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Abstract 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 δ 13 C 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. 

ABSTRACT 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. 

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.

 

The fate of organic matter (OM) in the deep ocean remains enigmatic, with little understood regarding the flux and its utilization by deep food webs. We used compound-specific nitrogen stable isotope ratios of source amino acids measured in particle size classes and deep zooplankton (700–1500 m) to determine the contribution of small (0.7–53 μm) vs. large particles (> 53 μm) to their diet at four sites in the North Pacific. Our results show that small particles constitute between 9% and 98% of zooplankton diets, being the contribution higher at sites with lower flux regimes. The contribution of small particles to the diet of deep zooplankton was also higher when biomass of vertical migrators, and therefore actively transported OM, was lower. Climate-driven changes in primary production and export are expected to shift particle fluxes to smaller size classes, and thus their importance in midwater food webs may become more widespread. 

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 (δ¹⁵N 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 inδ¹⁵N values mirroring their main prey, zooplankton. Higher variance inδ¹⁵N values of bathypelagic species points to the increasing reliance of deeper dwelling micronekton on microbially reworked, very small suspended particles. Migrators have higherδ¹⁵N 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 inδ¹⁵N values seasonally than nonmigrators, likely because of their higher energy needs. The dependence on material at depth enriched in¹⁵N 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.

 

The oceans are an important global reservoir for mercury (Hg), and marine fish consumption is the dominant human exposure pathway for its toxic methylated form. A more thorough understanding of the global biogeochemical cycle of Hg requires additional information on the mechanisms that control Hg cycling in pelagic marine waters. In this study, Hg isotope ratios and total Hg concentrations are used to explore Hg biogeochemistry in oligotrophic marine environments north of Hawaii. We present the first measurements of the vertical water column distribution of Hg concentrations and the Hg isotopic composition in precipitation, marine particles, and zooplankton near Station ALOHA (22°45′N, 158°W). Our results reveal production and demethylation of methylmercury in both the euphotic (0–175 m) and mesopelagic zones (200–1,000 m). We document a strong relationship between Hg isotopic composition and depth in particles, zooplankton, and fish in the water column and diurnal variations in Δ¹⁹⁹Hg values in zooplankton sampled near the surface (25 m). Based on these observations and stable Hg isotope relationships in the marine food web, we suggest that the Hg found in large pelagic fish at Station ALOHA was originally deposited largely by precipitation, transformed into methyl‐Hg, and bioaccumulated in situ in the water column. Our results highlight how Hg isotopic compositions reflect abiotic and biotic production and degradation of methyl‐Hg throughout the water column and the importance of particles and zooplankton in the vertical transport of Hg.