The contribution of water radiolysis to marine sedimentary life.

Water radiolysis continuously produces H2 and oxidized chemicals in wet sediment and rock. Radiolytic H2 has been identified as the primary electron donor (food) for microorganisms in continental aquifers kilometers below Earth's surface. Radiolytic products may also be significant for sustaining life in subseafloor sediment and subsurface environments of other planets. However, the extent to which most subsurface ecosystems rely on radiolytic products has been poorly constrained, due to incomplete understanding of radiolytic chemical yields in natural environments. Here we show that all common marine sediment types catalyse radiolytic H2 production, amplifying yields by up to 27X relative to pure water. In electron equivalents, the global rate of radiolytic H2 production in marine sediment appears to be 1-2% of the global organic flux to the seafloor. However, most organic matter is consumed at or near the seafloor, whereas radiolytic H2 is produced at all sediment depths. Comparison of radiolytic H2 consumption rates to organic oxidation rates suggests that water radiolysis is the principal source of biologically accessible energy for microbial communities in marine sediment older than a few million years. Where water permeates similarly catalytic material on other worlds, life may also be sustained by water radiolysis.

Atribacteria Reproducing over Millions of Years in the Atlantic Abyssal Subseafloor.

How microbial metabolism is translated into cellular reproduction under energy-limited settings below the seafloor over long timescales is poorly understood. Here, we show that microbial abundance increases an order of magnitude over a 5 million-year-long sequence in anoxic subseafloor clay of the abyssal North Atlantic Ocean. This increase in biomass correlated with an increased number of transcribed protein-encoding genes that included those involved in cytokinesis, demonstrating that active microbial reproduction outpaces cell death in these ancient sediments. Metagenomes, metatranscriptomes, and 16S rRNA gene sequencing all show that the actively reproducing community was dominated by the candidate phylum "Candidatus Atribacteria," which exhibited patterns of gene expression consistent with fermentative, and potentially acetogenic, metabolism. "Ca. Atribacteria" dominated throughout the 8 million-year-old cored sequence, despite the detection limit for gene expression being reached in 5 million-year-old sediments. The subseafloor reproducing "Ca. Atribacteria" also expressed genes encoding a bacterial microcompartment that has potential to assist in secondary fermentation by recycling aldehydes and, thereby, harness additional power to reduce ferredoxin and NAD+ Expression of genes encoding the Rnf complex for generation of chemiosmotic ATP synthesis were also detected from the subseafloor "Ca Atribacteria," as well as the Wood-Ljungdahl pathway that could potentially have an anabolic or catabolic function. The correlation of this metabolism with cytokinesis gene expression and a net increase in biomass over the million-year-old sampled interval indicates that the "Ca Atribacteria" can perform the necessary catabolic and anabolic functions necessary for cellular reproduction, even under energy limitation in millions-of-years-old anoxic sediments.IMPORTANCE The deep subseafloor sedimentary biosphere is one of the largest ecosystems on Earth, where microbes subsist under energy-limited conditions over long timescales. It remains poorly understood how mechanisms of microbial metabolism promote increased fitness in these settings. We discovered that the candidate bacterial phylum "Candidatus Atribacteria" dominated a deep-sea subseafloor ecosystem, where it exhibited increased transcription of genes associated with acetogenic fermentation and reproduction in million-year-old sediment. We attribute its improved fitness after burial in the seabed to its capabilities to derive energy from increasingly oxidized metabolites via a bacterial microcompartment and utilize a potentially reversible Wood-Ljungdahl pathway to help meet anabolic and catabolic requirements for growth. Our findings show that "Ca Atribacteria" can perform all the necessary catabolic and anabolic functions necessary for cellular reproduction, even under energy limitation in anoxic sediments that are millions of years old.

Archaea dominate oxic subseafloor communities over multimillion-year time scales.

Ammonia-oxidizing archaea (AOA) dominate microbial communities throughout oxic subseafloor sediment deposited over millions of years in the North Atlantic Ocean. Rates of nitrification correlated with the abundance of these dominant AOA populations, whose metabolism is characterized by ammonia oxidation, mixotrophic utilization of organic nitrogen, deamination, and the energetically efficient chemolithoautotrophic hydroxypropionate/hydroxybutyrate carbon fixation cycle. These AOA thus have the potential to couple mixotrophic and chemolithoautotrophic metabolism via mixotrophic deamination of organic nitrogen, followed by oxidation of the regenerated ammonia for additional energy to fuel carbon fixation. This metabolic feature likely reduces energy loss and improves AOA fitness under energy-starved, oxic conditions, thereby allowing them to outcompete other taxa for millions of years.

Cenozoic global cooling and increased seawater Mg/Ca via reduced reverse weathering.

