Hadal Amphipods Research Articles

Diet change of hadal amphipods revealed by fatty acid profile: A close relationship with surface ocean

The diet of hadal organisms remains elusive because of the difficulty in sampling and monitoring at the great water depths (6–11 km). Here we analyzed fatty acids of the amphipods collected from three Pacific trenches, namely New Britain Trench (NBT; 8.2–8.9 km), Mariana Trench (MT; 11 km) and Massau Trench (MS; 6.9 km). A total of 35 fatty acids including saturated, monounsaturated and polyunsaturated compounds were identified. The principal component analysis (PCA) divides major fatty acids into three groups indicative of carrion (C20:4ω6, C22:5ω6, C22:6ω3, C16:1ω7, and C18:1ω9), algae (C18:2ω6 and C20:5ω3) and bacteria (C15:0, isoC15:0, isoC17:0, anteisoC17:0 and C17:0), respectively. The predominance of C18:1ω9, high C18:1ω9/C18:1ω7 and high δ15N values suggest that hadal amphipods are necrophagous. The inter-trench comparisons based on C18:1ω9/C18:1ω7, C22:6ω3/C20:5ω3, ∑polyunsaturated/∑saturated fatty acids, ∑branched fatty acids and PCA show that the amphipods in the NBT are more dependent on high-quality organic matter (i.e., carrion), whereas those in the MT and MS utilize detritus and bacterial organic matter as supplementary food. This inter-trench difference has been attributed to a bottom-up effect of food availability that the NBT has higher net primary productivity (NPP) and a strong terrestrial influence, whereas the MT and MS have lower NPP and insignificant terrestrial influences. Our study demonstrates that the diet of hadal animals is closely related to surface ocean biogeochemical property.

Organic osmolytes of amphipods from littoral to hadal zones: Increases with depth in trimethylamine N-oxide, scyllo-inositol and other potential pressure counteractants

Deep-sea organisms must cope with hydrostatic pressure, up to ~ 110 MPa (~ 1100 atm) at 11 km in the Mariana Trench. Pressure perturbs protein conformations, ligand binding, and can promote damaging protein aggregates. Salinity is another stressor: seawater, averaging ~ 1000 mOsm/kg, is dehydrating towards the ~ 250–400 mOsm/kg of universal cellular solutes. Most marine organisms prevent dehydration by becoming isosmotic with cellular organic osmolytes, which, unlike NaCl, do not perturb proteins and can have chemical chaperone properties, stabilizing proteins against various physicochemical stressors. In shallow-dwelling invertebrates, these osmolytes are typically taurine, glycine, and betaine. Previous work on crustaceans down to 3 km found that “shallow” osmolytes decreased with depth, replaced with trimethylamine N-oxide (TMAO) and other apparent chemical chaperones. In bony fishes, TMAO increases with depth down to 8 km, and is probably a piezolyte (pressure counteractant) as it reverses pressure's inhibitory effects. Here we analyzed amphipods over the full ocean depth range of 0–11 km, from coastal habitats and numerous depths in the Kermadec and Mariana Trenches. We found that “shallow” osmolytes decreased while potential piezolytes, in different combinations in different species, increased with depth. These are TMAO, glycerophosphorylcholine and proline betaine (all methylamine chaperones), glycerophosphorylethanolamine, and scyllo-inositol, a polyol chaperone (being tested for Alzheimer's Disease) that works differently than methylamines by preventing damaging protein aggregations. Though only TMAO has been tested for piezolyte properties, these other solutes may explain how some hadal amphipods live deeper than fish, which appear to be limited to a maximum of 8.4 km.

