Hadal Environments Research Articles

Genomic Characteristics and Potential Metabolic Adaptations of Hadal Trench Roseobacter and Alteromonas Bacteria Based on Single-Cell Genomics Analyses.

Heterotrophic bacteria such as those from the Roseobacter group and genus Alteromonas dominate the hadal zones of oceans; however, we know little about the genomic characteristics and potential metabolic adaptations of hadal trench-dwelling bacteria. Here, we report multiple single amplified genomes (SAGs) belonging to Roseobacter and Alteromonas, recovered from the hadal zone of the Mariana Trench. While phylogenetic analyses show that these hadal SAGs cluster with their surface relatives, an analysis of genomic recruitment indicates that they have higher relative abundances in the hadal zone of the Mariana Trench. Comparative genomic analyses between the hadal SAGs and reference genomes of closely related shallow-water relatives indicate that genes involved in the mobilome (prophages and transposons) are overrepresented among the unique genes of the hadal Roseobacter and Alteromonas SAGs; the functional proteins encoded by this category of genes also shows higher amino acid sequence variation than those encoded by other gene sets within the Roseobacter SAGs. We also found that genes involved in cell wall/membrane/envelope biogenesis, transcriptional regulation, and metal transport may be important for the adaptation of hadal Roseobacter and Alteromonas lineages. These results imply that the modification of cell surface-related proteins and transporters is the major direction of genomic evolution in Roseobacter and Alteromonas bacteria adapting to the hadal environment, and that prophages and transposons may be the key factors driving this process.

Genomic analysis of Brevundimonas mediterranea D151-2-6 isolated from hadal sediment of the Pacific Ocean.

Brevundimonas mediterranea D151-2-6 is a marine bacterium that has been isolated from 6582-m hadal sediment of the Pacific Ocean. Here, we present the complete genome sequence of B. mediterranea D151-2-6. The genome of strain D151-2-6 is 3,383,373 base pairs in size. It contains one circular chromosome with an average G+C content of 67.41%, 53 tRNAs, and 3270 protein-coding genes. Genomic analysis of strain D151-2-6 revealed that its genome is more highly enriched in genes that encode proteins involved in signal transduction and transcription than any of the other available completely sequenced Brevundimonas genomes. Some of these genes might improve ecological fitness in the hadal extreme environment. Genomic information on B. mediterranea D151-2-6 provides insights into the adaptation strategies and physiological features of Brevundimonas spp. in the hadal environment.

Characteristics and implications of isoprenoid and hydroxy tetraether lipids in hadal sediments of Mariana and Yap Trenches

As one of the least-explored regions on Earth, the hadal zone remains poorly understood in terms of sedimentary organic geochemistry. This study examined the composition of isoprenoid glycerol dialkyl glycerol tetraethers (Iso-GDGTs) and hydroxy GDGTs (OH-GDGTs) in sediment cores with water depths ranging from 5058 to 10,911 m from the Mariana and Yap Trenches. The results showed a higher proportion of GDGT-0 (25–73%, mean = 49%) in the trench Iso-GDGTs pool than those from shallower ocean counterparts (<5000 m). Properties, including higher values of the [GDGT-2/GDGT-3] ratio (7.17–20.03, mean = 13.02) and the [GDGT-0/Crenarchaeol] ratio (0.49–3.94, mean = 1.48), as well as a dominance of OH-GDGT-0 in the OH-GDGTs, are similar to characteristics observed in other cold deep marine environments rather than tropical shallow ocean. Ring Index decreased with increasing water depth of the sampling sites, corresponding with increased fractional abundance of acyclic Iso-GDGTs and OH-GDGTs. Paleothermometer TEX86 in the surface sediments (>5000 m) revealed a significant negative linear correlation with water depth (TEX86H: R2 = 0.89, p < 0.01; TEX86L: R2 = 0.89, p < 0.01), leading to a bias toward lower proxy-derived temperatures. This is likely due to the increased incorporation of cold- and pressure- adapted species of archaea in dark ocean. Overall, this study provided implications of the extreme water depth effect on the distribution of isoprenoid and hydroxy tetraether lipids, as well as the proxy application in hadal environments.

