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Evidence of Positive Selection of Aquaporins Genes from Pontoporia blainvillei during the Evolutionary Process of Cetaceans.

São Pedro SL, Alves JM, Barreto AS, Lima AO - PLoS ONE (2015)

Bottom Line: Marine mammals are well adapted to their hyperosmotic environment.Several morphological and physiological adaptations for water conservation and salt excretion are known to be present in cetaceans, being responsible for regulating salt balance.Many genes have been identified to be involved in osmotic regulation, including the aquaporins.

View Article: PubMed Central - PubMed

Affiliation: Laboratório de Genética Molecular, Centro de Ciências Tecnológicas da Terra e do Mar, Universidade do Vale do Itajaí, Itajaí, SC, Brazil.

ABSTRACT

Background: Marine mammals are well adapted to their hyperosmotic environment. Several morphological and physiological adaptations for water conservation and salt excretion are known to be present in cetaceans, being responsible for regulating salt balance. However, most previous studies have focused on the unique renal physiology of marine mammals, but the molecular bases of these mechanisms remain poorly explored. Many genes have been identified to be involved in osmotic regulation, including the aquaporins. Considering that aquaporin genes were potentially subject to strong selective pressure, the aim of this study was to analyze the molecular evolution of seven aquaporin genes (AQP1, AQP2, AQP3, AQP4, AQP6, AQP7, and AQP9) comparing the lineages of cetaceans and terrestrial mammals.

Results: Our results demonstrated strong positive selection in cetacean-specific lineages acting only in the gene for AQP2 (amino acids 23, 83, 107,179, 180, 181, 182), whereas no selection was observed in terrestrial mammalian lineages. We also analyzed the changes in the 3D structure of the aquaporin 2 protein. Signs of strong positive selection in AQP2 sites 179, 180, 181, and 182 were unexpectedly identified only in the baiji lineage, which was the only river dolphin examined in this study. Positive selection in aquaporins AQP1 (45), AQP4 (74), AQP7 (342, 343, 356) was detected in cetaceans and artiodactyls, suggesting that these events are not related to maintaining water and electrolyte homeostasis in seawater.

Conclusions: Our results suggest that the AQP2 gene might reflect different selective pressures in maintaining water balance in cetaceans, contributing to the passage from the terrestrial environment to the aquatic. Further studies are necessary, especially those including other freshwater dolphins, who exhibit osmoregulatory mechanisms different from those of marine cetaceans for the same essential task of maintaining serum electrolyte balance.

No MeSH data available.


Three-dimensional mapping of positively selected AQP2 sites.A) AQP2 protein structure. Location of sites 23 (orange), 83 (red), and 107 (yellow) are highlighted. B) One subunit of AQP2 showing the location of sites 23, 83, and 107, which showed positive selection in cetaceans, colored as above. C) Superposition of the replacement of serine 107 by histidine, in the cetacean lineage.
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pone.0134516.g003: Three-dimensional mapping of positively selected AQP2 sites.A) AQP2 protein structure. Location of sites 23 (orange), 83 (red), and 107 (yellow) are highlighted. B) One subunit of AQP2 showing the location of sites 23, 83, and 107, which showed positive selection in cetaceans, colored as above. C) Superposition of the replacement of serine 107 by histidine, in the cetacean lineage.

Mentions: Positively selected sites 23, 83, and 107 were located in, or close to, the functional regions in the predicted 3D structures of the AQP2 gene (Fig 3). For instance, residue 23 involves three hydrophobic amino acids (leucine, valine, isoleucine) among the sequences analyzed. The same pattern was observed at site 83, where valine and isoleucine were present. According to McClellan & McCracken [38], the amino acids valine, leucine, and isoleucine, when located in a transmembrane domain, as in AQP2, are more susceptible to substitution among each other because that results in conservative changes. On the other hand, two polar amino acids, histidine and serine, were observed at residue 107. As previously observed [39], serine and histidine are found in 81% of active sites. Site 107 was also found to be under strong positive selection by Xu et al. [12], where it was numbered as 105.


