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.

Megafauna of the German exploration licence area for seafloor massive sulphides along the Central and South East Indian Ridge (Indian Ocean).

BACKGROUND: The growing interest in mineral resources of the deep sea, such as seafloor massive sulphide deposits, has led to an increasing number of exploration licences issued by the International Seabed Authority. In the Indian Ocean, four licence areas exist, resulting in an increasing number of new hydrothermal vent fields and the discovery of new species. Most studies focus on active venting areas including their ecology, but the non-vent megafauna of the Central Indian Ridge and South East Indian Ridge remains poorly known.In the framework of the Indian Ocean Exploration project in the German license area for seafloor massive sulphides, baseline imagery and sampling surveys were conducted yearly during research expeditions from 2013 to 2018, using video sledges and Remotely Operated Vehicles. NEW INFORMATION: This is the first report of an imagery collection of megafauna from the southern Central Indian- and South East Indian Ridge, reporting the taxonomic richness and their distribution. A total of 218 taxa were recorded and identified, based on imagery, with additional morphological and molecular confirmed identifications of 20 taxa from 89 sampled specimens. The compiled fauna catalogue is a synthesis of megafauna occurrences aiming at a consistent morphological identification of taxa and showing their regional distribution. The imagery data were collected during multiple research cruises in different exploration clusters of the German licence area, located 500 km north of the Rodriguez Triple Junction along the Central Indian Ridge and 500 km southeast of it along the Southeast Indian Ridge.

Eurythenes atacamensis sp. nov. (Crustacea: Amphipoda) exhibits ontogenetic vertical stratification across abyssal and hadal depths in the Atacama Trench, eastern South Pacific Ocean.

Eurythenes S.I. Smith in Scudder, 1882 (Crustacea: Amphipoda) are prevalent scavengers of the benthopelagic community from bathyal to hadal depths. While a well-studied genus, molecular systematic studies have uncovered cryptic speciation and multiple undescribed lineages. Here, we apply an integrative taxonomic approach and describe the tenth species, Eurythenes atacamensis sp. nov., based on specimens from the 2018 Atacamex and RV Sonne SO261 Expeditions to the southern sector of the Peru-Chile Trench, the Atacama Trench (24-⁠21°S). Eurythenes atacamensis sp. nov. is a large species, max. observed length 83.2 mm, possesses diagnostic features, including a short gnathopod 1 palm and a chelate gnathopod 2 palm, and a distinct genetic lineage based on a 16S rRNA and COI phylogeny. This species is a dominant bait-attending fauna with an extensive bathymetric range, spanning from 4974 to 8081 m. The RV Sonne SO261 specimens were recovered along a 10-station transect from abyssal to hadal depths and further examined for demographic and bathymetric-related patterns. Ontogenetic vertical stratification was evident across the trench axis, with only juveniles present at abyssal depths (4974-6025 m). Total length-depth analysis revealed that the size of females was unrelated to depth, whereas juveniles followed a sigmoidal relationship with a step-up in size at depths >7200 m. Thus, these bathymetric trends suggest that juveniles and females employ differing ecological strategies in subduction trench environments. This study highlights that even dominant and ecologically important species are still being discovered within the abyssal and hadal environments. Continued systematic expeditions will lead to an improved understanding of the eco-evolutionary drivers of speciation in the world's largest ecosystem.

New species of Eurythenes from hadal depths of the Mariana Trench, Pacific Ocean (Crustacea: Amphipoda).

Eurythenes S. I. Smith in Scudder, 1882 are one of the largest scavenging deep-sea amphipods (max. 154 mm) and are found in every ocean across an extensive bathymetric range from the shallow polar waters to hadal depths. Recent systematic studies of the genus have illuminated a cryptic species complex and highlighted the benefits of using a combination of morphological and molecular identification approaches. In this study, we present the ninth species, Eurythenes plasticus sp. nov., which was recovered using baited traps between the depths 6010 and 6949 m in the Mariana Trench (Northwest Pacific Ocean) in 2014. This new Eurythenes species was found to have distinct morphological characteristics and be a well-supported clade based on sequence variation at two mitochondrial regions (16S rDNA and COI). While this species is new to science and lives in the remote hadal zone, it is not exempt from the impacts of anthropogenic pollution. Indeed, one individual was found to have a microplastic fibre, 83.74% similar to polyethylene terephthalate (PET), in its hindgut. As this species has a bathymetric range spanning from abyssal to hadal depths in the Central Pacific Ocean basin, it offers further insights into the biogeography of Eurythenes.

