New insights into ion regulation of cephalopod molluscs: a role of epidermal ionocytes in acid-base regulation during embryogenesis

Hu, Marian Yong-An, Tseng, Yung-Che, Lin, Li-Yih, Chen, Po-Yen, Charmantier-Daures, Mireille, Hwang, Pung-Pung and Melzner, Frank (2011) New insights into ion regulation of cephalopod molluscs: a role of epidermal ionocytes in acid-base regulation during embryogenesis American Journal of Physiology: Regulatory, Integrative and Comparative Physiology, 301 (6). R1700-R1709. DOI 10.1152/ajpregu.00107.2011.

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Abstract

The constraints of an active life in a pelagic habitat led to numerous convergent morphological and physiological adaptations that enable cephalopod molluscs and teleost fishes to compete for similar resources. Here we show for the first time that such convergent developments are also found in the ontogenetic progression of ion regulatory tissues: as in teleost fish epidermal ionocytes scattered on skin and yolk sac of cephalopod embryos appear to be responsible for ionic and acid-base regulation before gill epithelia become functional. Ion and acid-base regulation is crucial in cephalopod embryos, as they are surrounded by a hypercapnic egg fluid with a pCO2 of 0.2-0.4 kPa. Epidermal ionocytes were characterized via immunohistochemistry, in situ hybridization and vital dye staining techniques. We found one group of cells that is recognized by Concavalin A and MitoTracker, which also expresses Na+/H+ exchangers (NHE) and Na+/K+-ATPase. Similar to findings obtained in teleosts these NHE3-rich cells take up sodium in exchange for protons, illustrating the energetic superiority of NHE based proton excretion in marine systems. In vivo electrophysiological techniques demonstrated that acid equivalents are secreted by the yolk and skin integument. Intriguingly, epidermal ionocytes of cephalopod embryos are ciliated as demonstrated by scanning electron microscopy suggesting a dual function of epithelial cells in water convection and ion regulation. These findings add significant knowledge to our mechanistic understanding of hypercapnia tolerance in marine organisms, as it demonstrates that marine taxa which were identified as powerful acid-base regulators during hypercapnic challenges already exhibit strong acid-base regulatory abilities during embryogenesis.

Document Type: Article
Additional Information: WOS:000298176700010
Keywords: Biogeochemistry; gill; embryonic development; mitochondrion-rich cells; squid; cuttlefish; CUTTLEFISH SEPIA-OFFICINALIS; MITOCHONDRION-RICH CELLS; COD GADUS-MORHUA; H+-ATPASE; ADENOSINE TRIPHOSPHATASE; EMBRYONIC-DEVELOPMENT; MOLECULAR-MECHANISMS; ZEBRAFISH LARVAE; TELEOST FISHES; RAINBOW-TROUT
Research affiliation: OceanRep > GEOMAR > FB3 Marine Ecology > FB3-EOE-B Experimental Ecology - Benthic Ecology
OceanRep > The Future Ocean - Cluster of Excellence
Refereed: Yes
Open Access Journal?: No
DOI etc.: 10.1152/ajpregu.00107.2011
ISSN: 0363-6119
Projects: BIOACID
Date Deposited: 05 Dec 2011 10:13
Last Modified: 25 Apr 2016 07:04
URI: http://oceanrep.geomar.de/id/eprint/12752

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