Evolution of Oxygen Secretion in Fishes and the Emergence of a Complex Physiological System

Berenbrink, Michael; Koldkjær, Pia; Kepp, Oliver; Cossins, Andrew R.

doi:10.1126/science.1107793

Cited by 229 publications

(240 citation statements)

References 25 publications

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“…Spiny dogfish sharks show no RBC βNHE pH regulation and no plasma bicarbonate disequilibria [see discussion in Randall (Randall, 1998)]. Dogfish Hbs also have more histidine residues and therefore a greater buffer value than teleost Hbs (Berenbrink et al, 2005). Elasmobranchs do produce lactate and become acidotic following burst swimming (Holeton and Heisler, 1983).…”

Section: Tissue Oxygenation In Elasmobranchs Lampreys and Hagfishmentioning

confidence: 99%

“…The Journal of Experimental Biology (2014) The Journal of Experimental Biology (Romero et al, 1996;Rummer et al, 2010;Weaver et al, 1999), and this occurs in species that have lost or exhibit a minimal Root effect (Berenbrink et al, 2005;Rummer et al, 2010). The loss of RBC βNHE activation may be related to requirements for RBC volume regulation.…”

Section: Reviewmentioning

confidence: 99%

“…This loss of plasmaaccessible CA slowed the Jacobs-Stewart cycle and the transfer of acid between plasma and the RBCs via AE and 'housekeeping' NHE transport proteins on the RBC membrane. With the uncoupling of plasma and RBC pH, the importance of Hb as a buffer diminished and led to a reduction in Hb buffering (Berenbrink et al, 2005;Regan and Brauner, 2010a;Regan and Brauner, 2010b), thus enhancing the tight coupling of O 2 and CO 2 transfer through the RBCs (Brauner et al, 2000). Many extant teleosts are able to regulate RBC pH and have Root effect Hbs that operate at physiological pH.…”

mentioning

confidence: 99%

“…Thus, fewer protons are bound to histidine residues and more are available to couple O 2 and CO 2 transfer. Berenbrink et al (Berenbrink et al, 2005) presented an elegant review of the evolution of vertebrate Hbs, concentrating on the relationship between the number of histidine side chains, specific buffer values and the magnitude of the Bohr coefficient. They point out that lamprey and many teleosts have a low Hb buffer value when compared with other vertebrates, which is related to a reduction in the number of histidine residues.…”

mentioning

confidence: 99%

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

Randall

Rummer

Wilson³

et al. 2014

Journal of Experimental Biology

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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 β-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. IntroductionTeleost fishes comprise 95% of all extant fishes, with approximately 26,000 named species (Helfman et al., 1997). Teleosts first appeared in the early Triassic period 200-250 million years ago (MYA) and have since radiated into almost all aquatic environments (Nelson, 1994;Near et al., 2012). The ray-finned fishes, to which the teleost fishes belong, diverged from the lobe-finned fishes (e.g. lungfishes) around the Devonian, 400 MYA. The lobe-finned fishes were very successful until the Permian crisis 252 MYA...

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Section: Tissue Oxygenation In Elasmobranchs Lampreys and Hagfishmentioning

confidence: 99%

Section: Reviewmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

See 2 more Smart Citations

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

Randall

Rummer

Wilson³

et al. 2014

Journal of Experimental Biology

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“…the fish is negatively buoyant but still gains lift from the bladder [4]. In addition to buoyancy functions controlled by gas secretion and reabsorption [5], the swimbladder can be converted to a sound-producing organ by the attachment of muscles [6][7][8][9] or an auditory organ if diverticula or ossicles connect the swimblader to the ear [10][11][12][13].…”

Section: Introductionmentioning

confidence: 99%

Wall structure and material properties cause viscous damping of swimbladder sounds in the oyster toadfishOpsanus tau

et al. 2016

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Despite rapid damping, fish swimbladders have been modelled as underwater resonant bubbles. Recent data suggest that swimbladders of soundproducing fishes use a forced rather than a resonant response to produce sound. The reason for this discrepancy has not been formally addressed, and we demonstrate, for the first time, that the structure of the swimbladder wall will affect vibratory behaviour. Using the oyster toadfish Opsanus tau, we find regional differences in bladder thickness, directionality of collagen layers (anisotropic bladder wall structure), material properties that differ between circular and longitudinal directions (stress, strain and Young's modulus), high water content (80%) of the bladder wall and a 300-fold increase in the modulus of dried tissue. Therefore, the swimbladder wall is a viscoelastic structure that serves to damp vibrations and impart directionality, preventing the expression of resonance.

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Combined crystallographic and spectroscopic analysis of Trematomus bernacchii hemoglobin highlights analogies and differences in the peculiar oxidation pathway of Antarctic fish hemoglobins

et al. 2009

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Recent studies have demonstrated that hemoglobins isolated from Antarctic fish undergo peculiar oxidation processes. Here we show, by combining crystallographic and spectroscopic data, that the oxidation pathway of Trematomus bernacchii hemoglobin (HbTb) is distinct from that observed for the major component of Trematomus newnesi (Hb1Tn), despite the high sequence identity of the two proteins and structural similarity of their ferrous and fully oxidized states. Resonance Raman analysis of HbTb autoxidation upon air-exposure reveals the absence of the oxidized pentacoordinated state that was observed for Hb1Tn. The HbTb oxidation pathway is characterized by two ferric species: an aquo hexacoordinated high spin state and a bis-histidyl hexacoordinated low spin form, which appear in the early stages of the oxidation process. The high resolution structure of an intermediate along the oxidation pathway has been determined at 1.4 A resolution. The analysis of the electron density of the heme pocket shows, for both the alpha and the beta iron, the coexistence of multiple binding states. In this partially oxidized form, HbTb exhibits significant deviations from the canonical R state both at the local and global level. The analysis of these modifications highlights the structural correlation between key functional regions of the protein.

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Evolution of Oxygen Secretion in Fishes and the Emergence of a Complex Physiological System

Cited by 229 publications

References 25 publications

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

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

Wall structure and material properties cause viscous damping of swimbladder sounds in the oyster toadfishOpsanus tau

Combined crystallographic and spectroscopic analysis of Trematomus bernacchii hemoglobin highlights analogies and differences in the peculiar oxidation pathway of Antarctic fish hemoglobins

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