Trends of Diverse POPs in Air and Water Across the Western Atlantic Ocean: Strong Gradients in the Ocean but Not in the Air.

Oceans have remained the least well-researched reservoirs of persistent organic pollutants (POPs) globally, due to their vast scale, difficulty of access, and challenging (trace) analysis. Little data on POPs exists along South America and the effect of different currents and river plumes on aqueous concentrations. Research cruise KN210-04 (R/V Knorr) offered a unique opportunity to determine POP gradients in air, water, and their air-water exchange along South America, covering both hemispheres. Compounds of interest included polychlorinated biphenyls (PCBs), organochlorine pesticides (OCPs), polybrominated diphenylethers (PBDEs), and polycyclic aromatic hydrocarbons (PAHs). Remote tropical Atlantic Ocean atmospheric concentrations varied little between both hemispheres; for HCB, BDEs 47 and 99, they were ∼5 pg/m3, PCBs were ∼1 pg/m3, α-HCH was ∼0.2 pg/m3, and phenanthrene and other PAHs were in the low 100s pg/m3. Aqueous concentrations were dominated by PCB 52 (mean 4.1 pg/L), HCB (1.6 pg/L), and ß-HCH (1.9 pg/L), with other compounds <1 pg/L. Target PCBs tended to undergo net volatilization from the surface ocean, while gradients indicated net deposition for a-HCH. In contrast to atmospheric concentrations, which were basically unchanged between hemispheres, we detected strong gradients in aqueous POPs, with mostly nondetects in the tropical western South Atlantic. These results highlight the importance of currents and loss processes on ocean scales for the distribution of POPs.

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.

Global distribution of microbial abundance and biomass in subseafloor sediment.

The global geographic distribution of subseafloor sedimentary microbes and the cause(s) of that distribution are largely unexplored. Here, we show that total microbial cell abundance in subseafloor sediment varies between sites by ca. five orders of magnitude. This variation is strongly correlated with mean sedimentation rate and distance from land. Based on these correlations, we estimate global subseafloor sedimentary microbial abundance to be 2.9⋅10(29) cells [corresponding to 4.1 petagram (Pg) C and ∼0.6% of Earth's total living biomass]. This estimate of subseafloor sedimentary microbial abundance is roughly equal to previous estimates of total microbial abundance in seawater and total microbial abundance in soil. It is much lower than previous estimates of subseafloor sedimentary microbial abundance. In consequence, we estimate Earth's total number of microbes and total living biomass to be, respectively, 50-78% and 10-45% lower than previous estimates.

Subseafloor sedimentary life in the South Pacific Gyre.

The low-productivity South Pacific Gyre (SPG) is Earth's largest oceanic province. Its sediment accumulates extraordinarily slowly (0.1-1 m per million years). This sediment contains a living community that is characterized by very low biomass and very low metabolic activity. At every depth in cored SPG sediment, mean cell abundances are 3 to 4 orders of magnitude lower than at the same depths in all previously explored subseafloor communities. The net rate of respiration by the subseafloor sedimentary community at each SPG site is 1 to 3 orders of magnitude lower than the rates at previously explored sites. Because of the low respiration rates and the thinness of the sediment, interstitial waters are oxic throughout the sediment column in most of this region. Consequently, the sedimentary community of the SPG is predominantly aerobic, unlike previously explored subseafloor communities. Generation of H(2) by radiolysis of water is a significant electron-donor source for this community. The per-cell respiration rates of this community are about 2 orders of magnitude higher (in oxidation/reduction equivalents) than in previously explored anaerobic subseafloor communities. Respiration rates and cell concentrations in subseafloor sediment throughout almost half of the world ocean may approach those in SPG sediment.

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.

Subseafloor life and its biogeochemical impacts.

Subseafloor microbial activities are central to Earth's biogeochemical cycles. They control Earth's surface oxidation and major aspects of ocean chemistry. They affect climate on long timescales and play major roles in forming and destroying economic resources. In this review, we evaluate present understanding of subseafloor microbes and their activities, identify research gaps, and recommend approaches to filling those gaps. Our synthesis suggests that chemical diffusion rates and reaction affinities play a primary role in controlling rates of subseafloor activities. Fundamental aspects of subseafloor communities, including features that enable their persistence at low catabolic rates for millions of years, remain unknown.

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.

Mesoscale convective system surface pressure anomalies responsible for meteotsunamis along the U.S. East Coast on June 13th, 2013.

Two destructive high-frequency sea level oscillation events occurred on June 13th, 2013 along the U.S. East Coast. Seafloor processes can be dismissed as the sources, as no concurrent offshore earthquakes or landslides were detected. Here, we present evidence that these tsunami-like events were generated by atmospheric mesoscale convective systems (MCSs) propagating from inland to offshore. The USArray Transportable Array inland and NOAA tide gauges along the coast recorded the pressure anomalies associated with the MCSs. Once offshore, the pressure anomalies generated shallow water waves, which were amplified by the resonance between the water column and atmospheric forcing. Analysis of the tidal data reveals that these waves reflected off the continental shelf break and reached the coast, where bathymetry and coastal geometry contributed to their hazard potential. This study demonstrates that monitoring MCS pressure anomalies in the interior of the U.S. provides important observations for early warnings of MCS-generated tsunamis.

Aerobic microbial respiration in 86-million-year-old deep-sea red clay.

Microbial communities can subsist at depth in marine sediments without fresh supply of organic matter for millions of years. At threshold sedimentation rates of 1 millimeter per 1000 years, the low rates of microbial community metabolism in the North Pacific Gyre allow sediments to remain oxygenated tens of meters below the sea floor. We found that the oxygen respiration rates dropped from 10 micromoles of O(2) liter(-1) year(-1) near the sediment-water interface to 0.001 micromoles of O(2) liter(-1) year(-1) at 30-meter depth within 86 million-year-old sediment. The cell-specific respiration rate decreased with depth but stabilized at around 10(-3) femtomoles of O(2) cell(-1) day(-1) 10 meters below the seafloor. This result indicated that the community size is controlled by the rate of carbon oxidation and thereby by the low available energy flux.