Mercury isotopic evidence for the importance of particles as a source of mercury to marine organisms.

The origin of methylmercury in pelagic fish remains unclear, with many unanswered questions regarding the production and degradation of this neurotoxin in the water column. We used mercury (Hg) stable isotope ratios of marine particles and biota to elucidate the cycling of methylmercury prior to incorporation into the marine food web. The Hg isotopic composition of particles, zooplankton, and fish reveals preferential methylation of Hg within small (< 53 µm) marine particles in the upper 400 m of the North Pacific Ocean. Mass-dependent Hg isotope ratios (δ202Hg) recorded in small particles overlap with previously estimated δ202Hg values for methylmercury sources to Pacific and Atlantic Ocean food webs. Particulate compound specific isotope analysis of amino acids (CSIA-AA) yield δ15N values that indicate more-significant microbial decomposition in small particles compared to larger particles. CSIA-AA and Hg isotope data also suggest that large particles (> 53 µm) collected in the equatorial ocean are distinct from small particles and resemble fecal pellets. Additional evidence for Hg methylation within small particles is provided by a statistical mixing model of even mass-independent (Δ200Hg and Δ204Hg) isotope values, which demonstrates that Hg within near-surface marine organisms (0-150 m) originates from a combination of rainfall and marine particles. In contrast, in meso- and upper bathypelagic organisms (200-1,400 m), the majority of Hg originates from marine particles with little input from wet deposition. The occurrence of methylation within marine particles is supported further by a correlation between Δ200Hg and Δ199Hg values, demonstrating greater overlap in the Hg isotopic composition of marine organisms with marine particles than with total gaseous Hg or wet deposition.

Mercury isotopes identify near-surface marine mercury in deep-sea trench biota.

Mercury isotopic compositions of amphipods and snailfish from deep-sea trenches reveal information on the sources and transformations of mercury in the deep oceans. Evidence for methyl-mercury subjected to photochemical degradation in the photic zone is provided by odd-mass independent isotope values (Δ199Hg) in amphipods from the Kermadec Trench, which average 1.57‰ (±0.14, n = 12, SD), and amphipods from the Mariana Trench, which average 1.49‰ (±0.28, n = 13). These values are close to the average value of 1.48‰ (±0.34, n = 10) for methyl-mercury in fish that feed at ∼500-m depth in the central Pacific Ocean. Evidence for variable contributions of mercury from rainfall is provided by even-mass independent isotope values (Δ200Hg) in amphipods that average 0.03‰ (±0.02, n = 12) for the Kermadec and 0.07‰ (±0.01, n = 13) for the Mariana Trench compared to the rainfall average of 0.13 (±0.05, n = 8) in the central Pacific. Mass-dependent isotope values (δ202Hg) are elevated in amphipods from the Kermadec Trench (0.91 ±0.22‰, n = 12) compared to the Mariana Trench (0.26 ±0.23‰, n = 13), suggesting a higher level of microbial demethylation of the methyl-mercury pool before incorporation into the base of the foodweb. Our study suggests that mercury in the marine foodweb at ∼500 m, which is predominantly anthropogenic, is transported to deep-sea trenches primarily in carrion, and then incorporated into hadal (6,000-11,000-m) food webs. Anthropogenic Hg added to the surface ocean is, therefore, expected to be rapidly transported to the deepest reaches of the oceans.

Climate change considerations are fundamental to management of deep-sea resource extraction.

