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

Marian Y. Hu, Ying Jey Guh, Meike Stumpp, Jay Ron Lee, Ruo Dong Chen, Po Hsuan Sung, Yu Chi Chen, Pung Pung Hwang, Yung-Che Tseng

Research output: Contribution to journalArticle

28 Citations (Scopus)

Abstract

Background: Cephalopods have evolved strong acid-base regulatory abilities to cope with CO2 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, NH4 + 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 HCO3 - 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+/HCO3 - 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 NH4 + 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.

Original languageEnglish
Article number55
JournalFrontiers in Zoology
Volume11
Issue number1
DOIs
Publication statusPublished - 2014 Aug 6

Fingerprint

Cephalopoda
squid
energy metabolism
acidification
H-transporting ATP synthase
seawater
metabolism
cephalopod
acid-base balance
acids
acid
energy
protein
proteins
Sepiidae
sodium-potassium-exchanging ATPase
active transport
carbonate dehydratase
immunocytochemistry
energetics

Keywords

  • Acid-base regulation
  • Invertebrate
  • Metabolism
  • Ocean acidification
  • Rh proteins

ASJC Scopus subject areas

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

Cite this

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.

In: Frontiers in Zoology, Vol. 11, No. 1, 55, 06.08.2014.

Research output: Contribution to journalArticle

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. In: Frontiers in Zoology. 2014 ; Vol. 11, No. 1.
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abstract = "Background: Cephalopods have evolved strong acid-base regulatory abilities to cope with CO2 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, NH4 + 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 HCO3 - 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+/HCO3 - 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 NH4 + 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.",
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AU - Guh, Ying Jey

AU - Stumpp, Meike

AU - Lee, Jay Ron

AU - Chen, Ruo Dong

AU - Sung, Po Hsuan

AU - Chen, Yu Chi

AU - Hwang, Pung Pung

AU - Tseng, Yung-Che

PY - 2014/8/6

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N2 - Background: Cephalopods have evolved strong acid-base regulatory abilities to cope with CO2 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, NH4 + 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 HCO3 - 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+/HCO3 - 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 NH4 + 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.

AB - Background: Cephalopods have evolved strong acid-base regulatory abilities to cope with CO2 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, NH4 + 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 HCO3 - 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+/HCO3 - 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 NH4 + 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.

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KW - Invertebrate

KW - Metabolism

KW - Ocean acidification

KW - Rh proteins

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