Branchial NH4 +-dependent acid–base transport mechanisms and energy metabolism of squid (Sepioteuthis lessoniana) affected by seawater acidification

Abstract Background Cephalopods have evolved strong acid–base regulatory abilities to cope with CO 2 induced pH fluctuations in their extracellular compartments to protect gas transport via highly pH sensitive hemocyanins. To date, the mechanistic basis of branchial acid–base regulation in cephalopo...

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Main Authors: Hu, Marian Y, Guh, Ying-Jey, Stumpp, Meike, Lee, Jay-Ron, Chen, Ruo-Dong, Sung, Po-Hsuan, Chen, Yu-Chi, Hwang, Pung-Pung, Tseng, Yung-Che
Format: Other/Unknown Material
Language:English
Published: BioMed Central Ltd. 2014
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Online Access:http://www.frontiersinzoology.com/content/11/1/55
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spelling ftbiomed:oai:biomedcentral.com:s12983-014-0055-z 2023-05-15T17:52:03+02:00 Branchial NH4 +-dependent acid–base transport mechanisms and energy metabolism of squid (Sepioteuthis lessoniana) affected by seawater acidification Hu, Marian Y Guh, Ying-Jey Stumpp, Meike Lee, Jay-Ron Chen, Ruo-Dong Sung, Po-Hsuan Chen, Yu-Chi Hwang, Pung-Pung Tseng, Yung-Che 2014-08-06 http://www.frontiersinzoology.com/content/11/1/55 en eng BioMed Central Ltd. http://www.frontiersinzoology.com/content/11/1/55 Copyright 2014 Hu et al. Acid–base regulation Invertebrate Metabolism Ocean acidification Rh proteins Research 2014 ftbiomed 2014-08-10T00:36:27Z Abstract Background Cephalopods have evolved strong acid–base regulatory abilities to cope with CO 2 induced pH fluctuations in their extracellular compartments to protect gas transport via highly pH sensitive hemocyanins. To date, the mechanistic basis of branchial acid–base regulation in cephalopods is still poorly understood, and associated energetic limitations may represent a critical factor in high power squids during prolonged exposure to seawater acidification. Results The present work used adult squid Sepioteuthis lessoniana to investigate the effects of short-term (few hours) to medium-term (up to 168 h) seawater acidification on pelagic squids. Routine metabolic rates, NH 4 + excretion, extracellular acid–base balance were monitored during exposure to control (pH 8.1) and acidified conditions of pH 7.7 and 7.3 along a period of 168 h. Metabolic rates were significantly depressed by 40% after exposure to pH 7.3 conditions for 168 h. Animals fully restored extracellular pH accompanied by an increase in blood HCO 3 − levels within 20 hours. This compensation reaction was accompanied by increased transcript abundance of branchial acid–base transporters including V-type H + -ATPase (VHA), Rhesus protein (RhP), Na + /HCO 3 − cotransporter (NBC) and cytosolic carbonic anhydrase (CAc). Immunocytochemistry demonstrated the sub-cellular localization of Na + /K + -ATPase (NKA), VHA in basolateral and Na + /H + -exchanger 3 (NHE3) and RhP in apical membranes of the ion-transporting branchial epithelium. Branchial VHA and RhP responded with increased mRNA and protein levels in response to acidified conditions indicating the importance of active NH 4 + transport to mediate acid–base balance in cephalopods. Conclusion The present work demonstrated that cephalopods have a well developed branchial acid–base regulatory machinery. However, pelagic squids that evolved a lifestyle at the edge of energetic limits are probably more sensitive to prolonged exposure to acidified conditions compared to their more sluggish relatives including cuttlefish and octopods. Other/Unknown Material Ocean acidification BioMed Central
institution Open Polar
collection BioMed Central
op_collection_id ftbiomed
language English
topic Acid–base regulation
Invertebrate
Metabolism
Ocean acidification
Rh proteins
spellingShingle Acid–base regulation
Invertebrate
Metabolism
Ocean acidification
Rh proteins
Hu, Marian Y
Guh, Ying-Jey
Stumpp, Meike
Lee, Jay-Ron