Climate change manifestation in the ocean, through warming, oxygen loss, increasing acidification, and changing particulate organic carbon flux (one metric of altered food supply), is projected to affect most deep-ocean ecosystems concomitantly with increasing direct human disturbance. Climate drivers will alter deep-sea biodiversity and associated ecosystem services, and may interact with disturbance from resource extraction activities or even climate geoengineering. We suggest that to ensure the effective management of increasing use of the deep ocean (e.g., for bottom fishing, oil and gas extraction, and deep-seabed mining), environmental management and developing regulations must consider climate change. Strategic planning, impact assessment and monitoring, spatial management, application of the precautionary approach, and full-cost accounting of extraction activities should embrace climate consciousness. Coupled climate and biological modeling approaches applied in the water and on the seafloor can help accomplish this goal. For example, Earth-System Model projections of climate-change parameters at the seafloor reveal heterogeneity in projected climate hazard and time of emergence (beyond natural variability) in regions targeted for deep-seabed mining. Models that combine climate-induced changes in ocean circulation with particle tracking predict altered transport of early life stages (larvae) under climate change. Habitat suitability models can help assess the consequences of altered larval dispersal, predict climate refugia, and identify vulnerable regions for multiple species under climate change. Engaging the deep observing community can support the necessary data provisioning to mainstream climate into the development of environmental management plans. To illustrate this approach, we focus on deep-seabed mining and the International Seabed Authority, whose mandates include regulation of all mineral-related activities in international waters and protecting the marine environment from the harmful effects of mining. However, achieving deep-ocean sustainability under the UN Sustainable Development Goals will require integration of climate consideration across all policy sectors.

Gut Microbial Divergence between Two Populations of the Hadal Amphipod Hirondellea gigas.

Hadal environments sustain diverse microorganisms. A few studies have investigated hadal microbial communities consisting of free-living or particle-associated bacteria and archaea. However, animal-associated microbial communities in hadal environments remain largely unexplored, and comparative analyses of animal gut microbiota between two isolated hadal environments have never been done so far. In the present study, 228 Gb of gut metagenomes of the giant amphipod Hirondellea gigas from two hadal trenches, the Mariana Trench and Japan Trench, were sequenced and analyzed. Taxonomic analysis identified 49 microbial genera commonly shared by the gut microbiota of the two H. gigas populations. However, the results of statistical analysis, in congruency with the alpha and beta diversity analyses, revealed significant differences in gut microbial composition across the two trenches. Abundance variation of Psychromonas, Propionibacterium, and Pseudoalteromonas species was observed. Microbial cooccurrence was demonstrated for microbes that were overrepresented in the Mariana trench. Comparison of functional potential showed that the percentage of carbohydrate metabolic genes among the total microbial genes was significantly higher in the guts of H. gigas specimens from the Mariana Trench. Integrating carbon input information and geological characters of the two hadal trenches, we propose that the differences in the community structure might be due to several selective factors, such as environmental variations and microbial interactions.IMPORTANCE The taxonomic composition and functional potential of animal gut microbiota in deep-sea environments remain largely unknown. Here, by performing comparative metagenomics, we suggest that the gut microbial compositions of two Hirondellea gigas populations from the Mariana Trench and the Japan Trench have undergone significant divergence. Through analyses of functional potentials and microbe-microbe correlations, our findings shed light on the contributions of animal gut microbiota to host adaptation to hadal environments.

Differences in the trophic ecology of micronekton driven by diel vertical migration.

Many species of micronekton perform diel vertical migrations (DVMs), which ultimately contributes to carbon export to the deep sea. However, not all micronekton species perform DVM, and the nonmigrators, which are often understudied, have different energetic requirements that might be reflected in their trophic ecology. We analyze bulk tissue and whole animal stable nitrogen isotopic compositions (δ 15N values) of micronekton species collected seasonally between 0 and 1250 m depth to explore differences in the trophic ecology of vertically migrating and nonmigrating micronekton in the central North Pacific. Nonmigrating species exhibit depth-related increases in δ 15N values mirroring their main prey, zooplankton. Higher variance in δ 15N values of bathypelagic species points to the increasing reliance of deeper dwelling micronekton on microbially reworked, very small suspended particles. Migrators have higher δ 15N values than nonmigrators inhabiting the epipelagic zone, suggesting the consumption of material during the day at depth, not only at night when they migrate closer to the surface. Migrating species also appear to eat larger prey and exhibit a higher range of variation in δ 15N values seasonally than nonmigrators, likely because of their higher energy needs. The dependence on material at depth enriched in 15N relative to surface particles is higher in migratory fish that ascend only to the lower epipelagic zone. Our results confirm that stark differences in the food habits and dietary sources of micronekton species are driven by vertical migrations.

