Some like it hot: population-specific adaptations in venom production to abiotic stressors in a widely distributed cnidarian

Abstract

Background In cnidarians, antagonistic interactions with predators and prey are mediated by their venom, whose synthesis may be metabolically expensive. The potentially high cost of venom production has been hypothesized to drive population-specific variation in venom expression due to differences in abiotic conditions. However, the effects of environmental factors on venom production have been rarely demonstrated in animals. Here, we explore the impact of specific abiotic stresses on venom production of distinct populations of the sea anemone Nematostella vectensis (Actiniaria, Cnidaria) inhabiting estuaries over a broad geographic range where environmental conditions such as temperatures and salinity vary widely. Results We challenged Nematostella polyps with heat, salinity, UV light stressors, and a combination of all three factors 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. Strikingly, under a range of abiotic stressors, individuals from different geographic locations along this latitudinal cline modulate differently their venom production levels. Conclusions We demonstrate that abiotic stress results in venom regulation in Nematostella. Together with anecdotal observations from other cnidarian species, our results suggest this might be a universal phenomenon in Cnidaria. The decrease in venom production under stress conditions across species coupled with the evidence for its high metabolic cost in Nematostella suggests downregulation of venom production under certain conditions may be highly advantageous and adaptive. Furthermore, our results point towards local adaptation of this mechanism in Nematostella populations along a latitudinal cline, possibly resulting from distinct genetics and significant environmental differences between their habitats.

The influence of ecological factors on cnidarian venoms

“…We can therefore conclude that environmental temperature can impact cnidarian venom toxins in both short term ( Sachkova et al, 2020 ) and long term ( O'Hara et al, 2018 ) instances. Whilst the gene analysis of the two studies was quantitative, changes in the venom toxicity were not analysed, so it remains unknown what precise ecological impacts the changes in the toxins have.…”

“…This is the only evidence of a controlled environment study, whereby the separate populations were raised in identical conditions, in which toxin gene expression from each population was measured in response to heat shock and salinity. It has been described that N. vectensis animals from North Carolina express toxin genes differently in response to heat stress than those from Massachusetts ( Sachkova et al, 2020 ). Whilst not a comparison of standard venom content across location, the authors describe that populations from different climatic conditions respond differently to heat stress ( Sachkova et al, 2020 ), thus evidencing the ecological significance of cnidarian venom plasticity.…”

“…Research into the effect of salinity on the venom/toxins of not only cnidarians, but marine animals as a whole is scarce. Only one study could be found examining this in zootoxins, in which toxin gene expression was analysed in the sea anemone Nematostella vectensis ( Sachkova et al, 2020 ) . Although this was analysed in relation to population specific adaptations to salinity stress, rather than a salinity oriented study, it demonstrated that reduced salinity stress causes varying levels of toxin gene expression in a number of geographically separated sea anemone populations, suggesting salinity is a contributing ecological factor in venom/toxin production.…”

“…Secondly, toxin gene expression in the sea anemone N. vectensis was analysed in response to short-term (24hr) environmental heat stress ( Sachkova et al, 2020 ). As also noted in the geographic location and salinity sections of this review, it has been described that sea anemone populations from different climatic conditions respond differently to heat stress in relation to venom production.…”

“…As also noted in the geographic location and salinity sections of this review, it has been described that sea anemone populations from different climatic conditions respond differently to heat stress in relation to venom production. Strong evidence highlights that the thermal ecology of the animal plays a role in toxin gene expression, as the thermal regimes differ between N. vectensis habitats, and those populations not naturally exposed to higher temperatures respond differently in their toxin gene expression ( Sachkova et al, 2020 ).…”