Population Specific Adaptations in Venom Production to Abiotic Stressors in a Widely Distributed Cnidarian

Abstract

Nematostella vectensis is a sea anemone (Actiniaria, Cnidaria) inhabiting estuaries over a broad geographic range where environmental conditions such as temperatures and salinity vary widely.In cnidarians, antagonistic interactions with predators and prey are mediated by their venom, which may be metabolically expensive. In this study, we challenged Nematostella polyps with heat, salinity, UV light stressors and a combination of all three to determine how abiotic stressors impact toxin expression for individuals collected across this species' range. Transcriptomics and proteomics revealed that the highly abundant toxin Nv1 was the most downregulated gene under heat stress conditions in multiple populations. Physiological measurements demonstrated that venom is metabolically costly to produce suggesting that downregulating venom expression under stressful conditions may be advantageous. Strikingly, under a range of abiotic stressors, individuals from different geographic locations along this latitudinal cline modulate venom production levels differently in a pattern reflecting local adaptation.

Characterising Functional Venom Profiles of Anthozoans and Medusozoans within Their Ecological Context

“…Their success lies in part in their ability to respond to different environmental pressures [46]. Within actiniarians, ecological interactions and environmental conditions are key drivers of the expression of toxin genes, rather than the retention and expansion of gene families [16,47,48]. Comparative analysis supports the minimal impact of environmental factors on the toxin gene complement, revealing that closely related cnidarian species have more similar toxin gene complements than those that share an ecological niche [16].…”

“…These results suggest that speciation is an important driver of toxin gene complement and sequence variation. However, the influence of ecological factors on toxin expression results in dynamic spatial and temporal patterns of venom composition [16,47,48].…”

Implications of bleaching on cnidarian venom ecology

“…A range of ecological factors have been shown to impact on the venom profile and expenditure in cnidarians ( O'Hara et al, 2021 ). Briefly, venom variations and/or changes have been attributed to differences in temperature ( Jouiaei et al, 2015a ; O'Hara et al, 2018 ; Oakley et al, 2017 ; Richier et al, 2008 ; Sachkova et al, 2020 ; Sunagawa et al, 2009 ), age ( Columbus-Shenkar et al, 2018 ; Klompen et al, 2018 ; McClounan and Seymour, 2012 ; Underwood and Seymour, 2007 ), diet ( Underwood and Seymour, 2007 ), location ( Winter et al, 2010 ; Yue et al, 2019 ), salinity ( Sachkova et al, 2020 ), ultraviolet radiation ( Richier et al, 2008 ; Sachkova et al, 2020 ), interspecies competition ( Yosef et al, 2020 ) and predation pressure ( Ben-Ari et al, 2018 ).…”

“…As up to 46% of all cells within cnidarians, such as H. attenuata , may be either mature or developing cnidocytes ( Bode et al, 1973 ), there is an almost constant production of cnidocytes ( Tardent, 1995 ). The replenishment of cnidocysts (and venom) is hypothesized to come at a significant metabolic cost ( Fautin, 2009 ; Sachkova et al, 2020 ). The high metabolic costs of cnidae production has been demonstrated in Nematostella vectnsis (Actiniaria) as a rapid increase in the expression of genes associated with venom toxins and nematocyst structure, positively correlated to increased respiration rates over a 5 h period ( Sachkova et al, 2020 ).…”

“…The replenishment of cnidocysts (and venom) is hypothesized to come at a significant metabolic cost ( Fautin, 2009 ; Sachkova et al, 2020 ). The high metabolic costs of cnidae production has been demonstrated in Nematostella vectnsis (Actiniaria) as a rapid increase in the expression of genes associated with venom toxins and nematocyst structure, positively correlated to increased respiration rates over a 5 h period ( Sachkova et al, 2020 ). These results suggest that the replacement of venoms and also their delivery systems come at a significant energetic cost to the cnidarian.…”