The Lineage-Specific Evolution of Aquaporin Gene Clusters Facilitated Tetrapod Terrestrial Adaptation

Abstract

A major physiological barrier for aquatic organisms adapting to terrestrial life is dessication in the aerial environment. This barrier was nevertheless overcome by the Devonian ancestors of extant Tetrapoda, but the origin of specific molecular mechanisms that solved this water problem remains largely unknown. Here we show that an ancient aquaporin gene cluster evolved specifically in the sarcopterygian lineage, and subsequently diverged into paralogous forms of AQP2, -5, or -6 to mediate water conservation in extant Tetrapoda. To determine the origin of these apomorphic genomic traits, we combined aquaporin sequencing from jawless and jawed vertebrates with broad taxon assembly of >2,000 transcripts amongst 131 deuterostome genomes and developed a model based upon Bayesian inference that traces their convergent roots to stem subfamilies in basal Metazoa and Prokaryota. This approach uncovered an unexpected diversity of aquaporins in every lineage investigated, and revealed that the vertebrate superfamily consists of 17 classes of aquaporins (Aqp0 - Aqp16). The oldest orthologs associated with water conservation in modern Tetrapoda are traced to a cluster of three aqp2-like genes in Actinistia that likely arose >500 Ma through duplication of an aqp0-like gene present in a jawless ancestor. In sea lamprey, we show that aqp0 first arose in a protocluster comprised of a novel aqp14 paralog and a fused aqp01 gene. To corroborate these findings, we conducted phylogenetic analyses of five syntenic nuclear receptor subfamilies, which, together with observations of extensive genome rearrangements, support the coincident loss of ancestral aqp2-like orthologs in Actinopterygii. We thus conclude that the divergence of sarcopterygian-specific aquaporin gene clusters was permissive for the evolution of water conservation mechanisms that facilitated tetrapod terrestrial adaptation.

Molecular Characterization of Aquaporin 1 and Aquaporin 3 from the Gills of the African Lungfish, Protopterus annectens, and Changes in Their Branchial mRNA Expression Levels and Protein Abundance during Three Phases of Aestivation

“…Indeed, our dendrogramic analyses indicated that Aqp1 and Aqp3 of P. annectens were grouped closer to tetrapods than to teleost fishes, which corroborate previous reports on the evolution of Aqp/AQP (Finn et al, 2014; Finn and Cerdà, 2015). Furthermore, our results are in agreement with previous reports on genes/proteins of P. annectens that bear close relationship with those of tetrapods (argininosuccinate lyase, Chng et al, 2014; gulonolactone oxidase, Ching et al, 2014; Na + /K + -ATPase α-subunit isoforms, Hiong et al, 2014; betaine-homocysteine S -methyltransferase 1, Ong et al, 2015; coagulation factor II and fibrinogen gamma chain, Hiong et al, 2015).…”

“…To date, 17 AQP subfamilies (AQP0-16) have been described in a wide variety of animals (Finn et al, 2014), of which AQP0-12 have been categorized into three major groups: classical water-selective AQP (AQP0, −1, −2, −4, and −5), aquaglyceroporins (AQP3, −7, −9, and −10) permeable to glycerol, urea, and ammonia in addition to water, and unorthodox AQP (AQP6, −8, −11, and −12; Litman et al, 2009). Notably, Aqps are important water channels in the gills of many fishes and they may play a more crucial role in facilitating cell volume-regulatory fluxes of water than in transepithelial water transport (Madsen et al, 2015).…”

Bumetanide Derivatives AqB007 and AqB011 Selectively Block the Aquaporin-1 Ion Channel Conductance and Slow Cancer Cell Migration

“…To date, at least 15 mammalian subfamilies have been identified: AQP0-AQP14 (Ishibashi, 2009;Finn et al, 2014). Aquaporin is organized as a tetramer of subunits, each comprising six transmembrane domains and five loops (A-E) and carrying a monomeric pore that allows the movement of water or other small solutes (Jung et al, 1994;Fu et al, 2000;Sui et al, 2001).…”

Hormonal regulation of aquaporin 3: opposing actions of prolactin and cortisol in tilapia gill

“…Teleosts (e.g., Atlantic salmon (Salmo salar)) may express up to 42 paralogs (Finn et al 2014). Multiple teleost Aqps are expressed in osmoregulatory epithelia; for example, Aqp3, an aquaglyceroporin, which transports water, glycerol, and urea, has been studied in a suite of euryhaline teleosts with particular attention to its expression following changes in salinity.…”