Heat-shock protein adaptation in abyssal and hadal amphipods

Heat-shock proteins (HSPs) are a prominent family of cellular chaperones that are involved in the folding, assembly and degradation of cellular proteins, cell-cycling and signal transduction. HSPs are high conserved across taxa and form a key component of the stress response with signatures of molecular adaptation in some species exposed to extreme environmental stressors such as dehydration, heavy metal pollutants and arctic temperatures. Here we characterise two key heat-shock protein genes (hsp70 and hsp90) in deep-sea Lysianassoidea amphipods, with a focus on copy number variation and signatures of selection on the DNA sequences. Four phylogenetically distinct isoforms were resolved for both hsp70 and hsp90, with one isoform in each gene being exclusive to the hadal genus Hirondellea. Signatures of purifying selection were shown across hsp70 and hsp90 from dN:dS ratios. The GC content of each gene was lower, and the number of codons used was higher, than in shallow water amphipods suggesting a relaxation in codon usage bias. Such observations suggest that increased hydrostatic pressure is an important environmental stress that shapes the adaptation of heat-shock protein genes in deep-sea amphipods.

Genome Reduction in Psychromonas Species within the Gut of an Amphipod from the Ocean's Deepest Point.

Amphipods are the dominant scavenging metazoan species in the Mariana Trench, the deepest known point in Earth's oceans. Here the gut microbiota of the amphipod Hirondellea gigas collected from the Challenger and Sirena Deeps of the Mariana Trench were investigated. The 11 amphipod individuals included for analyses were dominated by Psychromonas, of which a nearly complete genome was successfully recovered (designated CDP1). Compared with previously reported free-living Psychromonas strains, CDP1 has a highly reduced genome. Genome alignment showed deletion of the trimethylamine N-oxide (TMAO) reducing gene cluster in CDP1, suggesting that the "piezolyte" function of TMAO is more important than its function in respiration, which may lead to TMAO accumulation. In terms of nutrient utilization, the bacterium retains its central carbohydrate metabolism but lacks most of the extended carbohydrate utilization pathways, suggesting the confinement of Psychromonas to the host gut and sequestration from more variable environmental conditions. Moreover, CDP1 contains a complete formate hydrogenlyase complex, which might be involved in energy production. The genomic analyses imply that CDP1 may have developed adaptive strategies for a lifestyle within the gut of the hadal amphipod H.gigas. IMPORTANCE As a unique but poorly investigated habitat within marine ecosystems, hadal trenches have received interest in recent years. This study explores the gut microbial composition and function in hadal amphipods, which are among the dominant carrion feeders in hadal habitats. Further analyses of a dominant strain revealed genomic features that may contribute to its adaptation to the amphipod gut environment. Our findings provide new insights into animal-associated bacteria in the hadal biosphere.

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.

Population structure of the hadal amphipod Bathycallisoma (Scopelocheirus) schellenbergi in the Kermadec Trench and New Hebrides Trench, SW Pacific

Deep-sea animals inhabiting the hadal zone (>6000m deep) are frequently reported to occupy large bathymetric ranges, but details of intra-specific population structure and the underlying drivers remain poorly understood. Here we describe the population structure of the dominant SW Pacific hadal amphipod, Bathycallisoma schellenbergi, across its bathymetric range in the Kermadec (10,047m) and New Hebrides (7156m) trenches and explore the factors likely responsible for the observed patterns. These two trenches are relatively close geographically but underlie different water masses and are topographically isolated by the Kermadec fore-arc. The minimum depth of B. schellenbergi was ~1000m shallower in the New Hebrides Trench than in the Kermadec Trench although similar patterns of ontogenetic stratification were present; juveniles were restricted to depths <~7000m, larger adults were deeper toward the trench axes, regardless of absolute depth. We suggest that the increased juvenile presence around the abyssal-hadal transition zone is driven by reduced competition and a relaxation of pressure effects on metabolism. Evidence is also presented for morphological heterogeneity indicating geographic isolation between the two trenches. Interestingly, the absence of another major scavenging amphipod, Hirondellea dubia, at mid-trench depths corresponded to maximum densities of B. schellenbergi, a trend that was reversed towards the trench axes regardless of actual depth. This suggests that the population structure and amphipod assemblages are more affected by how trench topography influences the distribution of food and potential ecological interactions, rather than simply by the effects of hydrostatic pressure.

