Beyond bouyancy and vision: The potential for the root effect to facilitate oxygen delivery to tissues other than the swim bladder and eye (original) (raw)
Related papers
A unique mode of tissue oxygenation and the adaptive radiation of teleost fishes
Journal of Experimental Biology, 2014
Teleost fishes constitute 95% of extant aquatic vertebrates, and we suggest that this is related in part to their unique mode of tissue oxygenation. We propose the following sequence of events in the evolution of their oxygen delivery system. First, loss of plasmaaccessible carbonic anhydrase (CA) in the gill and venous circulations slowed the Jacobs-Stewart cycle and the transfer of acid between the plasma and the red blood cells (RBCs). This ameliorated the effects of a generalised acidosis (associated with an increased capacity for burst swimming) on haemoglobin (Hb)-O 2 binding. Because RBC pH was uncoupled from plasma pH, the importance of Hb as a buffer was reduced. The decrease in buffering was mediated by a reduction in the number of histidine residues on the Hb molecule and resulted in enhanced coupling of O 2 and CO 2 transfer through the RBCs. In the absence of plasma CA, nearly all plasma bicarbonate ultimately dehydrated to CO 2 occurred via the RBCs, and chloride/bicarbonate exchange was the rate-limiting step in CO 2 excretion. This pattern of CO 2 excretion across the gills resulted in disequilibrium states for CO 2 hydration/dehydration reactions and thus elevated arterial and venous plasma bicarbonate levels. Plasma-accessible CA embedded in arterial endothelia was retained, which eliminated the localized bicarbonate disequilibrium forming CO 2 that then moved into the RBCs. Consequently, RBC pH decreased which, in conjunction with pH-sensitive Bohr/Root Hbs, elevated arterial oxygen tensions and thus enhanced tissue oxygenation. Counter-current arrangement of capillaries (retia) at the eye and later the swim bladder evolved along with the gas gland at the swim bladder. Both arrangements enhanced and magnified CO 2 and acid production and, therefore, oxygen secretion to those specialised tissues. The evolution of -adrenergically stimulated RBC Na + /H + exchange protected gill O 2 uptake during stress and further augmented plasma disequilibrium states for CO 2 hydration/dehydration. Finally, RBC organophosphates (e.g. NTP) could be reduced during hypoxia to further increase Hb-O 2 affinity without compromising tissue O 2 delivery because high-affinity Hbs could still adequately deliver O 2 to the tissues via Bohr/Root shifts. We suggest that the evolution of this unique mode of tissue O 2 transfer evolved in the Triassic/Jurassic Period, when O 2 levels were low, ultimately giving rise to the most extensive adaptive radiation of extant vertebrates, the teleost fishes. . Effects of anaerobic exercise accompanying catch-and-release fishing on blood-oxygen affinity of the sandbar shark (Carcharhinus plumbeus, Nardo). . Oxygen transport and cardiovascular responses in skipjack tuna (Katsuwonus pelamis) and yellowfin tuna (Thunnus albacares) exposed to acute hypoxia.
High blood oxygen affinity in the air-breathing swamp eel Monopterus albus
Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 2014
The Asian swamp eel (Monopterus albus, Zuiew 1793) is a facultative air-breathing fish with reduced gills. Previous studies have shown that gas exchange seems to occur across the epithelium of the buccopharyngeal cavity, the esophagus and the integument, resulting in substantial diffusion limitations that must be compensated by adaptations in others steps of the O 2 transport system to secure adequate O 2 delivery to the respiring tissues. We therefore investigated O 2 binding properties of whole blood, stripped hemoglobin (Hb), two major isoHb components and the myoglobin (Mb) from M. albus. Whole blood was sampled using indwelling catheters for blood gas analysis and determination of O 2 equilibrium curves. Hb was purified to assess the effects of endogenous allosteric effectors, and Mb was isolated from heart and skeletal muscle to determine its O 2 binding properties. The blood of M. albus has a high O 2 carrying capacity [hematocrit (Hct) of 42.4 ± 4.5%] and binds O 2 with an unusually high affinity (P 50 = 2.8 ± 0.4 mmHg at 27°C and pH 7.7), correlating with insensitivity of the Hb to the anionic allosteric effectors that normally decrease Hb-O 2 affinity. In addition, Mb is present at high concentrations in both heart and muscle (5.16 ± 0.99 and 1.08 ± 0.19 mg • g wet tissue -1 , respectively). We suggest that the high Hct and high blood O 2 affinity serve to overcome the low diffusion capacity in the relatively inefficient respiratory surfaces, while high Hct and Mb concentration aid in increasing the O 2 flux from the blood to the muscles.
The interaction between oxygen and carbon dioxide movements in fishes
Comparative Biochemistry and Physiology Part A: Physiology, 1996
Many teleost fishes have haemoglobins which possess a Root effect, a large Haldane effect and a low buffer capacity. This combination of characteristics influences the interaction between movements of oxygen and carbon dioxide in the red cell, in the respiratory epithelium, and in the tissues. The presence of the Root effect may limit oxygen uptake at the gills due to an accumulation of Bohr protons released upon oxygenation. However, the Root effect is probably important in maintaining or elevating blood PO, during muscle capillary transit, enhancing oxygen delivery to the tissues. Bohr protons are reversibly bound to haemoglobin. The release of Bohr protons during oxygenation facilitates bicarbonate dehydration at the gills, while Bohr proton binding facilitates CO, hydration at the tissues. In some teleost fishes, most of the Bohr protons are released and bound to haemoglobin, between 50 and 100% of haemoglobin-oxygen saturation (27). This trait is probably significant in maximizing oxygen uptake at the gills and in conserving body CO2 stores during exposure to hypoxia and exercise, when the lower reaches of the haemoglobin-oxygen equilibrium curve are used. COMP BIOCHEM PHYSIOL 113A;1:83-90, 1996.