Microbial community and geochemical analyses of trans-trench sediments for understanding the roles of hadal environments

Hadal trench bottom (>6000 m below sea level) sediments harbor higher microbial cell abundance compared with adjacent abyssal plain sediments. This is supported by the accumulation of sedimentary organic matter (OM), facilitated by trench topography. However, the distribution of benthic microbes in different trench systems has not been well explored yet. Here, we carried out small subunit ribosomal RNA gene tag sequencing for 92 sediment subsamples of seven abyssal and seven hadal sediment cores collected from three trench regions in the northwest Pacific Ocean: the Japan, Izu-Ogasawara, and Mariana Trenches. Tag-sequencing analyses showed specific distribution patterns of several phyla associated with oxygen and nitrate. The community structure was distinct between abyssal and hadal sediments, following geographic locations and factors represented by sediment depth. Co-occurrence network revealed six potential prokaryotic consortia that covaried across regions. Our results further support that the OM cycle is driven by hadal currents and/or rapid burial shapes microbial community structures at trench bottom sites, in addition to vertical deposition from the surface ocean. Our trans-trench analysis highlights intra- and inter-trench distributions of microbial assemblages and geochemistry in surface seafloor sediments, providing novel insights into ultradeep-sea microbial ecology, one of the last frontiers on our planet.

Biodiversity of echiurans (Echiura) of the Kuril-Kamchatka Trench area

During KuramBio and KuramBioII (Kuril Kamchatka Biodiversity Studies) expeditions of 2012 and 2016 years, 12 sites across the Kuril-Kamchatka abyssal plain and 11 sites along Kuril-Kamchatka Trench area (KKT) were surveyed and sampled and benthic communities were investigated. Samples, which comprised over 300 echiurans from 12 species of 11 genera belonging to the family Bonelliidae and Thalassematidae, were collected. The family Bonelliidae is most common in abyssal and hadal environments in the world ocean with high abundances in all investigated regions, while Thalassematidae is reported first time from the hadal depth. Species identified as representative of the genera Maxmuelleria have been noted first time in Pacific. Previously known echiuran Bonellia pacifica suggested to be Pseudoikedella achaeta. The description of deep-water echiurans from the investigated areas is the second one based on complete specimens with living colouration. The descriptions provide new information on the distribution, abundance, morphology and taxonomic details of the species, which were previously noted from the northwestern Pacific and described from damaged or incomplete specimens. The knowledge of the geographic ranges of these genera are expanded and discussed.

Massive Loss of Olfactory Receptors But Not Trace Amine-Associated Receptors in the World's Deepest-Living Fish (Pseudoliparis swirei).

Olfactory receptor repertoires show highly dynamic evolution associated with ecological adaptations in different species. The Mariana snailfish (Pseudoliparis swirei) living below a depth of 6000 m in the Mariana Trench evolved degraded vision and occupies a specific feeding habitat in a dark, low-food environment. However, whether such adaptations involve adaptive changes in the chemosensory receptor repertoire is not known. Here, we conducted a comparative analysis of the olfactory receptor (OR) and trace amine-associated receptor (TAAR) gene repertoires in nine teleosts with a focus on the evolutionary divergence between the Mariana snailfish and its shallow-sea relative, Tanaka’s snailfish (Liparis tanakae). We found many fewer functional OR genes and a significantly higher fraction of pseudogenes in the Mariana snailfish, but the numbers of functional TAAR genes in the two species were comparable. Phylogenetic analysis showed that the expansion patterns of the gene families were shared by the two species, but that Mariana snailfish underwent massive gene losses in its OR repertoire. Despite an overall decreased size in OR subfamilies and a reduced number of TAAR subfamilies in the Mariana snailfish, expansion of certain subfamilies was observed. Selective pressure analysis indicated greatly relaxed selective strength in ORs but a slightly enhanced selective strength in TAARs of Mariana snailfish. Overall, our study reveals simplified but specific OR and TAAR repertoires in the Mariana snailfish shaped by natural selection with respect to ecological adaptations in the hadal environment. This is the first study on the chemosensation evolution in vertebrates living in the hadal zone, which could provide new insights into evolutionary adaptation to the hadal environment.

