Functional Evolution of Clustered Aquaporin Genes Reveals Insights into the Oceanic Success of Teleost Eggs

Abstract

Aquaporin-mediated oocyte hydration is considered important for the evolution of pelagic eggs and the radiative success of marine teleosts. However, the molecular regulatory mechanisms controlling this vital process are not fully understood. Here, we analyzed >400 piscine genomes to uncover a previously unknown teleost-specific aquaporin-1 cluster (TSA1C) comprised of tandemly arranged aqp1aa-aqp1ab2-aqp1ab1 genes. Functional evolutionary analysis of the TSA1C reveals a ∼300-million-year history of downstream aqp1ab-type gene loss, neofunctionalization and subfunctionalization, but with marine species that spawn highly hydrated pelagic eggs almost exclusively retaining at least one of the downstream paralogs. Unexpectedly, one third of the modern marine euacanthomorph teleosts selectively retain both aqp1ab-type channels, and co-evolved protein kinase-mediated phosphorylation sites in the intracellular subdomains together with teleost-specific Ywhaz-like (14-3-3ζ-like) binding proteins for co-operative membrane trafficking regulation. To understand the selective evolutionary advantages of these mechanisms, we show that a two-step regulated channel shunt avoids competitive occupancy of the same plasma membrane space in the oocyte and accelerates hydration. These data suggest that the evolution of the adaptive molecular regulatory features of the TSA1C facilitated the rise of pelagic eggs and their subsequent geodispersal in the oceanic currents.

Neurohypophysial and paracrine vasopressinergic signaling regulates aquaporin trafficking to hydrate marine teleost oocytes

“…Up to 15 subfamilies (AQP0-14) are recognized in egg-laying mammals, but due to gene loss, only 13 subfamilies (AQP0-12) remain in placental mammals ( 6 ). Conversely, although a similar number of orthologous subfamilies have been identified in teleost fishes, the gene copy numbers are higher (19-26 in diploids, 38-48 in paleotetraploids) due to extra rounds of whole genome duplications combined with cladal- and lineage-level tandem duplications and gene losses ( 6 – 12 ).…”

“…In mammalian follicles AQP1, -5, -7, -8 and -9 are thought to mediate water transport via the granulosa cells to form the extracellular antrum ( 3 , 13 , 14 ). In contrast, in marine teleosts water flows intracellularly into the oocyte across the plasma membrane via tandemly duplicated orthologs of mammalian AQP1 (Aqp1ab1 and/or Aqp1ab2) ( 12 , 15 – 18 ). The Aqp1ab-type paralogs are encoded in an ancient teleost-specific aquaporin-1 cluster (TSA1C: aqp1aa-aqp1ab2-aqp1ab1 ) that evolved ~300 Ma with the emergence of the clade ( 12 ).…”

“…In contrast, in marine teleosts water flows intracellularly into the oocyte across the plasma membrane via tandemly duplicated orthologs of mammalian AQP1 (Aqp1ab1 and/or Aqp1ab2) ( 12 , 15 – 18 ). The Aqp1ab-type paralogs are encoded in an ancient teleost-specific aquaporin-1 cluster (TSA1C: aqp1aa-aqp1ab2-aqp1ab1 ) that evolved ~300 Ma with the emergence of the clade ( 12 ). The aqp1ab -type genes of the TSA1C are highly selectively retained in marine species that spawn pelagic eggs, and their loop D and C-terminal subdomains co-evolved together with protein kinase (PKA) pathways and 14-3-3ζ-like (YwhazL) binding proteins to establish a two-step regulated trafficking mechanism that avoids competitive occupancy of the same oocyte membrane space ( 12 ).…”

“…The Aqp1ab-type paralogs are encoded in an ancient teleost-specific aquaporin-1 cluster (TSA1C: aqp1aa-aqp1ab2-aqp1ab1 ) that evolved ~300 Ma with the emergence of the clade ( 12 ). The aqp1ab -type genes of the TSA1C are highly selectively retained in marine species that spawn pelagic eggs, and their loop D and C-terminal subdomains co-evolved together with protein kinase (PKA) pathways and 14-3-3ζ-like (YwhazL) binding proteins to establish a two-step regulated trafficking mechanism that avoids competitive occupancy of the same oocyte membrane space ( 12 ). This preovulatory process occurs during the maturational break down of the germinal vesicle (GVBD) and meiosis resumption to form highly hydrated pelagic eggs (>90% H 2 O) that are subsequently dispersed in the oceanic currents ( 12 , 19 ).…”

“…In the stinging catfish, in addition to the neuroendocrine/reproductive centers of the brain ( 28 ), an intraovarian vasopressinergic system has been described that could also be involved in the paracrine regulation of oocyte hydration ( 22 – 24 , 38 ). However, although the Aqp1ab2 channel has been implicated in this mechanism ( 23 ), no study has yet demonstrated its subcellular localization or indeed that of the Aqp1aa and Aqp1ab1 channels, which are also encoded in the TSA1C of catfishes ( 12 ). In contrast to freshwater fishes in which only ~1% produce semi-buoyant eggs, the great majority of modern euacanthomorph marine teleosts, such as the gilthead seabream ( Sparus aurata ), produce highly hydrated pelagic eggs ( 2 , 12 , 39 ), yet the ovarian production of Avp or Oxt has not been reported.…”