Adaptations of a deep sea scavenger: High ammonia tolerance and active NH 4 + excretion by the Pacific hagfish ( Eptatretus stoutii )

Clifford, Alexander M.; Goss, Greg G.; Wilkie, Michael P.

doi:10.1016/j.cbpa.2014.12.010

Cited by 24 publications

(25 citation statements)

References 88 publications

(108 reference statements)

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“…Deep-frozen plasma was later thawed on ice for measurement of plasma T CO2 and T Amm , using a Corning 965 CO 2 analyser (Ciba Corning Diagnostic, Halstead, Essex, UK) and an enzymatic reagent kit based on the glutamate dehydrogenase/NAD method (Raichem™ R85446, Cliniqua, San Marcos, CA, USA), respectively. In our experience, these procedures yield values identical to those obtained from freshly collected samples, and our measured control plasma ammonia and acid-base data were very close to those reported in previous studies on the same species (Clifford et al, 2015(Clifford et al, , 2017Giacomin et al, 2019). Because of background interference by hagfish plasma in the T Amm measurement, a standard curve was created using the plasma as a matrix spiked with increasing concentrations of NH 4 Cl, in order to compensate for the matrix effect.…”

Section: Blood and Water Chemistry Analysessupporting

confidence: 79%

“…The low doses using 35 mmol l −1 ammonium salts were made up in a background concentration of 500 mmol l −1 NaCl to minimize osmotic disturbance. The predicted initial concentrations (T Amm ) in hagfish plasma (14% of body mass) or extracellular fluid (ECF, 30% of body mass; Forster et al, 2001) ranged between 500 µmol l −1 (low dose) and 7142 µmol l −1 (high dose) in plasma, or 233 µmol l −1 (low dose) and 3330 µmol l −1 (high dose) in ECF, respectively; these predicted concentrations cover the T Amm range reported in plasma of Pacific hagfish after natural feeding (Wilkie et al, 2017) for the low dose and after exposure to 20 mmol l −1 HEA for the high dose (Clifford et al, 2015).…”

Section: Series Iv: Relationship Between Ventilation and Altered Bloomentioning

confidence: 72%

“…HEA) in nature. They are extremely tolerant of HEA in the laboratory (Clifford et al, 2015(Clifford et al, , 2017. Their behaviour of writhing and coiling, and releasing vast amounts of slime when disturbed, makes them difficult to work with, but recently we have developed methods for measuring ventilation in the Pacific hagfish (Eom and Wood, 2019).…”

Section: Introductionmentioning

confidence: 99%

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Ventilatory sensitivity to ammonia in the Pacific hagfish (Eptatretus stoutii), a representative of the oldest extant connection to the ancestral vertebrates

Eom

Giacomin

Clifford

et al. 2019

Journal of Experimental Biology

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Ventilatory sensitivity to ammonia occurs in teleosts, elasmobranchs and mammals. Here, we investigated whether the response is also present in hagfish. Ventilatory parameters (nostril flow, pressure amplitude, velar frequency and ventilatory index, the last representing the product of pressure amplitude and frequency), together with blood and water chemistry, were measured in hagfish exposed to either high environmental ammonia (HEA) in the external sea water or internal ammonia loading by intra-vascular injection. HEA exposure (10 mmol l −1 NH 4 HCO 3 or 10 mmol l −1 NH 4 Cl) caused a persistent hyperventilation by 3 h, but further detailed analysis of the NH 4 HCO 3 response showed that initially (within 5 min) there was a marked decrease in ventilation (80% reduction in ventilatory index and nostril flow), followed by a later 3-fold increase, by which time plasma total ammonia concentration had increased 11-fold. Thus, hyperventilation in HEA appeared to be an indirect response to internal ammonia elevation, rather than a direct response to external ammonia. HEA-mediated increases in oxygen consumption also occurred. Responses to NH 4 HCO 3 were greater than those to NH 4 Cl, reflecting greater increases over time in water pH and P NH3 in the former. Hagfish also exhibited hyperventilation in response to direct injection of isotonic NH 4 HCO 3 or NH 4 Cl solutions into the caudal sinus. In all cases where hyperventilation occurred, plasma total ammonia and P NH3 levels increased significantly, while blood acid-base status remained unchanged, indicating specific responses to internal ammonia elevation. The sensitivity of breathing to ammonia arose very early in vertebrate evolution.

