The Adaptive Evolution and Gigantism Mechanisms of the Hadal “Supergiant” Amphipod Alicella gigantea

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.

Morphological and molecular evolution of hadal amphipod’s eggs provides insights into embryogenesis under high hydrostatic pressure

“…Evolutionary adaptation of adult organisms dwelling in deep-sea environments and hadal zones has been extensively studied in various species, including teleosts ( Lan et al, 2018 ; Wang et al, 2019 ), bivalve molluscs ( Sun et al, 2017 ), and amphipods ( Lan et al, 2017 ; Li et al, 2021 ), but rarely in embryos because of the lack of accessibility ( Grassle & Sanders, 1973 ; Perrone et al, 2002 ; Blankenship-Williams & Levin, 2009 ; Ritchie et al, 2017 ). Sampling of gestational amphipods in hadal zones is especially difficult because of limited responses to bait traps and avoided cannibalism, defined as interspecific predation ( Fox 1975 ; Perrone et al, 2002 ; Blankenship-Williams & Levin, 2009 ).…”

“…By comparing the results of the eggs with the adults transcriptome analysis ( Li et al, 2021 ), we found the PSGs obtained from the eggs and the adults were both involved in “cell cycle regulation”. However, in the adults whole body, PSGs were closely related to meiotic or mitotic process, such as “meiotic cell cycle”, “female meiotic nuclear division”, “spindle pole”, “mitotic prometaphase” and “condensed chromosome” ( Li et al, 2021 ). Meiosis is a special type of cell division for gametogenesis in gonad.…”

“…During an expedition of the New Britain Trench (8,824 m, 7.02◦S, 149.16◦E) in the West Pacific Ocean conducted in 2016, our group collected 10 A. gigantea individuals with attached eggs with a full ocean depth lander vehicle launched from the “Zhang Jian” research vessel that were immediately stored at −80 °C immediately. Detailed information about the lander vehicle and sampling process is described by Chan et al (2020 ; 2022 ; 2021) and Li et al (2021) . The specimens were stored in bubble chamber full of dry ice and delivered to Shanghai Ocean University.…”

“…Numerous studies of this “supergiant” amphipod have been conducted, including a mitochondrial genome study of the phylogeny and adaptation mechanisms ( Li et al, 2019 ) and a trace element studies suggested the use of amphipods as potential indicators of trace element bioavailability in hadal zones ( Zhu et al, 2022 ). Transcriptome and evolutionary analyses conducted by Li et al (2021) identified seven positively selected genes (PSGs) of the “supergiant” A . gigantea involved in inositol phosphate metabolism, insulin signaling, and glycogenesis signaling, which are ultimately related to growth and proliferation.…”

“…Numerous studies of this "supergiant" amphipod have been conducted, including a mitochondrial genome study of the phylogeny and adaptation mechanisms (Li et al, 2019) and a trace element studies suggested the use of amphipods as potential indicators of trace element bioavailability in hadal zones (Zhu et al, 2022). Transcriptome and evolutionary analyses conducted by Li et al (2021) identified seven positively selected genes (PSGs) of the "supergiant" A. gigantea involved in inositol phosphate metabolism, insulin signaling, and glycogenesis signaling, which are ultimately related to growth and proliferation. However, the disjunctive geographical distribution (Jamieson et al, 2013;Ritchie et al, 2015), low observation frequency (Jamieson et al, 2013), and limited genomic resources have hindered elucidation of the adaptation of embryos to the environmental extremes of hadal zones (Jamieson et al, 2013).…”