Characteristics of the archaeal and bacterial communities in core sediments from Southern Yap Trench via in situ sampling by the manned submersible Jiaolong

The hadal environment is the deepest part of the ocean and harbors a significant number of unique microbial communities. Here, we collected core sediment samples of Southern Yap Trench with the deep-sea manned submersible Jiaolong and analyzed the microbial community structure and abundance in the samples through high-throughput sequencing and real-time fluorescence quantitative PCR (qPCR), taking physicochemical parameters into account to explore potential environmental drivers and metabolic pathways therein. Considering the typical “V-shape” topography and frequent sediment collapses on trench walls, the core sediments of Southern Yap Trench harbored distinct microbial populations with fluctuating distributions and metabolic processes dominated by Proteobacteria and Thaumarchaeota. To discover the main potential metabolic processes of microbes, functional genes were detected by qPCR. The abundance of bacteria was greater than that of archaea in Southern Yap Trench sediments. The abundance of ammonia-oxidizing archaea (AOA), ammonia-oxidizing bacteria (AOB), sulfate-reducing bacteria (SRB) and denitrifying bacteria (denitrifier) decreased with increasing depth and decreasing total organic carbon (TOC%) and total nitrogen (TN%) and showed a positive and significant correlation with TOC% (P < 0.01), TN% (P < 0.01), TOC/TN molar ratio (C/N ratio) (P < 0.01) and median grain size (P < 0.01). From the perspective of function based on the 16S rRNA gene, aerobic ammonium oxidization, carbon assimilation, and chemoheterotrophic function may be the dominant processes in Southern Yap Trench sediments. Moreover, considering the isolated geomorphological and hydrological characteristics of Southern Yap Trench, we hypothesized that the distinct hadal microbial ecosystem was driven by the endogenous recycling of organic matter in the hadal sediments associated with the trench geomorphology.

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.

On the Success of the Hadal Snailfishes.

SynopsisDeep-sea trenches, depths 6000–11,000 m, are characterized by high pressures, low temperatures, and absence of sunlight. These features make up the majority of the deepest marine habitat—the hadal zone—home to distinct communities from those in the surrounding abyssal plains. The snailfishes, family Liparidae (Scorpaeniformes), have found notable success in the hadal zone from ∼6000 to 8200 m, comprising the dominant ichthyofauna in at least six trenches worldwide. The hadal fish community is distinct from the abyssal community where elongate, scavenging fishes such as rattails (Macrouridae), cutthroat eels (Synaphobranchidae), tripodfishes (Ipnopidae), eelpouts (Zoarcidae), and cusk eels (Ophidiidae) are most common. Until recently, little was known about the biology of these deepest-living fishes, or the factors that drive their success at hadal depths. Here, I review recent investigations spanning the abyssal–hadal boundary and discuss the factors structuring these communities, including the roles of pressure adaptation, feeding ecology, and life history. Hadal fishes show specialized adaptation to hydrostatic pressure both in accumulation of the pressure-counteractant trimethylamine n-oxide and in intrinsic changes to enzymes. Stomach content and amino acid isotope analyses, and jaw morphology suggest that suction-feeding predatory fishes like hadal liparids may find an advantage to descending into the trench where amphipods are increasingly abundant. Analysis of otolith growth zones suggest that snailfishes may be adapted to a seismically active, high-disturbance hadal environment by having relatively short life-spans. This review synthesizes the known literature on the planet’s deepest-living fishes and informs new understanding of adaptations to life in the trenches.

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.

A full-ocean-depth rated modular lander and pressure-retaining sampler capable of collecting hadal-endemic microbes under in situ conditions

The hadal zone remains one of the least studied environments because of its inaccessibility, in part because of hydrostatic pressures extending to 110 MPa. Few instruments are capable of sampling from such great depths. We have developed a full-ocean-depth-capable lander that can be fit with sampling packages for the collection of still images, video, motile megafauna, and hadal seawater. One payload includes a pressure-retaining sampler (PRS) able to maintain seawater samples under in situ pressure during recovery. We describe the technical specifications of the lander and the PRS and preliminary results from three deployments at depths in excess of 10,700 m in the Mariana Trench. Seawater from full-ocean depth was recovered at 81% of the in situ pressure. This facilitated the collection of microbial genomes affiliated with the family Flavobacteriaceae within the Bacteroidetes and the phylum Marinimicrobia. We show that these microbes are specifically enriched in hadal zones, representing novel trench lineages, and describe their adaptations for living in hadal environments. These findings highlight the utility of this lander system, which facilitates scientific inquiry at depths greater than 6000 m.

Metagenomics Reveals Microbial Diversity and Metabolic Potentials of Seawater and Surface Sediment From a Hadal Biosphere at the Yap Trench.

