Adaptive venom evolution and toxicity in octopods is driven by extensive novel gene formation, expansion, and loss

Abstract

Background Cephalopods represent a rich system for investigating the genetic basis underlying organismal novelties. This diverse group of specialized predators has evolved many adaptations including proteinaceous venom. Of particular interest is the blue-ringed octopus genus (Hapalochlaena), which are the only octopods known to store large quantities of the potent neurotoxin, tetrodotoxin, within their tissues and venom gland. Findings To reveal genomic correlates of organismal novelties, we conducted a comparative study of 3 octopod genomes, including the Southern blue-ringed octopus (Hapalochlaena maculosa). We present the genome of this species and reveal highly dynamic evolutionary patterns at both non-coding and coding organizational levels. Gene family expansions previously reported in Octopus bimaculoides (e.g., zinc finger and cadherins, both associated with neural functions), as well as formation of novel gene families, dominate the genomic landscape in all octopods. Examination of tissue-specific genes in the posterior salivary gland revealed that expression was dominated by serine proteases in non–tetrodotoxin-bearing octopods, while this family was a minor component in H. maculosa. Moreover, voltage-gated sodium channels in H. maculosa contain a resistance mutation found in pufferfish and garter snakes, which is exclusive to the genus. Analysis of the posterior salivary gland microbiome revealed a diverse array of bacterial species, including genera that can produce tetrodotoxin, suggestive of a possible production source. Conclusions We present the first tetrodotoxin-bearing octopod genome H. maculosa, which displays lineage-specific adaptations to tetrodotoxin acquisition. This genome, along with other recently published cephalopod genomes, represents a valuable resource from which future work could advance our understanding of the evolution of genomic novelty in this family.

Genome Analysis of Lagocephalus sceleratus: Unraveling the Genomic Landscape of a Successful Invader

“…This could also suggest that the position of the replacement is more important than the amino acid change per se. Our results are also congruent with previous findings for Hapalochlaena lunulata (Geffeney et al, 2019) and Hapalochlaena maculosa (Whitelaw et al, 2020), as NaV1.4a Domain I is highly conserved in both octopod species. Furthermore, unlike the pufferfishes A. nigropunctatus and T. nigroviridis (Jost et al, 2008), the garter snake Thamnophis couchii (Feldman et al, 2012) and the octopuses Hapalochlaena lunulata (Geffeney et al, 2019) and Hapalochlaena maculosa (Whitelaw et al, 2020), replacements were also not observed in the NaV1.4a Domain III of L. sceleratus.…”

“…Previously, these mutations for T. rubripes and T. nigroviridis had not been associated with TTX resistance ( Venkatesh et al, 2005 ; Soong and Venkatesh, 2006 ). At the last positions of Domain IV, there are also two replacements to His and Ser in H. lunulata ( Geffeney et al, 2019 ) and H. maculosa ( Whitelaw et al, 2020 ), which may inhibit TTX binding.…”

Marine Neurotoxins’ Effects on Environmental and Human Health: An OMICS Overview

“…DNA sequencing and RNA-Seq [32] Takifugu rubripes Involvement of the immune system in the liver. RT-PCR [33] Takifugu rubripes Involvement of the immune system in the liver.…”

Convergent Loss of Chemoreceptors across Independent Origins of Slave-Making in Ants

“…Although the benefits of acquired genes and the utilization of existing or duplicated genes ( Kondrashov 2012 ; Qian and Zhang 2014 ) for novel traits have been well studied through comparative evolutionary genomics and transcriptomics ( Zhou et al 2019 ; Whitelaw et al 2020 ; Calla 2021 ), the benefits of gene losses are more difficult to verify. The study of convergent gene loss patterns may represent a first step in this direction, as such convergence provides insights into potential adaptive benefits of gene losses.…”