Genome of a giant isopod, Bathynomus jamesi, provides insights into body size evolution and adaptation to deep-sea environment

Abstract

Background The deep-sea may be regarded as a hostile living environment, due to low temperature, high hydrostatic pressure, and limited food and light. Isopods, a species-rich group of crustaceans, are widely distributed across different environments including the deep sea and as such are a useful model for studying adaptation, migration, and speciation. Similar to other deep-sea organisms, giant isopods have larger body size than their shallow water relatives and have large stomachs and fat bodies presumably to store organic reserves. In order to shed light on the genetic basis of these large crustaceans adapting to the oligotrophic environment of deep-sea, the high-quality genome of a deep-sea giant isopod Bathynomus jamesi was sequenced and assembled. Results B. jamesi has a large genome of 5.89 Gb, representing the largest sequenced crustacean genome to date. Its large genome size is mainly attributable to the remarkable proliferation of transposable elements (84%), which may enable high genome plasticity for adaptive evolution. Unlike its relatives with small body size, B. jamesi has expanded gene families related to pathways of thyroid and insulin hormone signaling that potentially contribute to its large body size. Transcriptomic analysis showed that some expanded gene families related to glycolysis and vesicular transport were specifically expressed in its digestive organs. In addition, comparative genomics and gene expression analyses in six tissues suggested that B. jamesi has inefficient lipid degradation, low basal metabolic rate, and bulk food storage, suggesting giant isopods adopt a more efficient mechanism of nutrient absorption, storage, and utilization to provide sustained energy supply for their large body size. Conclusions Taken together, the giant isopod genome may provide a valuable resource for understanding body size evolution and adaptation mechanisms of macrobenthic organisms to deep-sea environments.

Recent advances in crustacean genomics and their potential application in aquaculture

“…Additionally, the genome of a deep-sea isopod has been published recently. 30 The five amphipods with published genomes mainly include sand-hoppers and some epibenthic organisms, and all five genomes were assembled based on Illumina data with short contigs (Table 1).…”

“…39 The large genome sizes of Amphipoda and Isopoda are also correlated with their size gigantism. 30,42 Among the members of the order Decapoda, the genomes of the members of the Penaeidae (average 2.64 pg) and Ocypodidae (average 2.52 pg) families are smaller than those of other decapods. The genome size of decapods is also believed to be negatively correlated with the number of larval stages.…”

“…Their genome expansion has been suggested to be the result of repeated proliferation rather than WGD. 30,31,[54][55][56] Even in closely related species, such as those in the genus Armadillidium, the recent proliferation of TEs can also lead to an increase in genome size. 57 As expected, branchiopods and copepods generally have smaller genomes and lower levels of TEs, whereas some isopods (e.g., B. jamesi) and decapods (e.g., P. platypus, P. carinicauda and Synalpheus snapping shrimp) have larger genomes and higher levels of TEs (Table 3).…”

Transposable element expansion and low-level piRNA silencing in grasshoppers may cause genome gigantism

“…Large amounts of DNA insertion or deletion would result in a high genome plasticity [106]. Research has shown that the proliferation of DNA transposons and LINEs in deep-sea species might play an important role in shaping highly plastic genomes and helping them adapt to the deep-sea environment [8]. We speculate that the expansion of TEs in the giant genome grasshopper species might help them better adapt to the living environment, because the A. rhodopa species was collected at higher altitude areas (average altitude of 3000 m).…”

“…Perplexingly, the large variation in genome size occurs between morphologically similar species, and gigantic genomes emerge in relatively simple organisms [3]. In the tree of life, species with gigantic genomes (larger than 10 GB) only account for a tiny fraction, including lungfishes [4], salamanders [5,6], deep-sea crustaceans [7,8], and orthoptera insects [9,10]. The evolutionary mechanism of gigantic genomes has always been a mystery that researchers are eager to unravel.…”