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

Hu, Marian Yong-An; Guh, Ying Jey; Stumpp, Meike; Lee, Jay Ron; Chen, Ruo Dong; Sung, Po Hsuan; Chen, Shen‐Ming; Hwang, Pung Pung; Tseng, Yung‐Che

doi:10.1186/s12983-014-0055-z

Cited by 35 publications

(76 citation statements)

References 69 publications

(137 reference statements)

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“…The compensation reaction happens within few hours and can lead to a partial compensation in S. officinalis accompanied by an increase in blood [HCO 3 ¡ ] from 3.4 to 10.4 mM 13 or a full compensation of blood pH as found in S. lessoniana with an increase in blood [HCO 3 ¡ ] from 2.3 to 4.3 mM. 12 Although acid-base regulatory abilities of cephalopods were investigated in great detail, 10,11,13 the responsible organs and mechanistic basis for extracellular pH regulation were just recently identified and characterized.…”

Section: Acid-base Physiology In Marine Vertebrates and Invertebratesmentioning

confidence: 99%

“…38 Additionally, recent studies provided compelling evidence that the NKA of cephalopods is also a major player in regulating acid-base homeostasis. 12,49 In cephalopods including squid, cuttlefish and octopus, the NKA is present in high concentrations in gill epithelia located in basolateral membranes providing an electrochemical gradient that is used by a variety of secondary active transporters and ion channels.…”

Section: The Ph Regulatory Machinerymentioning

confidence: 99%

“…Immunohistochemical analyses using antibodies specifically designed for squid (S. lessoniana) VHA could demonstrate that also in cephalopods the VHA is restricted to basolateral membranes in gill epithelia as well as epidermal ionocytes of embryonic stages. 12,89 Interestingly, positive VHA immunoractivity was additionally found in pilaster (or pillar) cells spanning through the blood sinus between the inner and the outer epithelium of the cephalopod gill. Expression studies demonstrated an up-regulation of the VHA (summarized in Table 1) in response to hypercapnia (acidification) indicating that this enzyme must be involved in regulating pH homeostasis during hypercapnic exposure in cephalopods.…”

Section: The Ph Regulatory Machinerymentioning

confidence: 99%

“…It was suggested that the basolateral orientation of the VHA in ionocytes and gill epithelia, as well as its expression in pillar cells may contribute to a local acidification of the blood to optimize gas exchange and/or facilitate the formation of the ammonium ion (NH 4 C ) that can be used as an alternative substrate by the NKA. 12 To date little information exists regarding the function of branchial pillar cells in aquatic organisms. Pillar cells characterized by high concentrations of Figure 4.…”

Section: The Ph Regulatory Machinerymentioning

confidence: 99%

“…To accommodate such temporal pH fluctuations cephalopods have evolved moderate to strong acid-base regulatory abilities to stabilize blood pH during exercise and hypercapnic exposure. [11][12][13] Accordingly, well developed acid-base regulatory abilities seem to represent another feature that underlines the convergence of cephalopods and other active marine organisms including fish and crustaceans.…”

Section: Introductionmentioning

confidence: 99%

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Recent advances in understanding trans-epithelial acid-base regulation and excretion mechanisms in cephalopods

Hwang

Tseng

2015

Tissue Barriers

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Cephalopods have evolved complex sensory systems and an active lifestyle to compete with fish for similar resources in the marine environment. Their highly active lifestyle and their extensive protein metabolism has led to substantial acid-base regulatory abilities enabling these organisms to cope with CO 2 induced acid-base disturbances. In convergence to teleost, cephalopods possess an ontogeny-dependent shift in ion-regulatory epithelia with epidermal ionocytes being the major site of embryonic acid-base regulation and ammonia excretion, while gill epithelia take these functions in adults. Although the basic morphology and excretory function of gill epithelia in cephalopods were outlined almost half a century ago, modern immunohistological and molecular techniques are bringing new insights to the mechanistic basis of acidbase regulation and excretion of nitrogenous waste products (e.g. NH 3 /NH 4 C ) across ion regulatory epithelia of cephalopods. Using cephalopods as an invertebrate model, recent findings reveal partly conserved mechanisms but also novel aspects of acid-base regulation and nitrogen excretion in these exclusively marine animals. Comparative studies using a range of marine invertebrates will create a novel and exciting research direction addressing the evolution of pH regulatory and excretory systems.