Authigenic clay minerals formed on or in the seafloor occur in every type of marine sediment. They are recognized to be a major sink of many elements in the ocean but are difficult to study directly due to dilution by detrital clay minerals. The extremely low dust fluxes and marine sedimentation rates in the South Pacific Gyre (SPG) provide a unique opportunity to examine relatively undiluted authigenic clay. Here, using Mg isotopes and element concentrations combined with multivariate statistical modeling, we fingerprint and quantify the abundance of authigenic clay within SPG sediment. Key reactants include volcanic ash (source of reactive aluminium) and reactive biogenic silica on or shallowly buried within the seafloor. Our results, together with previous studies, suggest that global reorganizations of biogenic silica burial over the Cenozoic reduced marine authigenic clay formation, contributing to the rise in seawater Mg/Ca and decline in atmospheric CO2 over the past 50 million years.Reverse weathering reactions on or in the seafloor are a major sink of many elements and alkalinity in seawater. Here, the authors show how reduced rates of reverse weathering may be responsible for global cooling and increased seawater Mg/Ca over the past 50 million years.

Matrix Effects in Quantitative Analysis of Laser-Induced Breakdown Spectroscopy (LIBS) of Rock Powders Doped with Cr, Mn, Ni, Zn, and Co.

Obtaining quantitative chemical information using laser-induced breakdown spectroscopy is challenging due to the variability in the bulk composition of geological materials. Chemical matrix effects caused by this variability produce changes in the peak area that are not proportional to the changes in minor element concentration. Therefore the use of univariate calibrations to predict trace element concentrations in geological samples is plagued by a high degree of uncertainty. This work evaluated the accuracy of univariate minor element predictions as a function of the composition of the major element matrices of the samples and examined the factors that limit the prediction accuracy of univariate calibrations. Five different sample matrices were doped with 10-85 000 ppm Cr, Mn, Ni, Zn, and Co and then independently measured in 175 mixtures by X-ray fluorescence, inductively coupled plasma atomic emission spectrometry, and laser-induced breakdown spectroscopy, the latter at three different laser energies (1.9, 2.8, and 3.7 mJ). Univariate prediction models for minor element concentrations were created using varying combinations of dopants, matrices, normalization/no normalization, and energy density; the model accuracies were evaluated using root mean square prediction errors and leave-one-out cross-validation. The results showed the superiority of using normalization for predictions of minor elements when the predicted sample and those in the training set had matrices with similar SiO2 contents. Normalization also mitigates differences in spectra arising from laser/sample coupling effects and the use of different energy densities. Prediction of minor elements in matrices that are dissimilar to those in the training set can increase the uncertainty of prediction by an order of magnitude. Overall, the quality of a univariate calibration is primarily determined by the availability of a persistent, measurable peak with a favorable transition probability that has little to no interference from neighboring peaks in the spectra of both the unknown and those used to train it.

Relationship of Bacterial Richness to Organic Degradation Rate and Sediment Age in Subseafloor Sediment.

UNLABELLED: Subseafloor sediment hosts a large, taxonomically rich, and metabolically diverse microbial ecosystem. However, the factors that control microbial diversity in subseafloor sediment have rarely been explored. Here, we show that bacterial richness varies with organic degradation rate and sediment age. At three open-ocean sites (in the Bering Sea and equatorial Pacific) and one continental margin site (Indian Ocean), richness decreases exponentially with increasing sediment depth. The rate of decrease in richness with increasing depth varies from site to site. The vertical succession of predominant terminal electron acceptors correlates with abundance-weighted community composition but does not drive the vertical decrease in richness. Vertical patterns of richness at the open-ocean sites closely match organic degradation rates; both properties are highest near the seafloor and decline together as sediment depth increases. This relationship suggests that (i) total catabolic activity and/or electron donor diversity exerts a primary influence on bacterial richness in marine sediment and (ii) many bacterial taxa that are poorly adapted for subseafloor sedimentary conditions are degraded in the geologically young sediment, where respiration rates are high. Richness consistently takes a few hundred thousand years to decline from near-seafloor values to much lower values in deep anoxic subseafloor sediment, regardless of sedimentation rate, predominant terminal electron acceptor, or oceanographic context. IMPORTANCE: Subseafloor sediment provides a wonderful opportunity to investigate the drivers of microbial diversity in communities that may have been isolated for millions of years. Our paper shows the impact of in situ conditions on bacterial community structure in subseafloor sediment. Specifically, it shows that bacterial richness in subseafloor sediment declines exponentially with sediment age, and in parallel with organic-fueled oxidation rate. This result suggests that subseafloor diversity ultimately depends on electron donor diversity and/or total community respiration. This work studied how and why biological richness changes over time in the extraordinary ecosystem of subseafloor sediment.