Molecular adaptation to high pressure in cytochrome P450 1A and aryl hydrocarbon receptor systems of the deep-sea fish Coryphaenoides armatus.

Limited knowledge of the molecular evolution of deep-sea fish proteomes so far suggests that a few widespread residue substitutions in cytosolic proteins binding hydrophilic ligands contribute to resistance to the effects of high hydrostatic pressure (HP). Structure-function studies with additional protein systems, including membrane bound proteins, are essential to provide a more general picture of adaptation in these extremophiles. We explored molecular features of HP adaptation in proteins binding hydrophobic ligands, either in lipid bilayers (cytochrome P450 1A - CYP1A) or in the cytosol (the aryl hydrocarbon receptor - AHR), and their partners P450 oxidoreductase (POR) and AHR nuclear translocator (ARNT), respectively. Cloning studies identified the full-length coding sequence of AHR, CYP1A and POR, and a partial sequence of ARNT from Coryphaenoides armatus, an abyssal gadiform fish thriving down to 5000m depth. Inferred protein sequences were aligned with many non-deep-sea homologs to identify unique amino acid substitutions of possible relevance in HP adaptation. Positionally unique substitutions of various physicochemical properties were found in all four proteins, usually at sites of strong-to-absolute residue conservation. Some were in domains deemed important for protein-protein interaction or ligand binding. In addition, some involved removal or addition of beta-branched residues; local modifications of beta-branched residue patterns could be important to HP adaptation. In silico predictions further suggested that some unique substitutions might substantially modulate the flexibility of the polypeptide segment in which they are found. Repetitive motifs unique to the abyssal fish AHR were predicted to be rich in glycosylation sites, suggesting that post-translational changes could be involved in adaptation as well. Recombinant CYP1A and AHR showed functional properties (spectral characteristics, catalytic activity and ligand binding) that demonstrate proper folding at 1atm, indicating that they could be used as deep-sea fish protein models to further evaluate protein function under pressure. This article is part of a Special Issue entitled: Cytochrome P450 biodiversity and biotechnology, edited by Erika Plettner, Gianfranco Gilardi, Luet Wong, Vlada Urlacher, Jared Goldstone".

Climate change is projected to reduce carrying capacity and redistribute species richness in North Pacific pelagic marine ecosystems.

Climate change is expected to impact all aspects of marine ecosystems, including fisheries. Here, we use output from a suite of 11 earth system models to examine projected changes in two ecosystem-defining variables: temperature and food availability. In particular, we examine projected changes in epipelagic temperature and, as a proxy for food availability, zooplankton density. We find that under RCP8.5, a high business-as-usual greenhouse gas scenario, increasing temperatures may alter the spatial distribution of tuna and billfish species richness across the North Pacific basin. Furthermore, warmer waters and declining zooplankton densities may act together to lower carrying capacity for commercially valuable fish by 2-5% per decade over the 21st century. These changes have the potential to significantly impact the magnitude, composition, and distribution of commercial fish catch across the pelagic North Pacific. Such changes will in turn ultimately impact commercial fisheries' economic value. Fishery managers should anticipate these climate impacts to ensure sustainable fishery yields and livelihoods.

Carbon, Nitrogen, and Mercury Isotope Evidence for the Biogeochemical History of Mercury in Hawaiian Marine Bottomfish.

