Phylogenomic and functional analyses of salmon lice aquaporins uncover the molecular diversity of the superfamily in Arthropoda
Abstract Background An emerging field in biomedical research is focusing on the roles of aquaporin water channels in parasites that cause debilitating or lethal diseases to their vertebrate hosts. The primary vectorial agents are hematophagous arthropods, including mosquitoes, flies, ticks and lice,...
Main Authors: | , , , , , |
---|---|
Format: | Article in Journal/Newspaper |
Language: | English |
Published: |
BioMed Central Ltd.
2015
|
Subjects: | |
Online Access: | http://www.biomedcentral.com/1471-2164/16/618 |
id |
ftbiomed:oai:biomedcentral.com:s12864-015-1814-8 |
---|---|
record_format |
openpolar |
spelling |
ftbiomed:oai:biomedcentral.com:s12864-015-1814-8 2023-05-15T15:31:37+02:00 Phylogenomic and functional analyses of salmon lice aquaporins uncover the molecular diversity of the superfamily in Arthropoda Stavang, Jon Chauvigné, Francois Kongshaug, Heidi Cerdà, Joan Nilsen, Frank Finn, Roderick 2015-08-19 http://www.biomedcentral.com/1471-2164/16/618 en eng BioMed Central Ltd. http://www.biomedcentral.com/1471-2164/16/618 Copyright 2015 Stavang et al. Aquaporin Aquaglyceroporin Arthropod Crustacea Copepod Salmon louse Lepeoptheirus Parasite Atlantic salmon Evolution Osmoregulation Fluid homeostasis Permeability Selectivity Research article 2015 ftbiomed 2015-08-23T00:04:43Z Abstract Background An emerging field in biomedical research is focusing on the roles of aquaporin water channels in parasites that cause debilitating or lethal diseases to their vertebrate hosts. The primary vectorial agents are hematophagous arthropods, including mosquitoes, flies, ticks and lice, however very little is known concerning the functional diversity of aquaporins in non-insect members of the Arthropoda. Here we conducted phylogenomic and functional analyses of aquaporins in the salmon louse, a marine ectoparasitic copepod that feeds on the skin and body fluids of salmonids, and used the primary structures of the isolated channels to uncover the genomic repertoires in Arthropoda. Results Genomic screening identified 7 aquaporin paralogs in the louse in contrast to 42 in its host the Atlantic salmon. Phylogenetic inference of the louse nucleotides and proteins in relation to orthologs identified in Chelicerata, Myriapoda, Crustacea and Hexapoda revealed that the arthropod aquaporin superfamily can be classified into three major grades (1) classical aquaporins including Big brain (Bib) and Prip-like (PripL) channels (2) aquaglyceroporins (Glp) and (3) unorthodox aquaporins (Aqp12-like). In Hexapoda, two additional subfamilies exist as Drip and a recently classified entomoglyceroporin (Eglp) group. Cloning and remapping the louse cDNAs to the genomic DNA revealed that they are encoded by 1–7 exons, with two of the Glps being expressed as N-terminal splice variants (Glp1_v1, −1_v2, −3_v1, −3_v2). Heterologous expression of the cRNAs in amphibian oocytes demonstrated that PripL transports water and urea, while Bib does not. Glp1_v1, −2, −3_v1 and −3_v2 each transport water, glycerol and urea, while Glp1_v2 and the Aqp12-like channels were retained intracellularly. Transcript abundance analyses revealed expression of each louse paralog at all developmental stages, except for glp1_v1 , which is specific to preadult and adult males. Conclusions Our data suggest that the aquaporin repertoires of extant arthropods have expanded independently in the different lineages, but can be phylogenetically classified into three major grades as opposed to four present in deuterostome animals. While the aquaporin repertoire of Atlantic salmon represents a 6-fold redundancy compared to the louse, the functional assays reveal that the permeation properties of the different crustacean grades of aquaporin are largely conserved to the vertebrate . Article in Journal/Newspaper Atlantic salmon BioMed Central The Louse ENVELOPE(-56.415,-56.415,51.700,51.700) |
institution |
Open Polar |
collection |
BioMed Central |
op_collection_id |
ftbiomed |
language |
English |
topic |
Aquaporin Aquaglyceroporin Arthropod Crustacea Copepod Salmon louse Lepeoptheirus Parasite Atlantic salmon Evolution Osmoregulation Fluid homeostasis Permeability Selectivity |
spellingShingle |