Radiolytic Hydrogen Production in the Subseafloor Basaltic Aquifer.

Hydrogen (H2) is produced in geological settings by dissociation of water due to radiation from radioactive decay of naturally occurring uranium ((238)U, (235)U), thorium ((232)Th) and potassium ((40)K). To quantify the potential significance of radiolytic H2 as an electron donor for microbes within the South Pacific subseafloor basaltic aquifer, we use radionuclide concentrations of 43 basalt samples from IODP Expedition 329 to calculate radiolytic H2 production rates in basement fractures. The samples are from three sites with very different basement ages and a wide range of alteration types. U, Th, and K concentrations vary by up to an order of magnitude from sample to sample at each site. Comparison of our samples to each other and to the results of previous studies of unaltered East Pacific Rise basalt suggests that significant variations in radionuclide concentrations are due to differences in initial (unaltered basalt) concentrations (which can vary between eruptive events) and post-emplacement alteration. However, there is no clear relationship between alteration type and calculated radiolytic yields. Local maxima in U, Th, and K produce hotspots of H2 production, causing calculated radiolytic rates to differ by up to a factor of 80 from sample to sample. Fracture width also greatly influences H2 production, where microfractures are hotspots for radiolytic H2 production. For example, H2 production rates normalized to water volume are 190 times higher in 1 µm wide fractures than in fractures that are 10 cm wide. To assess the importance of water radiolysis for microbial communities in subseafloor basaltic aquifers, we compare electron transfer rates from radiolysis to rates from iron oxidation in subseafloor basalt. Radiolysis appears likely to be a more important electron donor source than iron oxidation in old (>10 Ma) basement basalt. Radiolytic H2 production in the volume of water adjacent to a square cm of the most radioactive SPG basalt may support as many as 1500 cells.

Hydrogen Utilization Potential in Subsurface Sediments.

Subsurface microbial communities undertake many terminal electron-accepting processes, often simultaneously. Using a tritium-based assay, we measured the potential hydrogen oxidation catalyzed by hydrogenase enzymes in several subsurface sedimentary environments (Lake Van, Barents Sea, Equatorial Pacific, and Gulf of Mexico) with different predominant electron-acceptors. Hydrogenases constitute a diverse family of enzymes expressed by microorganisms that utilize molecular hydrogen as a metabolic substrate, product, or intermediate. The assay reveals the potential for utilizing molecular hydrogen and allows qualitative detection of microbial activity irrespective of the predominant electron-accepting process. Because the method only requires samples frozen immediately after recovery, the assay can be used for identifying microbial activity in subsurface ecosystems without the need to preserve live material. We measured potential hydrogen oxidation rates in all samples from multiple depths at several sites that collectively span a wide range of environmental conditions and biogeochemical zones. Potential activity normalized to total cell abundance ranges over five orders of magnitude and varies, dependent upon the predominant terminal electron acceptor. Lowest per-cell potential rates characterize the zone of nitrate reduction and highest per-cell potential rates occur in the methanogenic zone. Possible reasons for this relationship to predominant electron acceptor include (i) increasing importance of fermentation in successively deeper biogeochemical zones and (ii) adaptation of H2ases to successively higher concentrations of H2 in successively deeper zones.

Glacial to Holocene changes in trans-Atlantic Saharan dust transport and dust-climate feedbacks.

Saharan mineral dust exported over the tropical North Atlantic is thought to have significant impacts on regional climate and ecosystems, but limited data exist documenting past changes in long-range dust transport. This data gap limits investigations of the role of Saharan dust in past climate change, in particular during the mid-Holocene, when climate models consistently underestimate the intensification of the West African monsoon documented by paleorecords. We present reconstructions of African dust deposition in sediments from the Bahamas and the tropical North Atlantic spanning the last 23,000 years. Both sites show early and mid-Holocene dust fluxes 40 to 50% lower than recent values and maximum dust fluxes during the deglaciation, demonstrating agreement with records from the northwest African margin. These quantitative estimates of trans-Atlantic dust transport offer important constraints on past changes in dust-related radiative and biogeochemical impacts. Using idealized climate model experiments to investigate the response to reductions in Saharan dust's radiative forcing over the tropical North Atlantic, we find that small (0.15°C) dust-related increases in regional sea surface temperatures are sufficient to cause significant northward shifts in the Atlantic Intertropical Convergence Zone, increased precipitation in the western Sahel and Sahara, and reductions in easterly and northeasterly winds over dust source regions. Our results suggest that the amplifying feedback of dust on sea surface temperatures and regional climate may be significant and that accurate simulation of dust's radiative effects is likely essential to improving model representations of past and future precipitation variations in North Africa.