Functional support for a novel mechanism that enhances tissue oxygen extraction in a teleost fish
Proceedings of The Royal Society B: Biological Sciences, 2019
A successful spawning migration in salmon depends on their athletic ability, and thus on efficient cardiovascular oxygen (O 2) transport. Most teleost fishes have highly pH-sensitive haemoglobins (Hb) that can release large amounts of O 2 when the blood is acidified at the tissues. We hypothesized that plasma-accessible carbonic anhydrase (paCA; the enzyme that catalyses proton production from CO 2) is required to acidify the blood at the tissues and promote tissue O 2 extraction. Previous studies have reported an elevated tissue O 2 extraction in hypoxia-acclimated teleosts that may also be facilitated by paCA. Thus, to create experimental contrasts in tissue O 2 extraction, Atlantic salmon were acclimated to normoxia or hypoxia (40% air saturation for more than six weeks), and the role of paCA in enhancing tissue O 2 extraction was tested by inhibiting paCA at rest and during submaximal exercise. Our results show that: (i) in both acclimation groups, the inhibition of paCA increased cardiac output by one-third, indicating a role of paCA in promoting tissue O 2 extraction during exercise, recovery and at rest; (ii) the recruitment of paCA was plastic and increased following hypoxic acclimation; and (iii) maximal exercise performance in salmon, and thus a successful spawning migration, may not be possible without paCA.
The Odyssey of Atmospheric Oxygen in their Futile Attempt to Reach the Interior of the Cell
It is possible that the contradictions that emerge when contrasting hypotheses about gas exchange in the lungs with different clinical and experimental findings in both pulmonary and systemic diseases can be solved if we modify in our mind the role of atmospheric oxygen as the main source of oxygen in the blood and take into account both the intrinsic property of melanin to dissociate and re-form the water molecule which is the true source of intracellular molecular oxygen and also the intrinsic property of hemoglobin to dissociate the water molecule that is a significant contributor of oxygen levels in blood. Recall that chlorophyll and hemoglobin are virtually identical, as is the Mg the prosthetic group in chlorophyll and Fe in hemoglobin; another difference is that chlorophyll has a non-polar end that serves to bind to the chloroplast.
2001
Some teleost fishes exhibit a non-linear release of H + with haemoglobin oxygen saturation (SO 2 ) in whole blood that may be related to the Root effect and a low apparent cooperativity in oxygen binding. To further investigate this correlation, the relationship between red cell pH (pH i ) and SO 2 was evaluated in two teleost fishes, the carp (Cyprinus carpio) and tambaqui (Colossoma macropomum). Carp possess a relatively small Root effect within the physiological pH range, while that in tambaqui is relatively large. It was therefore hypothesized that both species would possess a non-linear release of H + with SO 2 under in vivo conditions, but that the degree of non-linearity would be less pronounced in carp than in tambaqui. Red cell suspensions of tambaqui showed a marked non-linear relationship between pH i and SO 2 at in vivo pH values (pH e = 7.66), where the majority of Bohr protons were released between 50 and 100% SO 2 . In whole blood of carp, the relationship between pH i and SO 2 was almost linear at normal resting extracellular pH values (pH e = 8.10) where Hills n 50 (cooperativity) was 1.3. Under acidic conditions (pH e = 7.11), n 50 decreased to 0.9 and the release of H + with SO 2 became slightly non-linear. The reduction in pH in carp blood was associated with the onset of the Root effect, and the oxygen tension at half saturation (P 50 ) increased from 3.8 to 38.2 mmHg. The relationship between total CO 2 and SO 2 in carp whole blood changed from being almost linear at pH e 8.1 to being non-linear at pH e 7.1, consistent with the relationship between pH i and SO 2 . Thus, possession of a Root effect could be a prerequisite for a non-linear release of Bohr protons with oxygenation, but the expression in whole blood may depend upon a species-specific cooperativity threshold. The non-linear release of Bohr protons with oxygenation may be a general phenomenon in teleosts with important implications for gas transport and acid-base homeostasis.
The Journal of experimental biology, 1997
Two major strategies are apparent for the regulation of gas transport by vertebrate blood except in the myxinoids, which seem to have little scope for such regulation. In lampreys and teleost fish, haemoglobins have low buffering capacities and large Bohr/Haldane effects. Na+/H+ exchange plays an important role in the control of haemoglobin oxygen-affinity in these vertebrate groups. The large Bohr/Haldane effect also facilitates carbon dioxide transport: the blood (or erythrocyte) pH increases upon deoxygenation, thus increasing the concentration of bicarbonate formed at a given carbon dioxide tension. In lampreys, the bicarbonate permeability of the erythrocyte membrane is low. As a consequence, extracellular acid loads cannot be buffered by haemoglobin. In contrast, teleost erythrocytes possess a functional anion exchange, allowing extracellular proton loads to be buffered by haemoglobin. However, because the buffering capacity of teleost haemoglobins is low, buffering of extrace...