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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Main Authors: 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
Format: Article
Language:English
Published: Frontiers Media S.A. 2016-02-01
Series:Frontiers in Physiology
Subjects:
Online Access:http://journal.frontiersin.org/Journal/10.3389/fphys.2016.00014/full
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spelling 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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