowledge about the metabolic functional repertoire of marine benthic archaea.
Extracellular DNA has been reported to comprise a large fraction of total DNA in near-seafloor sediment. However, the potential effect of extracellular DNA, arising from dead or moribund cells, on sequencing surveys is a critical concern that has largely not been addressed for marine sedimentary habitats. To address this concern, we interrogated freshly collected Arctic and Pacific sediment for extracellular 16S rRNA genes using the photoactive DNA-binding dye Propidium Monoazide. Significant differences between relative abundances of total (intracellular + extracellular) Bacterial 16S rRNA genes and relative abundances of intracellular Bacterial 16S rRNA genes are only detected in three of twelve shallow [10 cm below seafloor (cmbsf)] samples. Relative abundances of total Bacterial 16S rRNA genes are statistically indistinguishable from relative abundances of intracellular Bacterial 16S rRNA genes in all interrogated samples from depths greater than 10 cmbsf. 16S rRNA gene sequencing shows that even where significantly higher abundances of extracellular genes are detected, they have little or no influence on prokaryote community composition. Taxon-level analyses suggest that extracellular DNA, arising from in situdeath, may be sourced from different organisms in sediment of different ages. However, the overall effect of extracellular genes on sequencing surveys of marine sedimentary prokaryotes is minimal.
IODP Expedition 357 used two seabed drills to core 17 shallow holes at 9 sites across Atlantis Massif ocean core complex (Mid-Atlantic Ridge 30°N). The goals of this expedition were to investigate serpentinization processes and microbial activity in the shallow subsurface of highly altered ultramafic and mafic sequences that have been uplifted to the seafloor along a major detachment fault zone. More than 57 m of core were recovered, with borehole penetration ranging from 1.3 to 16.4 meters below seafloor, and core recovery as high as 75% of total penetration in one borehole. The cores show highly heterogeneous rock types and alteration associated with changes in bulk rock chemistry that reflect multiple phases of magmatism, fluid-rock interaction and mass transfer within the detachment fault zone. Recovered ultramafic rocks are dominated by pervasively serpentinized harzburgite with intervals of serpentinized dunite and minor pyroxenite veins; gabbroic rocks occur as melt impregnations and veins. Dolerite intrusions and basaltic rocks represent the latest magmatic activity. The proportion of mafic rocks is volumetrically less than the amount of mafic rocks recovered previously by drilling the central dome of Atlantis Massif at IODP Site U1309. This suggests a different mode of melt accumulation in the mantle peridotites at the ridge-transform intersection and/or a tectonic transposition of rock types within a complex detachment fault zone. The cores revealed a high degree of serpentinization and metasomatic alteration dominated by talc-amphibole-chlorite overprinting. Metasomatism is most prevalent at contacts between ultramafic and mafic domains (gabbroic and/or doleritic intrusions) and points to channeled fluid flow and silica mobility during exhumation along the detachment fault. The presence of the mafic lenses within the serpentinites and their alteration to mechanically weak talc, serpentine and chlorite may also be critical in the development of the detachment fault zone and may aid in continued unroofing of the upper mantle peridotite/gabbro sequences.
New technologies were also developed for the seabed drills to enable biogeochemical and microbiological characterization of the environment. An in situ sensor package and water sampling system recorded real-time variations in dissolved methane, oxygen, pH, oxidation reduction potential (Eh), and temperature and during drilling and sampled bottom water after drilling. Systematic excursions in these parameters together with elevated hydrogen and methane concentrations in post-drilling fluids provide evidence for active serpentinization at all sites. In addition, chemical tracers were delivered into the drilling fluids for contamination testing, and a borehole plug system was successfully deployed at some sites for future fluid sampling. A major achievement of IODP Expedition 357 was to obtain microbiological samples along a west–east profile, which will provide a better understanding of how microbial communities evolve as ultramafic and mafic rocks are altered and emplaced on the seafloor. Strict sampling handling protocols allowed for very low limits of microbial cell detection, and our results show that the Atlantis Massif subsurface contains a relatively low density of microbial life.
