Abstract
Hydrothermal vent organisms have evolved physiological adaptations to cope with extreme abiotic conditions including temperature and pH. To date, acid-base regulatory abilities of vent organisms are poorly investigated, although this physiological feature is essential for survival in low pH environments. We report the acid-base regulatory mechanisms of a hydrothermal vent crab, Xenograpsus testudinatus, endemic to highly acidic shallow-water vent habitats with average environment pH-values ranging between 5.4 and 6.6. Within a few hours, X. testudinatus restores extracellular pH (pHe) in response to environmental acidification of pH 6.5 (1.78 kPa pCO2) accompanied by an increase in blood levels from 8.8 ± 0.3 to 31 ± 6 mM. Branchial Na+/K+-ATPase (NKA) and V-type H+-ATPase (VHA), the major ion pumps involved in branchial acid-base regulation, showed dynamic increases in response to acidified conditions on the mRNA, protein and activity level. Immunohistochemical analyses demonstrate the presence of NKA in basolateral membranes, whereas the VHA is predominantly localized in cytoplasmic vesicles of branchial epithelial- and pillar-cells. X. testudinatus is closely related to other strong osmo-regulating brachyurans, which is also reflected in the phylogeny of the NKA. Accordingly, our results suggest that the evolution of strong ion regulatory abilities in brachyuran crabs that allowed the occupation of ecological niches in euryhaline, freshwater, and terrestrial habitats are probably also linked to substantial acid-base regulatory abilities. This physiological trait allowed X. testudinatus to successfully inhabit one of the world's most acidic marine environments.
Highlights
Deep sea hydrothermal vent systems support ecosystems with an enormous biomass, and reveal a rich biodiversity ranging from microbes to vertebrates (Tunnicliffe, 1992)
As gills were demonstrated to be the major site for ion and acid-base regulation in decapod crustaceans, (Henry et al, 2012) the following paragraph focuses on the branchial mechanisms that mediate extracellular acid-base balance in the hydrothermal vent crab X. testudinatus
Strong acid-base regulatory abilities of X. testudinatus can be regarded an essential feature of this species to successfully inhabit a highly acidic hydrothermal vent environment
Summary
Deep sea hydrothermal vent systems support ecosystems with an enormous biomass, and reveal a rich biodiversity ranging from microbes to vertebrates (Tunnicliffe, 1992). Acidified conditions due to the release of HCl and CO2 are a characteristic of most seafloor vent systems including the shallow-water hydrothermal vent system of Kueishan Island (24◦50′N, 121◦57′E), off the coast of Taiwan (Han et al, 2014). Even in the surrounding areas with depths between 2 and 14 m, the seawater is highly acidic ranging from pH 6.6 to 5.4 (Han et al, 2014) This challenging hydrothermal vent habitat is inhabited by Xenograpsus testudinatus, a crab species that is endemic to shallow-water (
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