Phylogenetic relationships among hadal amphipods of the Superfamily Lysianassoidea: Implications for taxonomy and biogeography

Amphipods of the superfamily Lysianassoidea are ubiquitous at hadal depths (>6000m) and therefore are an ideal model group for investigating levels of endemism and the drivers of speciation in deep ocean trenches. The taxonomic classification of hadal amphipods is typically based on conventional morphological traits but it has been suggested that convergent evolution, phenotypic plasticity, intra-specific variability and ontogenetic variation may obscure the ability to robustly diagnose taxa and define species. Here we use phylogenetic analysis of DNA sequence variation at two mitochondrial (COI and 16S rDNA) and one nuclear (18S rDNA) regions at to examine the evolutionary relationships among 25 putative amphipod species representing 14 genera and 11 families that were sampled from across seven hadal trenches. We identify several instances where species, genera and families do not resolve monophyletic clades, highlighting incongruence between the current taxonomic classification and the molecular phylogeny for this group. Our data also help extend and resolve the known biogeographic distributions for the different species, such as identifying the co-occurrence of Hirondellea dubia and Hirondellea gigas in the Mariana trench.

Bait-attending fauna of the Kermadec Trench, SW Pacific Ocean: Evidence for an ecotone across the abyssal–hadal transition zone

The bait-attending fauna of the abyssal–hadal transition zone of the Kermadec Trench, SW Pacific Ocean (4329–7966 m), was investigated using a baited camera and a trap lander. The abyssal stations (4329–6007 m) revealed a typical scavenging fish community comprising macrourids and synaphobranchid eels, as well as natantian decapods. At the hadal depths of 7199 and 7561 m, the endemic liparid Notoliparis kermadecensis was observed aggregating at the bait reaching surprisingly high numbers of 5 and 13, respectively. A total of 3183 invertebrate samples were collected (mean deployment time=16 h) of which 97.8% were of the order Amphipoda (nine families, 16 species). Ten of the amphipod species represent new distributional records for the Kermadec Trench and the New Zealand Exclusive Economic Zone; this includes the shallowest known record of the endemic hadal amphipod Hirondellea dubia (6000, 6007 m). Using amphipods to statistically examine the compositional change across the abyssal–hadal boundary, an ecotone between depths <6007 and >6890 m was found, indicating that there is an ecologically distinct bait-attending fauna in this trench.

Biochemical composition and trophic strategies of the amphipod Eurythenes gryllus at hadal depths (Atacama Trench, South Pacific)

Amphipods Eurythenes gryllus were collected at 7800 m depth in the Atacama Trench (South Pacific) for studying their biochemical composition (in terms of proteins, lipids and carbohydrates and fatty acid content) and to gather information on bioenergetic strategies and trophic habits of organisms living in this extreme environment. The effect of long-term formalin storage on the biochemical determinations was also determined. Proteins were the dominant biochemical class of organic compounds (39–53%D.W.), whereas carbohydrates accounted for a very small fraction (1–2%D.W.). Lipid concentrations of E. gryllus accounted for 7–18%D.W. and were much lower than those reported for other deep-sea amphipods. These differences are likely to be more dependent upon food availability in the Atacama Trench rather than upon temperature. Lipid composition of E. gryllus revealed the dominance of monounsaturated fatty acids with polyunsaturated fatty acids accounting for a very small fraction, suggesting that hadal amphipods are higher dependent upon lipid reserves than amphipods inhabiting at shallow depths. The ratio of C18:1Δ9 to C18:1Δ11 was >11 confirming the necrophagous trophic habits of this hadal amphipod.

Geographic variation among three isolated populations of the hadal amphipod Hirondellea gigas (Crustacea: Amphipoda: Lysianassoidea)

Geographic variation among three isolated populations of the hadal amphipod Hirondellea gigas (Crustacea: Amphipoda: Lysianassoidea)