Evidence of Positive Selection of Aquaporins Genes from Pontoporia blainvillei during the Evolutionary Process of Cetaceans.

São Pedro SL, Alves JM, Barreto AS, Lima AO - PLoS ONE (2015)

Three-dimensional mapping of positively selected AQP2 sites.A) AQP2 protein structure. Location of sites 23 (orange), 83 (red), and 107 (yellow) are highlighted. B) One subunit of AQP2 showing the location of sites 23, 83, and 107, which showed positive selection in cetaceans, colored as above. C) Superposition of the replacement of serine 107 by histidine, in the cetacean lineage.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4520692&req=5

pone.0134516.g003: Three-dimensional mapping of positively selected AQP2 sites.A) AQP2 protein structure. Location of sites 23 (orange), 83 (red), and 107 (yellow) are highlighted. B) One subunit of AQP2 showing the location of sites 23, 83, and 107, which showed positive selection in cetaceans, colored as above. C) Superposition of the replacement of serine 107 by histidine, in the cetacean lineage.
Mentions: Positively selected sites 23, 83, and 107 were located in, or close to, the functional regions in the predicted 3D structures of the AQP2 gene (Fig 3). For instance, residue 23 involves three hydrophobic amino acids (leucine, valine, isoleucine) among the sequences analyzed. The same pattern was observed at site 83, where valine and isoleucine were present. According to McClellan & McCracken [38], the amino acids valine, leucine, and isoleucine, when located in a transmembrane domain, as in AQP2, are more susceptible to substitution among each other because that results in conservative changes. On the other hand, two polar amino acids, histidine and serine, were observed at residue 107. As previously observed [39], serine and histidine are found in 81% of active sites. Site 107 was also found to be under strong positive selection by Xu et al. [12], where it was numbered as 105.

Bottom Line: Marine mammals are well adapted to their hyperosmotic environment.Several morphological and physiological adaptations for water conservation and salt excretion are known to be present in cetaceans, being responsible for regulating salt balance.Many genes have been identified to be involved in osmotic regulation, including the aquaporins.

View Article: PubMed Central - PubMed

Affiliation: Laboratório de Genética Molecular, Centro de Ciências Tecnológicas da Terra e do Mar, Universidade do Vale do Itajaí, Itajaí, SC, Brazil.

ABSTRACT

Background: Marine mammals are well adapted to their hyperosmotic environment. Several morphological and physiological adaptations for water conservation and salt excretion are known to be present in cetaceans, being responsible for regulating salt balance. However, most previous studies have focused on the unique renal physiology of marine mammals, but the molecular bases of these mechanisms remain poorly explored. Many genes have been identified to be involved in osmotic regulation, including the aquaporins. Considering that aquaporin genes were potentially subject to strong selective pressure, the aim of this study was to analyze the molecular evolution of seven aquaporin genes (AQP1, AQP2, AQP3, AQP4, AQP6, AQP7, and AQP9) comparing the lineages of cetaceans and terrestrial mammals.

Results: Our results demonstrated strong positive selection in cetacean-specific lineages acting only in the gene for AQP2 (amino acids 23, 83, 107,179, 180, 181, 182), whereas no selection was observed in terrestrial mammalian lineages. We also analyzed the changes in the 3D structure of the aquaporin 2 protein. Signs of strong positive selection in AQP2 sites 179, 180, 181, and 182 were unexpectedly identified only in the baiji lineage, which was the only river dolphin examined in this study. Positive selection in aquaporins AQP1 (45), AQP4 (74), AQP7 (342, 343, 356) was detected in cetaceans and artiodactyls, suggesting that these events are not related to maintaining water and electrolyte homeostasis in seawater.

Conclusions: Our results suggest that the AQP2 gene might reflect different selective pressures in maintaining water balance in cetaceans, contributing to the passage from the terrestrial environment to the aquatic. Further studies are necessary, especially those including other freshwater dolphins, who exhibit osmoregulatory mechanisms different from those of marine cetaceans for the same essential task of maintaining serum electrolyte balance.

No MeSH data available.