Hadal biosphere represents the deepest part of the ocean with water depth >6,000 m. Accumulating evidence suggests the existence of unique microbial communities dominated by heterotrophic processes in this environment. However, investigations of the microbial diversity and their metabolic potentials are limited because of technical constraints for sample collection. Here, we provide a detailed metagenomic analysis of three seawater samples at water depths 5,000–6,000 m below sea level (mbsl) and three surface sediment samples at water depths 4,435–6,578 mbsl at the Yap Trench of the western Pacific. Distinct microbial community compositions were observed with the dominance of Gammaproteobacteria in seawater and Thaumarchaeota in surface sediment. Comparative analysis of the genes involved in carbon, nitrogen and sulfur metabolisms revealed that heterotrophic processes (i.e., degradation of carbohydrates, hydrocarbons, and aromatics) are the most common microbial metabolisms in the seawater, while chemolithoautotrophic metabolisms such as ammonia oxidation with the HP/HB cycle for CO2 fixation probably dominated the surface sediment communities of the Yap Trench. Furthermore, abundant genes involved in stress response and metal resistance were both detected in the seawater and sediments, thus the enrichment of metal resistance genes is further hypothesized to be characteristic of the hadal microbial communities. Overall, this study sheds light on the metabolic versatility of microorganisms in the Yap Trench, their roles in carbon, nitrogen, and sulfur biogeochemical cycles, and how they have adapted to this unique hadal environment.

Insight Into the Pico- and Nano-Phytoplankton Communities in the Deepest Biosphere, the Mariana Trench.

As photoautotrophs, phytoplankton are generally present in the euphotic zone of the ocean, however, recently healthy phytoplankton cells were found to be also ubiquitous in the dark deep sea, i.e., at water depths between 2000 and 4000 m. The distributions of phytoplankton communities in much deeper waters, such as the hadal zone, are unclear. In this study, the vertical distribution of the pico- and nano-phytoplankton (PN) communities from the surface to 8320 m, including the epipelagic, mesopelagic, bathypelagic, and hadal zones, were investigated via both 18S and p23S rRNA gene analysis in the Challenger Deep of the Mariana Trench. The results showed that Dinoflagellata, Chrysophyceae, Haptophyta, Chlorophyta, Prochloraceae, Pseudanabaenaceae, Synechococcaceae, and Eustigmatophyceae, etc., were the predominant PN in the Mariana Trench. Redundancy analyses revealed that depth, followed by temperature, was the most important environmental factors correlated with vertical distribution of PN community. In the hadal zone, the PN community structure was considerably different from those in the shallower zones. Some PN communities, e.g., Eustigmatophyceae and Chrysophyceae, which have the heterotrophic characteristics, were sparse in shallower waters, while they were identified with high relative abundance (94.1% and 20.1%, respectively) at the depth of 8320 m. However, the dinoflagellates and Prochloraceae Prochlorococcus were detected throughout the entire water column. We proposed that vertical sinking, heterotrophic metabolism, and/or the transition to resting stage of phytoplankton might contribute to the presence of phytoplankton in the hadal zone. This study provided insight into the PN community in the Mariana Trench, implied the significance of phytoplankton in exporting organic matters from the euphotic to the hadal zone, and also hinted the possible existence of some undetermined energy metabolism (e.g., heterotrophy) of phytoplankton making themselves adapt and survive in the hadal environment.

Deep-sea spoon worms (Echiura) from the Sea of Okhotsk and the adjacent slope of the Kuril-Kamchatka Trench

During the SokhoBio (Sea of Okhotsk Biodiversity Studies) expedition from July to August 2015, eleven sites across the Kuril Basin of the Sea of Okhotsk and the landward abyssal slope of the Kuril-Kamchatka Trench (KKT) off the Bussol Strait were surveyed and benthic communities were investigated. Samples comprised 260 echiurans from seven species of seven genera belonging to the family Bonelliidae, were collected at eight of the eleven sites of the SokhoBio expedition. The family Bonelliidae is most common in abyssal and hadal environments in the world ocean with high abundances in all investigated regions. The description of deep-water echiurans from the Sea of Okhotsk is the first one based on complete collected specimens with living colouration. The descriptions provide new information on the morphology and taxonomic details of the species, which were previously noted from the northwestern Pacific and described from damaged or incomplete specimens. Two species are identified as representatives of the two genera, Bengalus and Bonelliopsis, which never have been noted before in the northwestern Pacific and the genus Bengalus is reported for the first time in the Pacific. The knowledge of the geographic ranges of these genera are expanded and discussed.