The complex biogeochemical cycle of Hg makes identifying primary sources of fish tissue Hg problematic. To identify sources and provide insight into this cycle, we combined carbon (δ13C), nitrogen amino acid (δ15NPhe), and Hg isotope (Δ199Hg, Δ201Hg, δ202Hg) data for six species of Hawaiian marine bottomfish. Results from these isotopic systems identified individuals within species that likely fed from separate food webs. Terrestrial freshwater inputs to coastal sediments were identified as the primary source of tissue Hg in the jack species, Caranx ignobilis, which inhabit shallow marine ecosystems. Thus, coastal C. ignobilis were a biological vector transporting Hg from freshwater environments into marine ecosystems. Depth profiles of Hg isotopic compositions for bottomfish (excludung C. ignobilis) were similar, but not identical, to profiles for open-ocean pelagic fishes, suggesting that in both settings inorganic Hg, which was ultimately transformed to monomethylmercury (MeHg) and bioaccumulated, was dominantly from a single source. However, differences between pelagic fish and bottomfish profiles were attributable to mass-dependent fractionation in the benthos prior to incorporation into the food web. Results also confirmed that bottomfish relied, at least in part, on a benthic food web and identified the incorporation of deeper water oceanic MeHg sources into deeper water sediments prior to food web uptake and transfer.

Marine fish may be biochemically constrained from inhabiting the deepest ocean depths.

No fish have been found in the deepest 25% of the ocean (8,400-11,000 m). This apparent absence has been attributed to hydrostatic pressure, although direct evidence is wanting because of the lack of deepest-living species to study. The common osmolyte trimethylamine N-oxide (TMAO) stabilizes proteins against pressure and increases with depth, going from 40 to 261 mmol/kg in teleost fishes from 0 to 4,850 m. TMAO accumulation with depth results in increasing internal osmolality (typically 350 mOsmol/kg in shallow species compared with seawater's 1,100 mOsmol/kg). Preliminary extrapolation of osmolalities of predicted isosmotic state at 8,000-8,500 m may indicate a possible physiological limit, as greater depths would require reversal of osmotic gradients and, thus, osmoregulatory systems. We tested this prediction by capturing five of the second-deepest known fish, the hadal snailfish (Notoliparis kermadecensis; Liparidae), from 7,000 m in the Kermadec Trench. We found their muscles to have a TMAO content of 386 ± 18 mmol/kg and osmolality of 991 ± 22 mOsmol/kg. These data fit previous extrapolations and, combined with new osmolalities from bathyal and abyssal fishes, predict isosmotic state at 8,200 m. This is previously unidentified evidence that biochemistry could constrain the depth of a large, complex taxonomic group.

Depth as a driver of evolution in the deep sea: Insights from grenadiers (Gadiformes: Macrouridae) of the genus Coryphaenoides.

Here we consider the role of depth as a driver of evolution in a genus of deep-sea fishes. We provide a phylogeny for the genus Coryphaenoides (Gadiformes: Macrouridae) that represents the breadth of habitat use and distributions for these species. In our consensus phylogeny species found at abyssal depths (>4000m) form a well-supported lineage, which interestingly also includes two non-abyssal species, C. striaturus and C. murrayi, diverging from the basal node of that lineage. Biogeographic analyses suggest the genus may have originated in the Southern and Pacific Oceans where contemporary species diversity is highest. The abyssal lineage seems to have arisen secondarily and likely originated in the Southern/Pacific Oceans but diversification of this lineage occurred in the Northern Atlantic Ocean. All abyssal species are found in the North Atlantic with the exception of C. yaquinae in the North Pacific and C. filicauda in the Southern Ocean. Abyssal species tend to have broad depth ranges and wide distributions, indicating that the stability of the deep oceans and the ability to live across wide depths may promote population connectivity and facilitate large ranges. We also confirm that morphologically defined subgenera do not agree with our phylogeny and that the Giant grenadier (formerly Albatrossia pectoralis) belongs to Coryphaenoides, indicating that a taxonomic revision of the genus is needed. We discuss the implications of our findings for understanding the radiation and diversification of this genus, and the likely role of adaptation to the abyss.

