Genomic insights into the adaptation and evolution of the nautilus, an ancient but evolving “living fossil”

Abstract

The nautilus, commonly known as a "living fossil," is endangered and may be at risk of extinction. The lack of genomic information hinders a thorough understanding of its biology and evolution, which can shed light on the conservation of this endangered species. Here, we report the first high-quality chromosome-level genome assembly of Nautilus pompilius. The assembled genome size comprised 785.15 Mb. Comparative genomic analyses indicated that transposable elements (TEs) and large-scale genome reorganizations may have driven lineage-specific evolution in the cephalopods.Remarkably, evolving conserved genes and recent TE insertion activities were identified in N. pompilius, and we speculate that these findings reflect the strong adaptability and long-term survival of the nautilus. We also identified gene families that are potentially responsible for specific adaptation and evolution events. Our study provides unprecedented insights into the specialized biology and evolution of N. pompilius, and the results serve as an important resource for future conservation genomics of the nautilus and closely related species.

Gene recruitments and dismissals in argonaut octopus genome provide insights to pelagic lifestyle adaptation and shell-like eggcase reacquisition

“…In this study, we found all of the eggcase matrix protein-coding genes in the genome of A. argo (Table S5) as identified by our previous multi-omics study to survey and identify major proteins of the eggcase matrices of two congeneric argonaut octopods, A. argo and A. hians (Setiamarga et al, 2021b). Exactly congruent to our previous result, most of the proteins are apparently not shared with the shell matrix proteins of Conchiferans, including those of the basal Cephalopoda Nautilus (Setiamarga et al, 2021a;Huang et al, 2021), although the genes / proteins themselves are present in the genomes of the Conchiferan mollusks such as the limpet L. gigantea (Simakov et al, 2013), the true oyster C. gigas (Peñaloza et al, 2021), and the Japanese pearl oyster P. fucata (Takeuchi et al, 2016). Meanwhile, the Conchiferan shell matrix protein-coding genes were also mostly found in the genomes of A. argo and the shell-less benthic octopod O. bimaculoides (Albertin et al, 2015), indicating their retention despite shell loss in the octopod lineage.…”

“…The ParaHox cluster of A. argo were found to conserve the structure of a typical Lophothrocozoan cluster, similar to those reported in Nautilus (Huang et al 2021) and the octopus (Li et al, 2020). Although further study is still needed, the highly conserved nature of the ParaHox clusters among Cephalopoda, mollusks, and even Lophotrochozoans, indicates a possible presence of an evolutionary constraint to conserve the cluster's presence and arrangement in the genome, after the breakage of Cdx from Gsx and Xlox.…”

“…More interestingly, an intact pif sequence was also found in the genome of N. pompilius (Huang et al 2021), although the sequence was not found in the transcriptome and proteome data of our recent shell matrix proteins multi-omics study of the species (Setiamarga et al, 2021a). The exon-intron structures of each cluster are different and are located at different positions in the genome of both A. argo (Figure 5b) and Nautilus.…”

“…Similarly, an older gene cluster that is widespread in the animal kingdom is Wnt. Most genomes of bilaterians have a common cluster, wnt9-wnt1-wnt6-wnt10, or parts of this cluster (Huang et al, 2021). This ancestral cluster of wnts is thought to originate in the evolution of the common ancestor of cnidarians and bilaterians (Janssen et al, 2010;Holstein 2012).…”

“…Until very recently, the lack of genome data had prevented us from understanding the genetic basis of Cephalopod biology, and even molluscan biology. This was remedied by recent reports of various Cephalopod genomes, such as the genomes of O. bimaculoides (Albertin et al, 2019), Euprymna scolopes (Belcaid et al, 2019), Architeuthis dux (da Forsa et al 2020), and the basal Cephalopod Nautilus pompilius (Zhang et al, 2021;Huang et al, 2021). Comparative genomics studies of these genomes have allowed us to identify notable characteristics of Cephalopod genomes except Nautilus, such as: (1) the average genome size of around 3 Gigabases (Gb), which is slightly bigger than that of other molluscan species (Gregory 2021), (2) highly rearranged genome with transposable element expansion, which have caused the genomes to be highly repetitive in nature (Albertin et al, 2015;da Fonseca et al, 2020), (3) lineage specific duplication of certain types of genes (Yoshida et al, 2011), and (4) whole transcript-wide adenosine to inosine (A-to-I) RNA editing (Alon et al 2015;Liscovitch-Brauer et al 2017).…”