A unique mode of tissue oxygenation and the adaptive radiation of teleost fishes

@article{Randall2014AUM,
  title={A unique mode of tissue oxygenation and the adaptive radiation of teleost fishes},
  author={D. Randall and J. Rummer and J. M. Wilson and S. Wang and C. Brauner},
  journal={Journal of Experimental Biology},
  year={2014},
  volume={217},
  pages={1205 - 1214}
}
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 plasma-accessible 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… Expand
The O2 and CO2 Transport System in Teleosts and the Specialized Mechanisms That Enhance Hb–O2 Unloading to Tissues
TLDR
A novel mechanism of enhanced Hb–O2 unloading in teleosts is described and discussed, one that relies on the heterogeneous distribution of plasma-accessible carbonic anhydrase (PACA), an intrinsic characteristic of the cardiovascular system, and a vastly understudied area not only in fishes. Expand
Beyond just hemoglobin: Red blood cell potentiation of hemoglobin-oxygen unloading in fish.
TLDR
Although data are limited, these attributes may be general characteristics of teleosts and the generation and elimination of pH disequilibrium states at the RBC will likely enhance Hb-O2 unloading to some degree in other vertebrates. Expand
Root Effect Haemoglobins in Fish May Greatly Enhance General Oxygen Delivery Relative to Other Vertebrates
TLDR
These characteristics may be central to performance of athletic fish species such as salmonids, but may indicate that general tissue oxygen delivery may have been the incipient function of Root effect Hbs in fish, a trait strongly associated with the adaptive radiation of teleosts. Expand
Functional support for a novel mechanism that enhances tissue oxygen extraction in a teleost fish
TLDR
Results show that maximal exercise performance in salmon, and thus a successful spawning migration, may not be possible without paCA, and the recruitment of paCA was plastic and increased following hypoxic acclimation. Expand
Teleost red blood cells actively enhance the passive diffusion of oxygen that was discovered by August Krogh.
  • T. Harter, C. Brauner
  • Medicine, Chemistry
  • Comparative biochemistry and physiology. Part A, Molecular & integrative physiology
  • 2020
TLDR
Teleost fishes have evolved a mechanism by which adrenergic sodium-proton-exchangers on the red blood cell membrane actively create H+ gradients that are short-circuited in the presence of plasma-accessible carbonic anhydrase at the tissue capillaries, which allows teleosts to unload more O2 at their tissues without compromising O2 diffusion gradients and therefore, to use the available O2 carrying capacity of the blood to a greater degree. Expand
Enhanced hemoglobin–oxygen unloading in migratory salmonids
TLDR
The present study determined that in rainbow trout this system may be functional even at low concentrations of circulating catecholamines, and with β-NHE short-circuiting, Atlantic and coho salmon may be able to increase Hb–O2 unloading by up to 74 and 159%, respectively, as determined by modeling based on O2 equilibrium curves. Expand
A novel acidification mechanism for greatly enhanced oxygen supply to the fish retina
TLDR
Strong evidence is shown that vacuolar-type H+-ATPase and plasma-accessible carbonic anhydrase in the vascular structure supplying the retina act together to acidify the red blood cell leading to O2 secretion, concluding that this mechanism for retinal oxygenation played a vital role in the adaptive evolution of vision in teleost fishes. Expand
Evidence for a plasma-accessible carbonic anhydrase in the lumen of salmon heart that may enhance oxygen delivery to the myocardium
TLDR
Results from research in coho salmon support the presence of an enhanced oxygen delivery system in the lumen of a salmonid heart, which could help support cardiac function when oxygen supply to this vital organ becomes limiting. Expand
Blood and Gill Carbonic Anhydrase in the Context of a Chondrichthyan Model of CO2 Excretion
TLDR
It appears that the pattern of CA distribution in fishes can be generally categorized as either chondrichthyan or teleost models, however, further studies should examine the functional significance of the within-chondrichthyans differences the authors observed and investigate whether CO2 excretion patterns exist along a continuum or in discrete groups. Expand
The importance of a single amino acid substitution in reduced red blood cell carbonic anhydrase function of early-diverging fish
TLDR
Data indicate that low-activity RBC CA may be present in all fish with branchial CA-IV, and that the high-activityRBC CA seen in most teleosts may have evolved in conjunction with enhanced hemoglobin pH sensitivity. Expand
...
1
2
3
4
5
...

