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

Abstract

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 10,929 m 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.

Morphology and genome of a snailfish from the Mariana Trench provide insights into deep-sea adaptation

“…8), most of which were Hirondellea gigas. The dominance of H. gigas is consistent with an earlier report 10 .…”

Comparative transcriptomic analysis of deep- and shallow-water barnacle species (Cirripedia, Poecilasmatidae) provides insights into deep-sea adaptation of sessile crustaceans

“…Many potential mechanisms of adaptation to deep-sea environments have been identified. Lan et al suggested that the expansion of cold-inducible proteins as well as zinc finger domains and positively selected genes related to βalanine biosynthesis, energy metabolism and genetic information processing played important roles in adaptation to the hadal environment in the amphipod Hirondellea gigas [6]. Zhang et al reported that the expression of the genes associated with sulfur metabolism and detoxification were upregulated in a deep-sea hydrothermal vent shrimp Rimicaris sp.…”

“…Compared with shallow waters, food availability is limited in the deep-sea, which may have encouraged evolution of more efficient energy metabolism [6,7]. Among the orthologous genes of the two barnacle species, those related to carbohydrate metabolism showed relatively higher expression in G. gigas than in O. warwicki, including the genes from the pathways of galactose metabolism, glycosphingolipid biosynthesis, and glycosaminoglycan biosynthesis ( Fig.…”

“…Conditions on the deep-sea floor are poorly known but generally are considered too harsh for the survival of most organisms, e.g., high hydrostatic pressure, darkness, hypoxia, low temperature, and limited food availability [1][2][3][4][5]. However, a macrofauna consisting of a growing range of newly discovered animals adapted to deep-sea habitats has been reported, including crustaceans [6][7][8], polychaetes [9,10], fishes [11,12], and mollusks [13,14]. Various mechanisms have adapted them for survival in deep-sea environments: e.g., squat lobsters and mussels have developed chemoautotrophic systems of symbiotic bacteria for inhabiting hydrothermal vents and cold seeps in the seafloor [15][16][17]; and snailfish have evolved special morphological and physiological characters to survive and thrive in the hadal zone [12].…”

“…Studies aimed at understanding survival strategies and adaptive evolution of organisms living in deep seas have also employed genomic or transcriptomic sequencing. For example, in the amphipod Hirondellea gigas, adaptation to the hadal environment is associated with gene family expansion and amino acid substitutions of specific proteins [6]; and the shrimp Rimicaris sp. upregulates genes associated with sulfur metabolism and detoxification to survive in deep-sea hydrothermal vent environments [8].…”