Depression chains in seafloor of contrasting morphology, Atacama Trench margin: a comment on Marsh et al. (2018).

This comment presents acoustic and visual data showing deep seafloor depression chains similar to those reported in Marsh et al. (R. Soc. open sci. 5: 180286), though from a different deep-sea setting. Marsh et al. present data collected during cruise JC120 from polymetallic nodule rich sites within the Clarion-Clipperton Fracture Zone (CCFZ), at water depths of between 3999 and 4258 m. Within this comment, we present data collected with equivalent acoustic and imaging devices on-board the RV Sonne (SO261-March/April 2018) from the Atacama Trench, approximately 4000 m depth, which shows comparable depression chains in the seafloor. In contrast with the CCFZ observations, our study area was wholly free of polymetallic nodules, an observation therefore weakening the 'ballast collection' by deep-sea diving mammals formation hypothesis discussed in their paper. We support their alternate hypothesis that if these features are indeed generated by deep-diving megafauna, then they are more likely the resultant traces of infauna feeding or marks made during opportunistic capture of benthic fish/cephalopods. We observed these potential prey fauna with lander and towed camera systems during the cruise, with example images of these presented here. Both the SO261 and JC120 cruises employed high-resolution sidescan systems at deployment altitudes seldom used routinely until the last few years during scientific deep-sea surveys. Given that both cruises found these depression chains in contrasting physical regions of the East Pacific, they may have a more ubiquitous distribution than at just these sites. Thus, the impacts of cetacean foraging behaviour on deep seafloor communities, and the potential relevance of these prey sources to deep-diving species, should be considered.

Bathyal and abyssal demersal bait-attending fauna of the Eastern Mediterranean Sea.

Baited cameras were deployed over a depth range of 532-5111 m in the Ionian Sea to characterise the large mobile fauna. The planned installation of a neutrino telescope also offers the potential for biological observatories. The current study was intended to aid observatory placement. At increasing depths, sediment was observed to become more uniform and animal burrows and tracks reduced. A total of 10 species of deep-sea fishes were identified from images; four elasmobranchs, which were not recorded deeper than 1841 m, and six teleosts. At depths > 3000 m, including Calypso Deep, the deepest point in the Mediterranean, only one fish species was observed; the Mediterranean grenadier, Coryphaenoides mediterraneus (3400-5111 m), extending this species' maximum recorded depth to 5111 m. Four species of decapod crustacea could be identified from images. The dressed deep-sea shrimp, Acanthephyra eximia (1346-5111 m) was the only invertebrate recorded at abyssal depths, including the deepest point. A faunal change was detected at ~ 1000 m depth. Incorporating other studies from the Eastern Mediterranean identified additional faunal boundaries at ~ 1500 m and ~ 2500 m. The time from landing the observation equipment to the arrival of the first fish increased exponentially with depth at a slower rate to that observed in the Atlantic Ocean. The estimated density of bait-attending deep-sea fish was, therefore, significantly impoverished compared to the Atlantic Ocean at equivalent depth. Barriers to colonisation, low resource input, and high temperature at depth relative to the Atlantic Ocean are probable causes of the impoverished fauna.

Pseudoliparis swirei sp. nov.: A newly-discovered hadal snailfish (Scorpaeniformes: Liparidae) from the Mariana Trench.

Pseudoliparis swirei sp. nov. is described from 37 individuals collected in the Mariana Trench at depths 6898-7966 m. The collection of this new species is the deepest benthic capture of a vertebrate with corroborated depth data. Here, we describe P. swirei sp. nov. and discuss aspects of its morphology, biology, distribution, and phylogenetic relationships to other hadal liparids based on analysis of three mitochondrial genes. Pseudoliparis swirei sp. nov. is almost certainly endemic to the Mariana Trench, as other hadal liparids appear isolated to a single trench/ trench system in the Kermadec, Macquarie, South Sandwich, South Orkney, Peru-Chile, Kurile-Kamchatka and Japan trenches. The discovery of another hadal liparid species, apparently abundant at depths where other fish species are few and only found in low numbers, provides further evidence for the dominance of this family among the hadal fish fauna.

