Beyond buoyancy and vision: the potential for the Root effect to deliver oxygen to tissues other than the swim bladder and eye

Rummer, J.L., and Brauner, C.J. (2008) Beyond buoyancy and vision: the potential for the Root effect to deliver oxygen to tissues other than the swim bladder and eye. Comparative Biochemistry and Physiology - Part A: Molecular and Integrative Physiology, 150 (Suppl 3). S52-S53.

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Abstract

Teleost fish possess a unique, pH-sensitive hemoglobin (Hb) that, in the presence of an acidosis, substantially reduces the affinity and carrying capacity for O₂ (Root effect). To date, this efficient O₂ delivery mechanism is only known for filling a swim bladder (SB) against huge pressure gradients (> 50 atm) associated with depth and for oxygenating the metabolically active, yet avascular retinal tissue of the eye. In spite of the clear benefits to O₂ delivery for buoyancy and vision, no study has been conducted to determine whether the Root effect may be important in optimizing O₂ delivery to other tissues such as muscle, which is the focus of this research.During environmental or exercise-induced stress, blood pH may fall; however, some fish regulate red blood cell (RBC) intracellular pH (pHi) by releasing catecholamines that activate the sodium/proton (Na⁺/H⁺) exchanger (βNHE) on the RBC membrane. The βNHE removes H⁺s from the RBC resulting in an intracellular alkalosis, an increase in Hb–O₂ affinity, and O₂ uptake at the respiratory surfaces is safeguarded, which is the ultimate goal of this mechanism. In our proposed model, when adrenergically stimulated blood encounters plasma-accessible carbonic anhydrase (CA), an enzyme found in the RBC but also membrane-bound and potentially plasma-accessible in select locations, it will catalyze H⁺s removed from the RBC to form CO₂. This CO₂ will back-diffuse into the RBC creating an intracellular acidosis (extracellular alkalosis), reducing Hb–O₂ affinity, and ultimately elevating PO₂ via the Root effect. We created an in vitro closed system using rainbow trout (Oncorhynchus mykiss) blood where we can (1) simulate an acid-induced Root effect, (2) adrenergically stimulate the RBCs, and finally (3) short-circuit the βNHE via CA (CA-mediated Root effect), all of which can be monitored in real-time ( Fig. 1). Data generated currently support our Hypothesis: adrenergic RBC pH regulation can be short-circuited in the presence of plasma-accessible CA, therefore generating a Root effect increase in PO₂. In fact, if this scenario also occurs in the tissues of O. mykiss, CA-mediated short-circuiting of adrenergic pH regulation can facilitate an increase in PO₂ over 30 times that which would be generated in vertebrates possessing only a Bohr shift! We are ready to test our model in vivo by implanting fiber-optic O₂ sensors in O. mykiss muscle while simulating environmental and exercise stress with and without CA blockers. Furthermore, even though CA is not found in general circulation, there are membrane-bound and potentially plasma-accessible isoforms in muscle endothelia, and research is underway to localize this enzyme to understand the relationship between location and function of the short-circuiting.

Teleost fish, which are more numerous than all other vertebrates combined (terrestrial and aquatic), have evolved an extraordinary O₂ delivery mechanism, the Root effect, that allows O₂ delivery to the eye and to the SB, thus allowing efficient buoyancy regulation, which may be one of the most important factors responsible for the extensive adaptive radiation in teleost fishes. Therefore, it is particularly interesting that the Root effect has not yet been investigated for general O₂ delivery. If the Root effect can also facilitate general O₂ delivery in vivo, which our data currently support, this would help shed insight into how the Root effect was selected for prior to the evolution of the βNHE, choroid gland and retia of the eye, and the gas gland and rete mirabile associated with the SB.

Item ID: 45332
Item Type: Article (Abstract)
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Abstracts of the Annual Main Meeting of the Society of Experimental Biology, 6th - 10th July 2008, Marseille, France

ISSN: 1531-4332
Date Deposited: 05 Sep 2016 22:39
FoR Codes: 06 BIOLOGICAL SCIENCES > 0602 Ecology > 060203 Ecological Physiology @ 100%
SEO Codes: 96 ENVIRONMENT > 9608 Flora, Fauna and Biodiversity > 960802 Coastal and Estuarine Flora, Fauna and Biodiversity @ 100%
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