Mercury sources and trophic ecology for Hawaiian bottomfish.

In Hawaii, some of the most important commercial and recreational fishes comprise an assemblage of lutjanids and carangids called bottomfish. Despite their importance, we know little about their trophic ecology or where the mercury (Hg) that ultimately resides in their tissue originates. Here we investigated these topics, by analyzing muscle samples for mercury content, nitrogen, carbon, and amino acid specific nitrogen isotope ratios in six species distributed across different depths from the Northwestern Hawaiian Islands (NWHI) and the Main Hawaiian Islands (MHI). Fishes had different sources of nitrogen and carbon, with isotopic values suggesting benthic food sources for shallow nearshore species. High trophic position lutjanids that foraged in deeper water, benthic environments generally had higher Hg levels. Model results also suggested that benthic Hg methylation was an important source of Hg for shallow benthic feeders, while deepwater sources of mercury may be important for those with a diet that derives, at least in part, from the pelagic environment. Further, despite the lack of freshwater sources of Hg in the NWHI, statistical models explaining the variation in tissue Hg in the MHI and NWHI were nearly identical, suggesting freshwater Hg inputs were not a major source of Hg in fish tissue.

Understanding the scale of Marine protection in Hawai'i: from community-based management to the remote Northwestern Hawaiian Islands.

Ancient Hawaiians developed a sophisticated natural resource management system that included various forms of spatial management. Today there exists in Hawai'i a variety of spatial marine management strategies along a range of scales, with varying degrees of effectiveness. State-managed no-take areas make up less than 0.4% of nearshore waters, resulting in limited ecological and social benefits. There is increasing interest among communities and coastal stakeholders in integrating aspects of customary Hawaiian knowledge into contemporary co-management. A network of no-take reserves for aquarium fish on Hawai'i Island is a stakeholder-driven, adaptive management strategy that has been successful in achieving ecological objectives and economic benefits. A network of large-scale no-take areas for deepwater (100-400m) bottomfishes suffered from a lack of adequate data during their initiation; however, better technology, more ecological data, and stakeholder input have resulted in improvements and the ecological benefits are becoming clear. Finally, the Papahanaumokuakea Marine National Monument (PMNM) is currently the single largest conservation area in the United States, and one of the largest in the world. It is considered an unqualified success and is managed under a new model of collaborative governance. These case studies allow an examination of the effects of scale on spatial marine management in Hawai'i and beyond that illustrate the advantages and shortcomings of different management strategies. Ultimately a marine spatial planning framework should be applied that incorporates existing marine managed areas to create a holistic, regional, multi-use zoning plan engaging stakeholders at all levels in order to maximize resilience of ecosystems and communities.

The influence of depth on mercury levels in pelagic fishes and their prey.

Mercury distribution in the oceans is controlled by complex biogeochemical cycles, resulting in retention of trace amounts of this metal in plants and animals. Inter- and intra-specific variations in mercury levels of predatory pelagic fish have been previously linked to size, age, trophic position, physical and chemical environmental parameters, and location of capture; however, considerable variation remains unexplained. In this paper, we focus on differences in ecology, depth of occurrence, and total mercury levels in 9 species of commercially important pelagic fish (Thunnus obesus, T. albacares, Katsuwonus pelamis, Xiphias gladius, Lampris guttatus, Coryphaena hippurus, Taractichthys steindachneri, Tetrapturus audax, and Lepidocybium flavobrunneum) and in numerous representatives (fishes, squids, and crustaceans) of their lower trophic level prey sampled from the central North Pacific Ocean. Results indicate that total mercury levels of predatory pelagic fishes and their prey increase with median depth of occurrence in the water column and mimic concentrations of dissolved organic mercury in seawater. Stomach content analysis results from this study and others indicate a greater occurrence of higher-mercury containing deeper-water prey organisms in the diets of the deeper-ranging predators, X. gladius, T. obesus, and L. guttatus. While present in trace amounts, dissolved organic mercury increases with depth in the water column suggesting that the mesopelagic habitat is a major entry point for mercury into marine food webs. These data suggest that a major determinant of mercury levels in oceanic predators is their depth of forage.