Tectonically-triggered sediment and carbon export to the Hadal zone

Sediments in deep ocean trenches may contain crucial information on past earthquake history and constitute important sites of carbon burial. Here we present 14C data on bulk organic carbon (OC) and its thermal decomposition fractions produced by ramped pyrolysis/oxidation for a core retrieved from the >7.5 km-deep Japan Trench. High-resolution 14C measurements, coupled with distinctive thermogram characteristics of OC, reveal hemipelagic sedimentation interrupted by episodic deposition of pre-aged OC in the trench. Low δ13C values and diverse 14C ages of thermal fractions imply that the latter material originates from the adjacent margin, and the co-occurrence of pre-aged OC with intervals corresponding to known earthquake events implies tectonically triggered, gravity-flow-driven supply. We show that 14C ages of thermal fractions can yield valuable chronological constraints on sedimentary sequences. Our findings shed new light on links between tectonically driven sedimentological processes and marine carbon cycling, with implications for carbon dynamics in hadal environments.

Life history of abyssal and hadal fishes from otolith growth zones and oxygen isotopic compositions

Hadal trenches are isolated habitats that cover the greatest ocean depths (6,500–11,000m) and are believed to host high levels of endemism across multiple taxa. A group of apparent hadal endemics is within the snailfishes (Liparidae), found in at least five geographically separated trenches. Little is known about their biology, let alone the reasons for their success at hadal depths around the world. This study investigated the life history of hadal liparids using sagittal otoliths of two species from the Kermadec (Notoliparis kermadecensis) and Mariana (Pseudoliparis swirei) trenches in comparison to successful abyssal macrourids found at the abyssal-hadal transition zone. Otoliths for each species revealed alternating opaque and translucent growth zones that could be quantified in medial sections. Assuming these annuli represent annual growth, ages were estimated for the two hadal liparid species to be from five to 16 years old. These estimates were compared to the shallower-living snailfish Careproctus melanurus, which were older than described in previous studies, expanding the potential maximum age for the liparid family to near 25 years. Age estimates for abyssal macrourids ranged from eight to 29 years for Coryphaenoides armatus and six to 16 years for C. yaquinae. In addition, 18O/16O ratios (δ18O) were measured across the otolith using secondary ion mass spectrometry (SIMS) to investigate the thermal history of the three liparids, and two macrourids. Changes in δ18O values were observed across the otoliths of C. melanurus, C. armatus, and both hadal liparids, the latter of which may represent a change of >5°C in habitat temperature through ontogeny. The results would indicate there is a pelagic larval stage for the hadal liparids that rises to a depth above 1000m, followed by a return to the hadal environment as these liparids grow. This result was unexpected for the hadal liparids given their isolated environment and large eggs, and the biological implications and plausibility of interpretations of these data are discussed. This study presents a first look at the life history of some of the deepest-living fishes through otolith analyses.

The metabolic potential of the single cell genomes obtained from the Challenger Deep, Mariana Trench within the candidate superphylum Parcubacteria (OD1).

Candidate phyla (CP) are broad phylogenetic clusters of organisms that lack cultured representatives. Included in this fraction is the candidate Parcubacteria superphylum. Specific characteristics that have been ascribed to the Parcubacteria include reduced genome size, limited metabolic potential and exclusive reliance on fermentation for energy acquisition. The study of new environmental niches, such as the marine versus terrestrial subsurface, often expands the understanding of the genetic potential of taxonomic groups. For this reason, we analyzed 12 Parcubacteria single amplified genomes (SAGs) from sediment samples collected within the Challenger Deep of the Mariana Trench, obtained during the Deepsea Challenge (DSC) Expedition. Many of these SAGs are closely related to environmental sequences obtained from deep-sea environments based on 16S rRNA gene similarity and BLAST matches to predicted proteins. DSC SAGs encode features not previously identified in Parcubacteria obtained from other habitats. These include adaptation to oxidative stress, polysaccharide modification and genes associated with respiratory nitrate reduction. The DSC SAGs are also distinguished by relative greater abundance of genes for nucleotide and amino acid biosynthesis, repair of alkylated DNA and the synthesis of mechanosensitive ion channels. These results present an expanded view of the Parcubacteria, among members residing in an ultra-deep hadal environment.

Molecular adaptation in the world's deepest-living animal: Insights from transcriptome sequencing of the hadal amphipod Hirondellea gigas.