References

SHOWING 1-10 OF 109 REFERENCES
Plasma-accessible carbonic anhydrase at the tissue of a teleost fish may greatly enhance oxygen delivery: in vitro evidence in rainbow trout, Oncorhynchus mykiss
TLDR
If plasma-accessible CA-mediated short-circuiting is operational in vivo, the combined Bohr-Root effect system unique to teleost fishes could markedly enhance tissue O2 delivery far in excess of that in vertebrates possessing a Bohr effect alone and may lead to insights about the early evolution of the Root effect. Expand
Oxygen and carbon dioxide transport in vertebrate erythrocytes: an evolutionary change in the role of membrane transport.
  • M. Nikinmaa
  • Biology, Medicine
  • The Journal of experimental biology
  • 1997
TLDR
The high buffering capacity of the haemoglobins diminishes the possibility of regulating haemoglobin oxygen-affinity via secondarily active Na+/H+ exchange, because intracellular pH changes, caused by proton efflux, remain small. Expand
The evolution of Root effect hemoglobins in the absence of intracellular pH protection of the red blood cell: insights from primitive fishes
The Root effect, a reduction in blood oxygen (O2) carrying capacity at low pH, is used by many fish species to maximize O2 delivery to the eye and swimbladder. It is believed to have evolved in theExpand
Organic phosphates in the red blood cells of fish.
  • A. Val
  • Biology, Medicine
  • Comparative biochemistry and physiology. Part A, Molecular & integrative physiology
  • 2000
TLDR
The present review examines the appearance of all the major erythrocyticorganic phosphates during the evolutionary radiation of fish and provides examples illustrating qualitative and quantitative ontogenetic changes of organic phosphates in the red blood cell of several fish species and describes their effects on oxygen affinities. Expand
The distribution and physiological significance of carbonic anhydrase in vertebrate gas exchange organs.
The enzyme carbonic anhydrase (CA) catalyzes the reversible hydration/dehydration of CO(2) and water, maintaining a near-instantaneous equilibrium among all chemical species involved in the reaction.Expand
Root Effect Hemoglobin May Have Evolved to Enhance General Tissue Oxygen Delivery
TLDR
It is reported that when rainbow trout are exposed to elevated water carbon dioxide, red muscle partial pressure of oxygen (PO2) increases by 65%—evidence that Root hemoglobins enhance general tissue O2 delivery during acidotic stress, and argues that CA activity in muscle capillaries short-circuits red blood cell (RBC) pH regulation. Expand
The transition in hemoglobin proton-binding characteristics within the basal actinopterygian fishes
TLDR
The findings suggest that the change in Hb-proton-binding strategy may be associated with the evolution of enhanced O2 delivery to the eye and an in vivo operational Root effect in bowfin. Expand
Why is there no carbonic anhydrase activity available to fish plasma?
TLDR
CA in plasma did not cause the expected reduction in blood oxygen content but did have a marked effect on plasma total CO2 content and pH, which cannot distinguish between acid loading at the muscle and acid excretion at the gills or the kidneys. Expand
Acid-base disequilibrium in the arterial blood of rainbow trout.
TLDR
An extracorporeal blood circulation and a stopflow technique were used to examine the acid-base status of arterial blood in the rainbow trout, Oncorhynchus mykiss, and an acid- base disequilibrium was found in the post-branchial blood. Expand
Evolution of Oxygen Secretion in Fishes and the Emergence of a Complex Physiological System
TLDR
The events that led to the evolution of a key physiological innovation underpinning the large adaptive radiation of fishes, namely their unique ability to secrete molecular oxygen (O2), are reconstructed. Expand
...
1
2
3
4
5
...