Chen, Ruo-Dong
Sung, Po-Hsuan
Chen, Yu-Chi
Hwang, Pung-Pung
Tseng, Yung-Che
Branchial NH4 +-dependent acid–base transport mechanisms and energy metabolism of squid (Sepioteuthis lessoniana) affected by seawater acidification
topic_facet Acid–base regulation
Invertebrate
Metabolism
Ocean acidification
Rh proteins
description Abstract Background Cephalopods have evolved strong acid–base regulatory abilities to cope with CO 2 induced pH fluctuations in their extracellular compartments to protect gas transport via highly pH sensitive hemocyanins. To date, the mechanistic basis of branchial acid–base regulation in cephalopods is still poorly understood, and associated energetic limitations may represent a critical factor in high power squids during prolonged exposure to seawater acidification. Results The present work used adult squid Sepioteuthis lessoniana to investigate the effects of short-term (few hours) to medium-term (up to 168 h) seawater acidification on pelagic squids. Routine metabolic rates, NH 4 + excretion, extracellular acid–base balance were monitored during exposure to control (pH 8.1) and acidified conditions of pH 7.7 and 7.3 along a period of 168 h. Metabolic rates were significantly depressed by 40% after exposure to pH 7.3 conditions for 168 h. Animals fully restored extracellular pH accompanied by an increase in blood HCO 3 − levels within 20 hours. This compensation reaction was accompanied by increased transcript abundance of branchial acid–base transporters including V-type H + -ATPase (VHA), Rhesus protein (RhP), Na + /HCO 3 − cotransporter (NBC) and cytosolic carbonic anhydrase (CAc). Immunocytochemistry demonstrated the sub-cellular localization of Na + /K + -ATPase (NKA), VHA in basolateral and Na + /H + -exchanger 3 (NHE3) and RhP in apical membranes of the ion-transporting branchial epithelium. Branchial VHA and RhP responded with increased mRNA and protein levels in response to acidified conditions indicating the importance of active NH 4 + transport to mediate acid–base balance in cephalopods. Conclusion The present work demonstrated that cephalopods have a well developed branchial acid–base regulatory machinery. However, pelagic squids that evolved a lifestyle at the edge of energetic limits are probably more sensitive to prolonged exposure to acidified conditions compared to their more sluggish relatives including cuttlefish and octopods.
format Other/Unknown Material
author Hu, Marian Y
Guh, Ying-Jey
Stumpp, Meike
Lee, Jay-Ron
Chen, Ruo-Dong
Sung, Po-Hsuan
Chen, Yu-Chi
Hwang, Pung-Pung
Tseng, Yung-Che
author_facet Hu, Marian Y
Guh, Ying-Jey
Stumpp, Meike
Lee, Jay-Ron
Chen, Ruo-Dong
Sung, Po-Hsuan
Chen, Yu-Chi
Hwang, Pung-Pung
Tseng, Yung-Che
author_sort Hu, Marian Y
title Branchial NH4 +-dependent acid–base transport mechanisms and energy metabolism of squid (Sepioteuthis lessoniana) affected by seawater acidification
title_short Branchial NH4 +-dependent acid–base transport mechanisms and energy metabolism of squid (Sepioteuthis lessoniana) affected by seawater acidification
title_full Branchial NH4 +-dependent acid–base transport mechanisms and energy metabolism of squid (Sepioteuthis lessoniana) affected by seawater acidification
title_fullStr Branchial NH4 +-dependent acid–base transport mechanisms and energy metabolism of squid (Sepioteuthis lessoniana) affected by seawater acidification
title_full_unstemmed Branchial NH4 +-dependent acid–base transport mechanisms and energy metabolism of squid (Sepioteuthis lessoniana) affected by seawater acidification
title_sort branchial nh4 +-dependent acid–base transport mechanisms and energy metabolism of squid (sepioteuthis lessoniana) affected by seawater acidification
publisher BioMed Central Ltd.
publishDate 2014
url http://www.frontiersinzoology.com/content/11/1/55
genre Ocean acidification
genre_facet Ocean acidification
op_relation http://www.frontiersinzoology.com/content/11/1/55
op_rights Copyright 2014 Hu et al.
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