The Challenger Deep in the Mariana Trench is the deepest point in the oceans of our planet. Understanding how animals adapt to this harsh environment characterized by high hydrostatic pressure, food limitation, dark and cold is of great scientific interest. Of the animals dwelling in the Challenger Deep, amphipods have been captured using baited traps. In this study, we sequenced the transcriptome of the amphipod Hirondellea gigas collected at a depth of 10,929m from the East Pond of the Challenger Deep. Assembly of these sequences resulted in 133,041 contigs and 22,046 translated proteins. Functional annotation of these contigs was made using the go and kegg databases. Comparison of these translated proteins with those of four shallow-water amphipods revealed 10,731 gene families, of which 5659 were single-copy orthologs. Base substitution analysis on these single-copy orthologs showed that 62 genes are positively selected in H.gigas, including genes related to β-alanine biosynthesis, energy metabolism and genetic information processing. For multiple-copy orthologous genes, gene family expansion analysis revealed that cold-inducible proteins (i.e., transcription factors II A and transcription elongation factor 1) as well as zinc finger domains are expanded in H.gigas. Overall, our results indicate that genetic adaptation to the hadal environment by H.gigas may be mediated by both gene family expansion and amino acid substitutions of specific proteins.

Identification of Free-Living and Particle-Associated Microbial Communities Present in Hadal Regions of the Mariana Trench.

Relatively few studies have described the microbial populations present in ultra-deep hadal environments, largely as a result of difficulties associated with sampling. Here we report Illumina-tag V6 16S rRNA sequence-based analyses of the free-living and particle-associated microbial communities recovered from locations within two of the deepest hadal sites on Earth, the Challenger Deep (10,918 meters below surface-mbs) and the Sirena Deep (10,667 mbs) within the Mariana Trench, as well as one control site (Ulithi Atoll, 761 mbs). Seawater samples were collected using an autonomous lander positioned ~1 m above the seafloor. The bacterial populations within the Mariana Trench bottom water samples were dissimilar to other deep-sea microbial communities, though with overlap with those of diffuse flow hydrothermal vents and deep-subsurface locations. Distinct particle-associated and free-living bacterial communities were found to exist. The hadal bacterial populations were also markedly different from one another, indicating the likelihood of different chemical conditions at the two sites. In contrast to the bacteria, the hadal archaeal communities were more similar to other less deep datasets and to each other due to an abundance of cosmopolitan deep-sea taxa. The hadal communities were enriched in 34 bacterial and 4 archaeal operational taxonomic units (OTUs) including members of the Gammaproteobacteria, Epsilonproteobacteria, Marinimicrobia, Cyanobacteria, Deltaproteobacteria, Gemmatimonadetes, Atribacteria, Spirochaetes, and Euryarchaeota. Sequences matching cultivated piezophiles were notably enriched in the Challenger Deep, especially within the particle-associated fraction, and were found in higher abundances than in other hadal studies, where they were either far less prevalent or missing. Our results indicate the importance of heterotrophy, sulfur-cycling, and methane and hydrogen utilization within the bottom waters of the deeper regions of the Mariana Trench, and highlight novel community features of these extreme habitats.

Single cells within the Puerto Rico trench suggest hadal adaptation of microbial lineages.

Hadal ecosystems are found at a depth of 6,000 m below sea level and below, occupying less than 1% of the total area of the ocean. The microbial communities and metabolic potential in these ecosystems are largely uncharacterized. Here, we present four single amplified genomes (SAGs) obtained from 8,219 m below the sea surface within the hadal ecosystem of the Puerto Rico Trench (PRT). These SAGs are derived from members of deep-sea clades, including the Thaumarchaeota and SAR11 clade, and two are related to previously isolated piezophilic (high-pressure-adapted) microorganisms. In order to identify genes that might play a role in adaptation to deep-sea environments, comparative analyses were performed with genomes from closely related shallow-water microbes. The archaeal SAG possesses genes associated with mixotrophy, including lipoylation and the glycine cleavage pathway. The SAR11 SAG encodes glycolytic enzymes previously reported to be missing from this abundant and cosmopolitan group. The other SAGs, which are related to piezophilic isolates, possess genes that may supplement energy demands through the oxidation of hydrogen or the reduction of nitrous oxide. We found evidence for potential trench-specific gene distributions, as several SAG genes were observed only in a PRT metagenome and not in shallower deep-sea metagenomes. These results illustrate new ecotype features that might perform important roles in the adaptation of microorganisms to life in hadal environments.