Microbiomes of Hadal Fishes across Trench Habitats Contain Similar Taxa and Known Piezophiles.

Hadal snailfishes are the deepest-living fishes in the ocean, inhabiting trenches from depths of ∼6,000 to 8,000 m. While the microbial communities in trench environments have begun to be characterized, the microbes associated with hadal megafauna remain relatively unknown. Here, we describe the gut microbiomes of two hadal snailfishes, Pseudoliparis swirei (Mariana Trench) and Notoliparis kermadecensis (Kermadec Trench), using 16S rRNA gene amplicon sequencing. We contextualize these microbiomes with comparisons to the abyssal macrourid Coryphaenoides yaquinae and the continental shelf-dwelling snailfish Careproctus melanurus. The microbial communities of the hadal snailfishes were distinct from their shallower counterparts and were dominated by the same sequences related to the Mycoplasmataceae and Desulfovibrionaceae. These shared taxa indicate that symbiont lineages have remained similar to the ancestral symbiont since their geographic separation or that they are dispersed between geographically distant trenches and subsequently colonize specific hosts. The abyssal and hadal fishes contained sequences related to known, cultured piezophiles, microbes that grow optimally under high hydrostatic pressure, including Psychromonas, Moritella, and Shewanella. These taxa are adept at colonizing nutrient-rich environments present in the deep ocean, such as on particles and in the guts of hosts, and we hypothesize they could make a dietary contribution to deep-sea fishes by degrading chitin and producing fatty acids. We characterize the gut microbiota within some of the deepest fishes to provide new insight into the diversity and distribution of host-associated microbial taxa and the potential of these animals, and the microbes they harbor, for understanding adaptation to deep-sea habitats. IMPORTANCE Hadal trenches, characterized by high hydrostatic pressures and low temperatures, are one of the most extreme environments on our planet. By examining the microbiome of abyssal and hadal fishes, we provide insight into the diversity and distribution of host-associated life at great depth. Our findings show that there are similar microbial populations in fishes geographically separated by thousands of miles, reflecting strong selection for specific microbial lineages. Only a few psychropiezophilic taxa, which do not reflect the diversity of microbial life at great depth, have been successfully isolated in the laboratory. Our examination of deep-sea fish microbiomes shows that typical high-pressure culturing methodologies, which have largely remained unchanged since the pioneering work of Claude ZoBell in the 1950s, may simulate the chemical environment found in animal guts and helps explain why the same deep-sea genera are consistently isolated.

Metabolism and enzyme activities of hagfish from shallow and deep water of the Pacific Ocean.

Although hagfishes are ecologically important members of benthic communities there has been little data available on their metabolism. The oxygen consumption, enzyme activities, and muscle proximate composition of shallow living Eptatretus stoutii and deeper living E. deani were measured to investigate hagfish metabolism. Very low rates of oxygen consumption and both aerobic and anaerobic enzyme activities in the body musculature confirmed the low metabolism of hagfishes. However, significant variation in oxygen consumption existed. E. stoutii had significantly lower rates compared to those of the deeper living E. deani and two other shallow living species for which literature data was used. Both species could regulate their oxygen consumption to very low oxygen concentrations. Epatretus deani, which lives in an oxygen minimum zone, had a significantly lower critical oxygen tension (0.83 kPa) compared to E. stoutii (1.47 kPa). The deeper E. deani had greater lipid stores than E. stoutii which may reflect its deeper habitat and more sporadic food supply.

Abyssal deposit feeders are secondary consumers of detritus and rely on nutrition derived from microbial communities in their guts.

