Giant African snail genomes provide insights into molluscan whole-genome duplication and aquatic-terrestrial transition

Abstract

Whole-genome duplication (WGD) has been observed across a wide variety of eukaryotic groups, contributing to evolutionary diversity and environmental adaptability. Mollusks are the second largest group of animals, and are among the organisms that have successfully adapted to the nonmarine realm through aquatic-terrestrial (A-T) transition, and no comprehensive research on WGD has been reported in this group. To explore WGD and the A-T transition in Mollusca, we assembled a chromosome-level reference genome for the giant African snail Achatina immaculata, a global invasive species, and compared the genomes of two giant African snails (A. immaculata and Achatina fulica) to the other available mollusk genomes. The chromosome-level macrosynteny, colinearity blocks, Ks peak and Hox gene clusters collectively suggested the occurrence of a WGD event shared by A. immaculata and A. fulica. The estimated timing of this WGD event (∼70 MYA) was close to the speciation age of the Sigmurethra-Orthurethra (within Stylommatophora) lineage and the Cretaceous-Tertiary (K-T) mass extinction, indicating that the WGD reported herein may have been a common event shared by all Sigmurethra-Orthurethra species and could have conferred ecological adaptability and genomic plasticity allowing the survival of the K-T extinction. Based on macrosynteny, we deduced an ancestral karyotype containing 8 conserved clusters for the Gastropoda-Bivalvia lineage. To reveal the mechanism of WGD in shaping adaptability to terrestrial ecosystems, we investigated gene families related to the respiration, aestivation and immune defense of giant African snails. Several mucus-related gene families expanded early in the Stylommatophora lineage, functioning in water retention, immune defense and wound healing. The hemocyanins, PCK and FBP families were doubled and retained after WGD, enhancing the capacity for gas exchange and glucose homeostasis in aestivation. After the WGD, zinc metalloproteinase genes were highly tandemly duplicated to protect tissue against ROS damage. This evidence collectively suggests that although the WGD may not have been the direct driver of the A-T transition, it provided an important legacy for the terrestrial adaptation of the giant African snail.

Thede novogenome of the “Spanish” slugArion vulgarisMoquin-Tandon, 1855 (Gastropoda: Panpulmonata): massive expansion of transposable elements in a major pest species

“…fulica, Ac. immaculata, Pomacea canaliculate, and Crassostrea gigas) while absent in other, noninvasive mollusks [22]. Significantly, the expansion of these two types of transposons in A. vulgaris is more obvious than the recently reported TEs expansion in two invasive snails Ac.…”

“…fulica [23], Ac. immaculata [22], Biomphalaria glabrata [47], Radix auricularia [48], Aplysia californica, and Elysia chlorotica [49]). Notably, the main class of TEs in A. californica, E. chlorotica and R. auricularia are DNA while in A. vulgaris, Ac.…”

“…In recent years, genome research has shown its advantages and potential in revealing evolutionary and adaptive mechanisms. However, so far only two land snail genomes were published [22,23]. Compared to land snails, land slugs have 'sacrificed' the protective function of a calcareous shell for less weight and energy costs, less dependence on calcium uptake, better mobility, fast body movements and ability to occupy very small spaces [5].…”

The Crown Pearl: a draft genome assembly of the European freshwater pearl mussel Margaritifera margaritifera (Linnaeus, 1758)

“…Bivalvia 21 , Cephalopoda 72 , Gastropoda 74 and Polyplacophora 80 , most Bivalvia seem to retain the gene composition expected for lophotrochozoans: Hox1, Hox2, Hox3, Hox5, Lox, Antp, Lox4, Lox2, Post2, Post1 for the Hox cluster and Gsx, Xlox, Cdx for the ParaHox cluster 81 .…”

“…65,66,70 ). Given the disparate body plans in molluscan classes, the study of Hox cluster composition, organization and gene expression has practically become a standard in Mollusca genome assembly studies 21,22,[78][79][80][81][82]57,[71][72][73][74][75][76][77] . Homeobox genes are divided into four classes, of which the Antennapedia (ANTP)-class (Hox, ParaHox, NK, Mega-homeobox, SuperHox) is the best studied, particularly the Hox and ParaHox clusters 57,70,75 .…”