Baited camera survey of deep-sea demersal fishes of the West African oil provinces off Angola: 1200-2500m depth, East Atlantic Ocean.

Deep-sea demersal fish surveys using baited cameras were undertaken in the West African oil provinces between 1297 m and 2453 m depth in 2002, 2005 and 2008. A total of 29 deployments amounting to 16,175 images encountered 31 species of bait attending deep-sea fish from 17 families. The extrapolated species richness was 34, indicating that the survey encountered over 90% of bait attending fish species in this area. The dominant species in the area were the morid Antimora rostrata, the synaphobranchids Synaphobranchus cf. kaupii and Simenchelys parasitica, the somniosid Centroscymnus coelolepis and the zoarcid Pachycara crassiceps. An unusually high diversity of bait attending macrourids was observed in addition to patchy aggregations of zoarcids. This study serves as baseline survey data on which to base future long-term environmental monitoring of fish populations in the vicinity of the West African oil provinces.

Distribution, composition and functions of gelatinous tissues in deep-sea fishes.

Many deep-sea fishes have a gelatinous layer, or subdermal extracellular matrix, below the skin or around the spine. We document the distribution of gelatinous tissues across fish families (approx. 200 species in ten orders), then review and investigate their composition and function. Gelatinous tissues from nine species were analysed for water content (96.53 ± 1.78% s.d.), ionic composition, osmolality, protein (0.39 ± 0.23%), lipid (0.69 ± 0.56%) and carbohydrate (0.61 ± 0.28%). Results suggest that gelatinous tissues are mostly extracellular fluid, which may allow animals to grow inexpensively. Further, almost all gelatinous tissues floated in cold seawater, thus their lower density than seawater may contribute to buoyancy in some species. We also propose a new hypothesis: gelatinous tissues, which are inexpensive to grow, may sometimes be a method to increase swimming efficiency by fairing the transition from trunk to tail. Such a layer is particularly prominent in hadal snailfishes (Liparidae); therefore, a robotic snailfish model was designed and constructed to analyse the influence of gelatinous tissues on locomotory performance. The model swam faster with a watery layer, representing gelatinous tissue, around the tail than without. Results suggest that the tissues may, in addition to providing buoyancy and low-cost growth, aid deep-sea fish locomotion.

The unique chemistry of Eastern Mediterranean water masses selects for distinct microbial communities by depth.

The waters of the Eastern Mediterranean are characterized by unique physical and chemical properties within separate water masses occupying different depths. Distinct water masses are present throughout the oceans, which drive thermohaline circulation. These water masses may contain specific microbial assemblages. The goal of this study was to examine the effect of physical and geological phenomena on the microbial community of the Eastern Mediterranean water column. Chemical measurements were combined with phospholipid fatty acid (PLFA) analysis and high-throughput 16S rRNA sequencing to characterize the microbial community in the water column at five sites. We demonstrate that the chemistry and microbial community of the water column were stratified into three distinct water masses. The salinity and nutrient concentrations vary between these water masses. Nutrient concentrations increased with depth, and salinity was highest in the intermediate water mass. Our PLFA analysis indicated different lipid classes were abundant in each water mass, suggesting that distinct groups of microbes inhabit these water masses. 16S rRNA gene sequencing confirmed the presence of distinct microbial communities in each water mass. Taxa involved in autotrophic nitrogen cycling were enriched in the intermediate water mass suggesting that microbes in this water mass may be important to the nitrogen cycle of the Eastern Mediterranean. The Eastern Mediterranean also contains numerous active hydrocarbon seeps. We sampled above the North Alex Mud Volcano, in order to test the effect of these geological features on the microbial community in the adjacent water column. The community in the waters overlaying the mud volcano was distinct from other communities collected at similar depths and was enriched in known hydrocarbon degrading taxa. Our results demonstrate that physical phenomena such stratification as well as geological phenomena such as mud volcanoes strongly affect microbial community structure in the Eastern Mediterranean water column.