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

Whitelaw, Brooke L., Cooke, Ira R., Finn, Julian, da Fonseca, Rute R., Ritschard, Elena A., Gilbert, M. T. P., Simakov, Oleg, and Strugnell, Jan M. (2020) Adaptive venom evolution and toxicity in octopods is driven by extensive novel gene formation, expansion, and loss. GigaScience, 9 (11). giaa120.

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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.

Item ID: 65046
Item Type: Article (Research - C1)
ISSN: 2047-217X
Keywords: cephalopod genome; comparative genomics; gene family expansions; transposable elements; venom evolution
Copyright Information: © The Author(s) 2020. Published by Oxford University Press GigaScience. This is an Open Access article distributed under the terms of the Creative Commons Attribution License.
Funders: Australian Biological Resources Study (ABRS), Austrian Science Fund (FWF)
Projects and Grants: ABRS grant RF211–41, FWF grant P30686-B29
Research Data: http://dx.doi.org/10.5524/100793.
Date Deposited: 16 Nov 2020 05:57
FoR Codes: 31 BIOLOGICAL SCIENCES > 3105 Genetics > 310509 Genomics @ 50%
31 BIOLOGICAL SCIENCES > 3105 Genetics > 310508 Genome structure and regulation @ 25%
31 BIOLOGICAL SCIENCES > 3105 Genetics > 310505 Gene expression (incl. microarray and other genome-wide approaches) @ 25%
SEO Codes: 96 ENVIRONMENT > 9608 Flora, Fauna and Biodiversity > 960808 Marine Flora, Fauna and Biodiversity @ 100%
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