Lineage-level divergence of copepod glycerol transporters and the emergence of isoform-specific trafficking regulation

Abstract

Transmembrane conductance of small uncharged solutes such as glycerol typically occurs through aquaglyceroporins (Glps), which are commonly encoded by multiple genes in metazoan organisms. To date, however, little is known concerning the evolution of Glps in Crustacea or what forces might underly such apparent gene redundancy. Here, we show that Glp evolution in Crustacea is highly divergent, ranging from single copy genes in species of pedunculate barnacles, tadpole shrimps, isopods, amphipods and decapods to up to 10 copies in diplostracan water fleas although with monophyletic origins in each lineage. By contrast the evolution of Glps in Copepoda appears to be polyphyletic, with surprisingly high rates of gene duplication occurring in a genera- and species-specific manner. Based upon functional experiments on the Glps from a parasitic copepod (Lepeophtheirus salmonis), we show that such lineage-level gene duplication and splice variation is coupled with a high rate of neofunctionalization. In the case of L. salmonis, splice variation of a given gene resulted in tissue- or sex-specific expression of the channels, with each variant evolving unique sites for protein kinase C (PKC)- or protein kinase A (PKA)-regulation of intracellular membrane trafficking. The combined data sets thus reveal that mutations favouring a high fidelity control of intracellular trafficking regulation can be a selection force for the evolution and retention of multiple Glps in copepods.

Parallel duplication and loss of aquaporin‐coding genes during the “out of the sea” transition as potential key drivers of animal terrestrialization

“…In the phylogenetic tree inferred for Aqp3‐like, we recovered several ancient duplications in the nodes where a habitat transition occurred. Previous studies have reported independent duplications of Aqp3‐like within chelicerates (Finn et al, 2015), myriapods and copepods (Catalán‐García et al, 2021). However, their results could have been biassed due to the omission of other major arthropod lineages in their inferences.…”

“…We identified a total of 2303 arthropodan, 1225 molluscan, and 52 onychophoran Aqps (Data S4) after annotating 310 arthropodan, 101 molluscan and four onychophoran genomic data sets. Only some Aqps from a few arthropod species and even fewer mollusc species had been previously annotated as aquaporins (Catalán‐García et al, 2021; Colgan & Santos, 2018; Finn et al, 2015; Stavang et al, 2015). We also report here the first identification of Aqps in the phylum Onychophora.…”

“…Meanwhile, others have focused on the diversity and evolution of animal aquaporins in groups of human interest, such as vertebrate (Finn et al, 2014) and hemipteran aquaporins (Van Ekert et al, 2016), or insect entomoglyceroporins (Finn et al, 2015). Recent studies have leveraged tnewly available transcriptomic and genomic resources to expand taxon sampling and dig deeper into aquaporin (or aquaglyceroporin) diversity in groups of animals that are not widely studied, such as copepods and crustaceans (Catalán‐García et al, 2021), gastropods (Colgan & Santos, 2018), annelids (Mucciolo et al, 2021), and nonvertebrate deuterostomes (Yilmaz et al, 2020). However, the aquaporin gene repertoire in other animal groups, such as molluscs and less studied arthropod orders (i.e., chelicerates other than spiders, scorpions and mites), has not yet been explored, let alone in a comparative framework within the context of animal terrestrialization.…”

Finding Aquaporins in Annelids: An Evolutionary Analysis and a Case Study

“…No aquaglyceroporins were recovered in the A. succinea transcriptome; however, their presence was retrieved in the congeneric A. virens (Sars, 1835) , as well as in the other annelids and invertebrates ( Figure 2 and Figure 3 ) [ 66 , 73 , 75 ]. Their presumed absence may be due to low sequencing depth (e.g., only one sample [ 43 ]) which may have resulted in a limited number of genes recovered in the transcriptome.…”

First Glimpse at the Diverse Aquaporins of Amphipod Crustaceans

“…Nevertheless, many species are recognized as successful invaders worldwide [ 39 , 40 ], disrupting ecosystem functioning in both marine [ 41 ] and freshwater environments [ 42 ]. To date, no study concerning amphipod AQPs has been carried out, and the only reports on the presence of some gene subfamilies have been indirectly addressed in works related to L. salmonis [ 16 , 43 ] but never further explored.…”