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Section: Blood and Water Chemistry Analysessupporting

confidence: 79%

Section: Series Iv: Relationship Between Ventilation and Altered Bloomentioning

confidence: 72%

Section: Introductionmentioning

confidence: 99%

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Ventilatory sensitivity to ammonia in the Pacific hagfish (Eptatretus stoutii), a representative of the oldest extant connection to the ancestral vertebrates

Eom

Giacomin

Clifford

et al. 2019

Journal of Experimental Biology

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“…) was calculated as previously described (Clifford et al, 2015a) based on T Amm accumulation in the water using the following equation:…”

Section: Experimental Seriesmentioning

confidence: 99%

It's all in the gills: Evaluation of O2 uptake in Pacific hagfish refutes a major respiratory role for the skin

Clifford

Zimmer

Wood

et al. 2016

Journal of Experimental Biology

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Hagfish skin has been reported as an important site for ammonia excretion and as the major site of systemic oxygen acquisition. However, whether cutaneous O 2 uptake is the dominant route of uptake remains under debate; all evidence supporting this hypothesis has been derived using indirect measurements. Here, we used partitioned chambers and direct measurements of oxygen consumption and ammonia excretion to quantify cutaneous and branchial exchanges in Pacific hagfish (Eptatretus stoutii) at rest and following exhaustive exercise. Hagfish primarily relied on the gills for both O 2 uptake (81.0%) and ammonia excretion (70.7%). Following exercise, both O 2 uptake and ammonia excretion increased, but only across the gill; cutaneous exchange was not increased. When branchial O 2 availability was reduced by exposure to anteriorly localized hypoxia (∼4.6 kPa O 2 ), cutaneous O 2 consumption was only slightly elevated on an absolute basis. These results refute a major role for cutaneous O 2 acquisition in the Pacific hagfish.

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“…Enhanced cutaneous ammonia transport capacity in response to high ambient ammonia levels could be a disadvantage if the entire surface of the hagfish (rather than just the anterior end) is surrounded by carrion, a situation that requires consideration. Hagfish would presumably benefit from mechanisms that limit ammonia gain when the anterior end of the animal is embedded in decaying carrion, and some indications support this possibility (3,4). For example, plasma ammonia concentrations stabilize over time in hagfish exposed to high ambient ammonia levels (3) and exposure of the anterior end of the animal to high ammonia levels has little impact on plasma ammonia relative to exposing the posterior end of the animal (4).…”

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confidence: 99%

Heads you gain, tails you lose

Gilmour

2017

American Journal of Physiology-Regulatory, Integrative and Comp

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THE FIELD OF TRANSPORT PHYSIOLOGY was fundamentally changed by the discovery of transport proteins that are specific for small neutral molecules such as urea, water, ammonia, and CO 2 . The identification of first urea transporters (12), then aquaporins or water channels (1), and most recently ammonia transporters (8) (that may also facilitate the movement of CO 2 ), challenged the long-held view that membranes were relatively permeable to these small neutral molecules, which were thought to traverse a lipid bilayer directly, driven by a diffusion gradient. By contrast, the involvement of specific transport proteins suggests a far higher capacity for control over the movement of these molecules, as is the case for ions that move across membranes via protein transporters or channels. The ammoniatransporting Rhesus-associated (Rh) glycoproteins are particularly interesting in this context because they function in the transport of either or both ammonia gas NH 3 , a small neutral molecule, and the ammonium ion NH 4 ϩ (2), the two forms of ammonia that are in equilibrium with each other ("ammonia" here is used to denote total ammonia, i.e., NH 3 ϩ NH 4 ϩ ). The mammalian Rh glycoproteins belong to solute transporter family SLC42 and comprise the red blood cell-specific Rhag, as well as Rhbg and Rhcg, which exhibit broader tissue distributions including prominent expression in the kidney (9). In the kidney, Rhbg and Rhcg play a vital role in ammonia secretion and hence in the maintenance of acid-base balance, which in mammals is largely dependent on renal bicarbonate ion reabsorption and net acid excretion. Net acid excretion, in turn, reflects renal ammonia metabolism, the balance between ammoniagenesis and ammonia excretion at the kidney (9).The primary role of the kidney in maintaining acid-base balance in mammals is in fish played by the gill (6). Moreover, the multifunctional gill also serves as a key site of ionic and osmotic regulation and nitrogen waste excretion, with most fish (the sharks, skates, and rays being notable exceptions) excreting nitrogen waste predominantly as ammonia. With the identification of Rh glycoproteins in fish (7), the scene was set for a paradigm shift in our understanding of nitrogen excretion in fish and its integration with ion transport pathways and acidbase balance (10), a shift in which epithelial transport of ammonia is viewed as a regulated process rather being dependent on passive diffusion. In the ensuing years, increasing research effort has focused on the branchial expression and regulation of Rh glycoproteins in a range of fish species and in response to changes in environmental conditions. But what happens to ammonia excretion when gill function is compromised, for example in species that emerge from water onto land with a resultant collapse of gill surface area? Study of such species has revealed interesting and often unexpected solutions to the problem of ammonia excretion in terrestrial conditions, including induction of urea production and excretion of ammonia acros...

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Adaptations of a deep sea scavenger: High ammonia tolerance and active NH 4 + excretion by the Pacific hagfish ( Eptatretus stoutii )

Cited by 24 publications

References 88 publications

Ventilatory sensitivity to ammonia in the Pacific hagfish (Eptatretus stoutii), a representative of the oldest extant connection to the ancestral vertebrates

Ventilatory sensitivity to ammonia in the Pacific hagfish (Eptatretus stoutii), a representative of the oldest extant connection to the ancestral vertebrates

It's all in the gills: Evaluation of O2 uptake in Pacific hagfish refutes a major respiratory role for the skin

Heads you gain, tails you lose

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