Development in a naturally acidified environment: Na+/H+-exchanger 3-based proton secretion leads to CO2 tolerance in cephalopod embryos

Marian Y. Hu, Jay Ron Lee, Li Yih Lin, Tin Han Shih, Meike Stumpp, Mong Fong Lee, Pung Pung Hwang, Yung Che Tseng

Research output: Contribution to journalArticle

27 Citations (Scopus)

Abstract

Background: Regulation of pH homeostasis is a central feature of all animals to cope with acid-base disturbances caused by respiratory CO2. Although a large body of knowledge is available for vertebrate and mammalian pH regulatory systems, the mechanisms of pH regulation in marine invertebrates remain largely unexplored.Results: We used squid (Sepioteuthis lessoniana), which are known as powerful acid-base regulators to investigate the pH regulatory machinery with a special focus on proton secretion pathways during environmental hypercapnia. We cloned a Rhesus protein (slRhP), V-type H+-ATPase (slVHA) and the Na+/H+ exchanger 3 (slNHE3) from S. lessoniana, which are hypothesized to represent key players in proton secretion pathways among different animal taxa. Specifically designed antibodies for S. lessoniana demonstrated the sub-cellular localization of NKA, VHA (basolateral) and NHE3 (apical) in epidermal ionocytes of early life stages. Gene expression analyses demonstrated that slNHE3, slVHA and slRhP are up regulated in response to environmental hypercapnia (pH 7.31; 0.46 kPa pCO2) in body and yolk tissues compared to control conditions (pH 8.1; 0.045 kPa pCO2). This observation is supported by H+ selective electrode measurements, which detected increased proton gradients in CO2 treated embryos. This compensatory proton secretion is EIPA sensitive and thus confirms the central role of NHE based proton secretion in cephalopods.Conclusion: The present work shows that in convergence to teleosts and mammalian pH regulatory systems, cephalopod early life stages have evolved a unique acid-base regulatory machinery located in epidermal ionocytes. Using cephalopod molluscs as an invertebrate model this work provides important insights regarding the unifying evolutionary principles of pH regulation in different animal taxa that enables them to cope with CO2 induced acid-base disturbances.

Original languageEnglish
Article number51
JournalFrontiers in Zoology
Volume10
Issue number1
DOIs
Publication statusPublished - 2013 Aug 29

Fingerprint

cephalopod
Cephalopoda
secretion
protons
embryo
embryo (animal)
tolerance
acid
machinery
animal
invertebrate
disturbance
hypercapnia
H-transporting ATP synthase
acids
homeostasis
teleost
mollusc
antibody
gene expression

Keywords

  • Acid-base regulation
  • Embryonic development
  • Ocean acidification
  • Rh proteins
  • V-type H+-ATPase

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Animal Science and Zoology

Cite this

Development in a naturally acidified environment : Na+/H+-exchanger 3-based proton secretion leads to CO2 tolerance in cephalopod embryos. / Hu, Marian Y.; Lee, Jay Ron; Lin, Li Yih; Shih, Tin Han; Stumpp, Meike; Lee, Mong Fong; Hwang, Pung Pung; Tseng, Yung Che.

In: Frontiers in Zoology, Vol. 10, No. 1, 51, 29.08.2013.

Research output: Contribution to journalArticle

Hu, Marian Y. ; Lee, Jay Ron ; Lin, Li Yih ; Shih, Tin Han ; Stumpp, Meike ; Lee, Mong Fong ; Hwang, Pung Pung ; Tseng, Yung Che. / Development in a naturally acidified environment : Na+/H+-exchanger 3-based proton secretion leads to CO2 tolerance in cephalopod embryos. In: Frontiers in Zoology. 2013 ; Vol. 10, No. 1.
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