Aquaporin Aquaglyceroporin Arthropod Crustacea Copepod Salmon louse Lepeoptheirus Parasite Atlantic salmon Evolution Osmoregulation Fluid homeostasis Permeability Selectivity Stavang, Jon Chauvigné, Francois Kongshaug, Heidi Cerdà, Joan Nilsen, Frank Finn, Roderick Phylogenomic and functional analyses of salmon lice aquaporins uncover the molecular diversity of the superfamily in Arthropoda |
topic_facet |
Aquaporin Aquaglyceroporin Arthropod Crustacea Copepod Salmon louse Lepeoptheirus Parasite Atlantic salmon Evolution Osmoregulation Fluid homeostasis Permeability Selectivity |
description |
Abstract Background An emerging field in biomedical research is focusing on the roles of aquaporin water channels in parasites that cause debilitating or lethal diseases to their vertebrate hosts. The primary vectorial agents are hematophagous arthropods, including mosquitoes, flies, ticks and lice, however very little is known concerning the functional diversity of aquaporins in non-insect members of the Arthropoda. Here we conducted phylogenomic and functional analyses of aquaporins in the salmon louse, a marine ectoparasitic copepod that feeds on the skin and body fluids of salmonids, and used the primary structures of the isolated channels to uncover the genomic repertoires in Arthropoda. Results Genomic screening identified 7 aquaporin paralogs in the louse in contrast to 42 in its host the Atlantic salmon. Phylogenetic inference of the louse nucleotides and proteins in relation to orthologs identified in Chelicerata, Myriapoda, Crustacea and Hexapoda revealed that the arthropod aquaporin superfamily can be classified into three major grades (1) classical aquaporins including Big brain (Bib) and Prip-like (PripL) channels (2) aquaglyceroporins (Glp) and (3) unorthodox aquaporins (Aqp12-like). In Hexapoda, two additional subfamilies exist as Drip and a recently classified entomoglyceroporin (Eglp) group. Cloning and remapping the louse cDNAs to the genomic DNA revealed that they are encoded by 1–7 exons, with two of the Glps being expressed as N-terminal splice variants (Glp1_v1, −1_v2, −3_v1, −3_v2). Heterologous expression of the cRNAs in amphibian oocytes demonstrated that PripL transports water and urea, while Bib does not. Glp1_v1, −2, −3_v1 and −3_v2 each transport water, glycerol and urea, while Glp1_v2 and the Aqp12-like channels were retained intracellularly. Transcript abundance analyses revealed expression of each louse paralog at all developmental stages, except for glp1_v1 , which is specific to preadult and adult males. Conclusions Our data suggest that the aquaporin repertoires of extant arthropods have expanded independently in the different lineages, but can be phylogenetically classified into three major grades as opposed to four present in deuterostome animals. While the aquaporin repertoire of Atlantic salmon represents a 6-fold redundancy compared to the louse, the functional assays reveal that the permeation properties of the different crustacean grades of aquaporin are largely conserved to the vertebrate . |
format |
Article in Journal/Newspaper |
author |
Stavang, Jon Chauvigné, Francois Kongshaug, Heidi Cerdà, Joan Nilsen, Frank Finn, Roderick |
author_facet |
Stavang, Jon Chauvigné, Francois Kongshaug, Heidi Cerdà, Joan Nilsen, Frank Finn, Roderick |
author_sort |
Stavang, Jon |
title |
Phylogenomic and functional analyses of salmon lice aquaporins uncover the molecular diversity of the superfamily in Arthropoda |
title_short |
Phylogenomic and functional analyses of salmon lice aquaporins uncover the molecular diversity of the superfamily in Arthropoda |
title_full |
Phylogenomic and functional analyses of salmon lice aquaporins uncover the molecular diversity of the superfamily in Arthropoda |
title_fullStr |
Phylogenomic and functional analyses of salmon lice aquaporins uncover the molecular diversity of the superfamily in Arthropoda |
title_full_unstemmed |
Phylogenomic and functional analyses of salmon lice aquaporins uncover the molecular diversity of the superfamily in Arthropoda |
title_sort |
phylogenomic and functional analyses of salmon lice aquaporins uncover the molecular diversity of the superfamily in arthropoda |
publisher |
BioMed Central Ltd. |
publishDate |
2015 |
url |
http://www.biomedcentral.com/1471-2164/16/618 |
long_lat |
ENVELOPE(-56.415,-56.415,51.700,51.700) |
geographic |
The Louse |
geographic_facet |
The Louse |
genre |
Atlantic salmon |
genre_facet |
Atlantic salmon |
op_relation |
http://www.biomedcentral.com/1471-2164/16/618 |
op_rights |
Copyright 2015 Stavang et al. |
_version_ |
1766362146567880704 |