Trophic ecology of detrital-based food webs is still poorly understood. Abyssal plains depend entirely on detritus and are among the most understudied ecosystems, with deposit feeders dominating megafaunal communities. We used compound-specific stable isotope ratios of amino acids (CSIA-AA) to estimate the trophic position of three abundant species of deposit feeders collected from the abyssal plain of the Northeast Pacific (Station M; ~ 4000 m depth), and compared it to the trophic position of their gut contents and the surrounding sediments. Our results suggest that detritus forms the base of the food web and gut contents of deposit feeders have a trophic position consistent with primary consumers and are largely composed of a living biomass of heterotrophic prokaryotes. Subsequently, deposit feeders are a trophic level above their gut contents making them secondary consumers of detritus on the abyssal plain. Based on δ13C values of essential amino acids, we found that gut contents of deposit feeders are distinct from the surrounding surface detritus and form a unique food source, which was assimilated by the deposit feeders primarily in periods of low food supply. Overall, our results show that the guts of deposit feeders constitute hotspots of organic matter on the abyssal plain that occupy one trophic level above detritus, increasing the food-chain length in this detritus-based ecosystem.

Evidence for long-term seamount-induced chlorophyll enhancements.

Seamounts are ubiquitous global features often characterized by biological hotspots of diversity, biomass, and abundance, though the mechanisms responsible are poorly understood. One controversial explanation suggests seamount-induced chlorophyll enhancements (SICE) subsidize seamount ecosystems. Using a decade of satellite chlorophyll data, we report substantial long-term chlorophyll enhancements around 17% of Pacific seamounts and 45% of shallow (< 100 m) seamounts, with the highest probability of detection at shallow, low-latitude seamounts. SICE is shown to enhance chlorophyll concentrations by up to 56% relative to oceanic conditions, and SICE seamounts have two-fold higher fisheries catch relative to non-enhancing seamounts. Therefore, seamount-induced bottom-up trophic subsidies are not rare, occurring most often at shallow, heavily exploited seamounts, suggesting an important subset of seamounts experience fundamentally different trophic dynamics than previously thought.

Deep-Sea Misconceptions Cause Underestimation of Seabed-Mining Impacts.

Scientific misconceptions are likely leading to miscalculations of the environmental impacts of deep-seabed mining. These result from underestimating mining footprints relative to habitats targeted and poor understanding of the sensitivity, biodiversity, and dynamics of deep-sea ecosystems. Addressing these misconceptions and knowledge gaps is needed for effective management of deep-seabed mining.

Microbial Community Diversity Within Sediments from Two Geographically Separated Hadal Trenches.

Hadal ocean sediments, found at sites deeper than 6,000 m water depth, are thought to contain microbial communities distinct from those at shallower depths due to high hydrostatic pressures and higher abundances of organic matter. These communities may also differ from one other as a result of geographical isolation. Here we compare microbial community composition in surficial sediments of two hadal environments-the Mariana and Kermadec trenches-to evaluate microbial biogeography at hadal depths. Sediment microbial consortia were distinct between trenches, with higher relative sequence abundances of taxa previously correlated with organic matter degradation present in the Kermadec Trench. In contrast, the Mariana Trench, and deeper sediments in both trenches, were enriched in taxa predicted to break down recalcitrant material and contained other uncharacterized lineages. At the 97% similarity level, sequence-abundant taxa were not trench-specific and were related to those found in other hadal and abyssal habitats, indicating potential connectivity between geographically isolated sediments. Despite the diversity of microorganisms identified using culture-independent techniques, most isolates obtained under in situ pressures were related to previously identified piezophiles. Members related to these same taxa also became dominant community members when native sediments were incubated under static, long-term, unamended high-pressure conditions. Our results support the hypothesis that there is connectivity between sediment microbial populations inhabiting the Mariana and Kermadec trenches while showing that both whole communities and specific microbial lineages vary between trench of collection and sediment horizon depth. This in situ biodiversity is largely missed when incubating samples within pressure vessels and highlights the need for revised protocols for high-pressure incubations.