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Section: Acid-base Physiology In Marine Vertebrates and Invertebratesmentioning

confidence: 99%

Section: The Ph Regulatory Machinerymentioning

confidence: 99%

Section: The Ph Regulatory Machinerymentioning

confidence: 99%

Section: The Ph Regulatory Machinerymentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Recent advances in understanding trans-epithelial acid-base regulation and excretion mechanisms in cephalopods

Hwang

Tseng

2015

Tissue Barriers

Self Cite

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Dose-dependence and small-scale variability in responses to ocean acidification during squid, Doryteuthis pealeii, development

2019

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Coastal squids lay their eggs on the benthos, leaving them to develop in a dynamic system that is undergoing rapid acidification due to human influence. Prior studies have broadly investigated the impacts of ocean acidification on embryonic squid, but have not addressed the thresholds at which these responses occur or their potential variability. We raised squid, Doryteuthis pealeii (captured in Vineyard Sound, Massachusetts, USA: 41° 23.370N 70° 46.418´W), eggs in three trials across the breeding season (May-September, 2013) in a total of six chronic pCO 2 exposures (400, 550, 850, 1300, 1900, and 2200 ppm). Hatchlings were counted and subsampled for mantle length, yolk volume, hatching time, hatching success, and statolith morphology. New methods for analysis of statolith shape, rugosity, and surface degradation were developed and are presented (with code). Responses to acidification (e.g., reduced mantle lengths, delayed hatching, and smaller, more degraded statoliths) were evident at ~ 1300 ppm CO 2. However, patterns of physiological response and energy management, based on comparisons of yolk consumption and growth, varied among trials. Interactions between pCO 2 and hatching day indicated a potential influence of exposure time on responses, while interactions with culture vessel highlighted the substantive natural variability within a clutch of eggs. While this study is consistent with, and expands upon, previous findings of sensitivity of the early life stages to acidification, it also highlights the plasticity and potential for resilience in this population of squid.

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Intracellular pH regulation in mantle epithelial cells of the Pacific oyster, Crassostrea gigas

Ramesh

Melzner

et al. 2020

J Comp Physiol B

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Shell formation and repair occurs under the control of mantle epithelial cells in bivalve molluscs. However, limited information is available on the precise acid–base regulatory machinery present within these cells, which are fundamental to calcification. Here, we isolate mantle epithelial cells from the Pacific oyster, Crassostrea gigas and utilise live cell imaging in combination with the fluorescent dye, BCECF-AM to study intracellular pH (pHi) regulation. To elucidate the involvement of various ion transport mechanisms, modified seawater solutions (low sodium, low bicarbonate) and specific inhibitors for acid–base proteins were used. Diminished pH recovery in the absence of Na+ and under inhibition of sodium/hydrogen exchangers (NHEs) implicate the involvement of a sodium dependent cellular proton extrusion mechanism. In addition, pH recovery was reduced under inhibition of carbonic anhydrases. These data provide the foundation for a better understanding of acid–base regulation underlying the physiology of calcification in bivalves.

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

Cited by 35 publications

References 69 publications

Recent advances in understanding trans-epithelial acid-base regulation and excretion mechanisms in cephalopods

Recent advances in understanding trans-epithelial acid-base regulation and excretion mechanisms in cephalopods

Dose-dependence and small-scale variability in responses to ocean acidification during squid, Doryteuthis pealeii, development

Intracellular pH regulation in mantle epithelial cells of the Pacific oyster, Crassostrea gigas

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