Strong ion regulatory abilities enable the crab Xenograpsus testudinatus to inhabit highly acidified marine vent systems
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 environm...
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doaj-cab68447022c4ba3b73997e1977bf5f62020-11-24T22:35:06ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2016-02-01710.3389/fphys.2016.00014163595Strong ion regulatory abilities enable the crab Xenograpsus testudinatus to inhabit highly acidified marine vent systemsMarian Yong-An Hu0Marian Yong-An Hu1Ying-Jey eGuh2Yi-Ta eShao3Pou-Long eKuan4Guan-Lin eChen5Jay-Ron eLee6Ming-Shiou eJeng7Yung-Che eTseng8Christian-Albrechts University KielAcademia SinicaAcademia SinicaNational Taiwan Ocean UniversityNational Taiwan Normal UniversityNational Taiwan Normal UniversityAcademia SinicaAcademia SinicaNational Taiwan Normal UniversityHydrothermal 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 HCO3- levels from 8.8 ± 0.3 mM 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.http://journal.frontiersin.org/Journal/10.3389/fphys.2016.00014/fullHypercapniacrustaceangillInvertebrate physiologyNa+/K+-ATPasehydrothermal vent |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Marian Yong-An Hu Marian Yong-An Hu Ying-Jey eGuh Yi-Ta eShao Pou-Long eKuan Guan-Lin eChen Jay-Ron eLee Ming-Shiou eJeng Yung-Che eTseng |
spellingShingle |
Marian Yong-An Hu Marian Yong-An Hu Ying-Jey eGuh Yi-Ta eShao Pou-Long eKuan Guan-Lin eChen Jay-Ron eLee Ming-Shiou eJeng Yung-Che eTseng Strong ion regulatory abilities enable the crab Xenograpsus testudinatus to inhabit highly acidified marine vent systems Frontiers in Physiology Hypercapnia crustacean gill Invertebrate physiology Na+/K+-ATPase hydrothermal vent |
author_facet |
Marian Yong-An Hu Marian Yong-An Hu Ying-Jey eGuh Yi-Ta eShao Pou-Long eKuan Guan-Lin eChen Jay-Ron eLee Ming-Shiou eJeng Yung-Che eTseng |
author_sort |
Marian Yong-An Hu |
title |
Strong ion regulatory abilities enable the crab Xenograpsus testudinatus to inhabit highly acidified marine vent systems |
title_short |
Strong ion regulatory abilities enable the crab Xenograpsus testudinatus to inhabit highly acidified marine vent systems |
title_full |
Strong ion regulatory abilities enable the crab Xenograpsus testudinatus to inhabit highly acidified marine vent systems |
title_fullStr |
Strong ion regulatory abilities enable the crab Xenograpsus testudinatus to inhabit highly acidified marine vent systems |
title_full_unstemmed |
Strong ion regulatory abilities enable the crab Xenograpsus testudinatus to inhabit highly acidified marine vent systems |
title_sort |
strong ion regulatory abilities enable the crab xenograpsus testudinatus to inhabit highly acidified marine vent systems |
publisher |
Frontiers Media S.A. |
series |
Frontiers in Physiology |
issn |
1664-042X |
publishDate |
2016-02-01 |
description |
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 HCO3- levels from 8.8 ± 0.3 mM 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. |
topic |
Hypercapnia crustacean gill Invertebrate physiology Na+/K+-ATPase hydrothermal vent |
url |
http://journal.frontiersin.org/Journal/10.3389/fphys.2016.00014/full |
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