Molecular evidence of intertidal habitats selecting for repeated ice-binding protein evolution in invertebrates

Abstract

Ice-binding proteins (IBPs) have evolved independently in multiple taxonomic groups to improve their survival at sub-zero temperatures. Intertidal invertebrates in temperate and polar regions frequently encounter sub-zero temperatures, yet there is little information on IBPs in these organisms. We hypothesized that there are far more IBPs than are currently known and that the occurrence of freezing in the intertidal zone selects for these proteins. We compiled a list of genome-sequenced invertebrates across multiple habitats and a list of known IBP sequences and used BLAST to identify a wide array of putative IBPs in those invertebrates. We found that the probability of an invertebrate species having an IBP was significantly greater in intertidal species than in those primarily found in open ocean or freshwater habitats. These intertidal IBPs had high sequence similarity to fish and tick antifreeze glycoproteins and fish type II antifreeze proteins. Previously established classifiers based on machine learning techniques further predicted ice-binding activity in the majority of our newly identified putative IBPs. We investigated the potential evolutionary origin of one putative IBP from the hard-shelled mussel Mytilus coruscus and suggest that it arose through gene duplication and neofunctionalization. We show that IBPs likely readily evolve in response to freezing risk and that there is an array of uncharacterized IBPs, and highlight the need for broader laboratory-based surveys of the diversity of ice-binding activity across diverse taxonomic and ecological groups.

Ocean acidification increases susceptibility to sub-zero air temperatures in ecosystem engineers and limits poleward range shifts

“…While we were unable to explain the variation in freeze tolerance under present-day and acidified conditions, variation in freeze tolerance among populations and congeners may be explained by high molecular weight cryoprotectants, for example, ice binding proteins, not measured here. Indeed, the influence of antifreeze proteins on freeze tolerance in Mytilus ought to be explored further as their potential role seems to vary among populations ( Box et al, 2022 ; Loomis, 1995 ). Furthermore, thermal tolerance variation may be explained at the gene level ( Clark et al, 2021 ; Peck et al, 2015 ).…”

“…low molecular weight compounds), such as trimethylamine n-oxide (TMAO), betaine, strombine, and the amino acid taurine, likely acts as cryoprotectants that increase freeze tolerance ( Kennedy et al, 2020 ; Loomis et al, 1988 ). While underexplored, it also appears that many intertidal species may have an array of ice binding proteins that help manage ice growth and propagation ( Box et al, 2022 ).…”

Microhabitat-specific diurnal metabolomic responses of the intertidal limpet Cellana toreuma to winter low temperature

“… 39 , 40 , 41 , 42 , 43 When organisms encounter low temperatures, a series of metabolites are produced to protect them from cryoinjuries. 10 , 44 , 45 , 46 , 47 To resist cold stress, for instance, intertidal mussels accumulated osmolytes to increase freeze tolerance. 10 , 48 Consequently, metabolic adaptations are crucial for resisting cold stress during dynamic environmental changes.…”