Abstract

Hadal trenches are commonly referred to as the deepest areas in the ocean and are characterized by extreme environmental conditions such as high hydrostatic pressures and very limited food supplies. Amphipods are considered the dominant scavengers in the hadal food web. Alicella gigantea is the largest hadal amphipod and, as such, has attracted a lot of attention. However, the adaptive evolution and gigantism mechanisms of the hadal “supergiant” remain unknown. In this study, the whole-body transcriptome analysis was conducted regarding the two hadal amphipods, one being the largest sized species A. gigantea from the New Britain Trench and another the small-sized species Bathycallisoma schellenbergi from the Marceau Trench. The size and weight measurement of the two hadal amphipods revealed that the growth of A. gigantea was comparatively much faster than that of B. schellenbergi. Phylogenetic analyses showed that A. gigantea and B. schellenbergi were clustered into a Lysianassoidea clade, and were distinct from the Gammaroidea consisting of shallow-water Gammarus species. Codon substitution analyses revealed that “response to starvation,” “glycerolipid metabolism,” and “meiosis” pathways were enriched among the positively selected genes (PSGs) of the two hadal amphipods, suggesting that hadal amphipods are subjected to intense food shortage and the pathways are the main adaptation strategies to survive in the hadal environment. To elucidate the mechanisms underlying the gigantism of A. gigantea, small-sized amphipods were used as the background for evolutionary analysis, we found the seven PSGs that were ultimately related to growth and proliferation. In addition, the evolutionary rate of the gene ontology (GO) term “growth regulation” was significantly higher in A. gigantea than in small-sized amphipods. By combining, those points might be the possible gigantism mechanisms of the hadal “supergiant” A. gigantea.

Highlights

  • Hadal, the deepest area of the ocean (6,000–11,000 m), is a unique harsh environment characterized by extremely high hydrostatic pressures, low temperature, and limited food sources (Somero, 1992; Jamieson et al, 2010)

  • 2.56E-02 2.81E-02 7.42E-03 5.38E-03 4.31E-03. Among these 14 critically positively selected genes (PSGs) (FDR

  • We found that a gene-encoding rate-limiting enzyme, inosine-5′monophosphate dehydrogenase 1 (IMPDH1) (Figure 5A and Table 2), which was involved in the de novo synthesis of guanine nucleotides and acts as a homotetramer to regulate cell growth (Slee and Bownes, 1995; Hossain et al, 2016), was under positive selection in A. gigantea (Figure 5A and Table 2)

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Summary

Introduction

The deepest area of the ocean (6,000–11,000 m), is a unique harsh environment characterized by extremely high hydrostatic pressures, low temperature, and limited food sources (Somero, 1992; Jamieson et al, 2010). With increasing sampling efforts regarding the hadal trenches, a wide range of organisms was found to thrive within the extreme environment (Nunoura et al, 2015; Tarn et al, 2016). How those hadal creatures adapted to the extreme environment is a topic of great interest to researchers. Hadal creatures were found to own some external types of “assistance” to improve protein stability and functional adaptability under high hydrostatic pressures. The types of “assistance” include stress proteins, phospholipids, and micromolecular counteractants, for example, trimethylamine N-oxide (TMAO), which was reported to be of great significance for the adaptation of hadal species (Yancey, 2020)

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