Genomic and physiological mechanisms underlying skin plasticity during water to air transition in an amphibious fish

Abstract

The terrestrial radiation of vertebrates required changes in skin that resolved the dual demands of maintaining a mechanical and physiological barrier while also facilitating ion and gas transport. Using the amphibious killifish Kryptolebias marmoratus, we found that transcriptional regulation of skin morphogenesis was quickly activated upon air exposure (1 h). Rapid regulation of cell–cell adhesion complexes and pathways that regulate stratum corneum formation was consistent with barrier function and mechanical reinforcement. Unique blood vessel architecture and regulation of angiogenesis likely supported cutaneous respiration. Differences in ionoregulatory transcripts and ionocyte morphology were correlated with differences in salinity acclimation and resilience to air exposure. Evolutionary analyses reinforced the adaptive importance of these mechanisms. We conclude that rapid plasticity of barrier, respiratory and ionoregulatory functions in skin evolved to support the amphibious lifestyle of K. marmoratus; similar processes may have facilitated the terrestrial radiation of other contemporary and ancient fishes.

The time course of molecular acclimation to seawater in a euryhaline fish

“…At the same time, genes involved in keratinization, a process by which keratin accumulate inside epithelial tissue cells to provide barrier-like functions, started to be upregulated. Keratinization gene expression has been found to be salinity dependent in tilapia 113 and to be upregulated following air exposure in the skin of the mangrove rivulus, Kryptolebias marmoratus 114 . Keratinization may represent a strategy to reduce the amount of water loss during dehydration, possibly also following increased environmental salinity, as seen in Arabian pupfish.…”

Adaptations and plastic phenotypic responses of marine animals to the environmental challenges of the high intertidal zone

“…Kryptolebias marmoratus can maintain whole-body water levels while emersed for several days, and is also able to increase cutaneous water influx during this time, which may benefit water absorption through the skin (e.g., while remaining in a moist refuge during the dry season) (LeBlanc et al 2010, Heffell et al 2018. These changes in water permeability could be, in part, related to a rapid (i.e., within hours) increase in the expression of aquaporin genes (e.g., aquaporin 3) (Dong et al 2021). Finally, females of some upper intertidal porcelain crab species (e.g., Petrolisthes laevigatus and P. violaceus) provide ~20% more water to their embryos than subtidal species (such as Allopetrolisthes punctatus) from the same local environment, which likely improves their survival in air (Viña et al 2018).…”

Respiratory plasticity during acclimation to hypoxia and following a recovery in normoxia

“…Phenotypic plasticity in response to hypoxia can occur rapidly in fishes and enhances Dybowski, 1869), for example, remodels its entire gill structure after just a 30-min hypoxic exposure (Yang et al, 2021). Similarly, the mangrove rivulus (Kryptolebias marmoratus Poey, 1880) remodels epidermal ionocytes and respiratory traits after just 24 h of air exposure (Blanchard et al, 2019;Dong et al, 2021). Moreover, a brief ischemic period can precondition fish cardiac myocytes to help maintain stroke volume and cardiac output, can induce cardiac hypertrophy and can enhance the sarcolemmal ATP-sensitive K + channels, helping fish to perform better in a subsequent hypoxic episode (Gamperl et al, 2001b;Gillis and Johnston, 2017;Carnevale et al, 2021).…”