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Root Effect Haemoglobins in Fish May Greatly Enhance General Oxygen Delivery Relative to Other Vertebrates.

Rummer JL, Brauner CJ - PLoS ONE (2015)

Bottom Line: A reduction in pH reduces both Hb-O2 affinity (Bohr effect) and carrying capacity (Root effect).Using known ΔpHa-v and assuming a constant arterial-venous PO2 difference (Pa-vO2), Root effect Hbs can enhance O2 release to the tissues by 73.5% in trout; whereas, the Bohr effect alone is responsible for enhancing O2 release by only 1.3% in humans.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Zoology, University of British Columbia, 6270 University Blvd., Vancouver, BC, V6T 1Z4 Canada; ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, QLD 4811 Australia.

ABSTRACT
The teleost fishes represent over half of all extant vertebrates; they occupy nearly every body of water and in doing so, occupy a diverse array of environmental conditions. We propose that their success is related to a unique oxygen (O2) transport system involving their extremely pH-sensitive haemoglobin (Hb). A reduction in pH reduces both Hb-O2 affinity (Bohr effect) and carrying capacity (Root effect). This, combined with a large arterial-venous pH change (ΔpHa-v) relative to other vertebrates, may greatly enhance tissue oxygen delivery in teleosts (e.g., rainbow trout) during stress, beyond that in mammals (e.g., human). We generated oxygen equilibrium curves (OECs) at five different CO2 tensions for rainbow trout and determined that, when Hb-O2 saturation is 50% or greater, the change in oxygen partial pressure (ΔPO2) associated with ΔpHa-v can exceed that of the mammalian Bohr effect by at least 3-fold, but as much as 21-fold. Using known ΔpHa-v and assuming a constant arterial-venous PO2 difference (Pa-vO2), Root effect Hbs can enhance O2 release to the tissues by 73.5% in trout; whereas, the Bohr effect alone is responsible for enhancing O2 release by only 1.3% in humans. Disequilibrium states are likely operational in teleosts in vivo, and therefore the ΔpHa-v, and thus enhancement of O2 delivery, could be even larger. Modeling with known Pa-vO2 in fish during exercise and hypoxia indicates that O2 release from the Hb and therefore potentially tissue O2 delivery may double during exercise and triple during some levels of hypoxia. 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.

No MeSH data available.


Related in: MedlinePlus

The degree to which O2 release from Hb is enhanced for a given ΔpH for a Bohr effect Hb system (human, panel A) and a Root effect Hb system (rainbow trout, panel B).The increase in O2 release with respective right-shifts in the OECs is represented by vertical double arrows here and as a percent increase over what is possible without the right shift in the text (see above section “Series 2: Differences in ΔPO2…” for details).
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pone.0139477.g002: The degree to which O2 release from Hb is enhanced for a given ΔpH for a Bohr effect Hb system (human, panel A) and a Root effect Hb system (rainbow trout, panel B).The increase in O2 release with respective right-shifts in the OECs is represented by vertical double arrows here and as a percent increase over what is possible without the right shift in the text (see above section “Series 2: Differences in ΔPO2…” for details).

Mentions: The OECs generated for human and trout blood were used to model O2 release from Hb and tissue O2 delivery. For the human model, a PaO2 of 115 mmHg (labeled “a” on Fig 2A), a PvO2 of 27 mmHg (labeled “v” on Fig 2A), and a physiologically relevant ∆pHa-v of 0.035 were used. All above values correspond to values obtained from previous studies [6,32–35]. The corresponding right-shifted OEC was plotted assuming a constant Bohr coefficient, Φ = -0.35, between 20 and 80% Hb-O2 saturation [4]. For the rainbow trout model, a PaO2 of 110 mmHg was used (labeled “a” on Fig 2B), and PvO2 (labeled “v” on Fig 2B) was estimated from muscle O2 values of 45–47 mmHg, both of which correspond to values obtained in vivo [21]. The OEC curves generated from the current study were used to simulate the various ∆pHa-v for the model and also to accommodate the non-linear Bohr shift known to occur at the different Hb-O2 saturations in teleosts.


Root Effect Haemoglobins in Fish May Greatly Enhance General Oxygen Delivery Relative to Other Vertebrates.

Rummer JL, Brauner CJ - PLoS ONE (2015)

The degree to which O2 release from Hb is enhanced for a given ΔpH for a Bohr effect Hb system (human, panel A) and a Root effect Hb system (rainbow trout, panel B).The increase in O2 release with respective right-shifts in the OECs is represented by vertical double arrows here and as a percent increase over what is possible without the right shift in the text (see above section “Series 2: Differences in ΔPO2…” for details).
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4593521&req=5

pone.0139477.g002: The degree to which O2 release from Hb is enhanced for a given ΔpH for a Bohr effect Hb system (human, panel A) and a Root effect Hb system (rainbow trout, panel B).The increase in O2 release with respective right-shifts in the OECs is represented by vertical double arrows here and as a percent increase over what is possible without the right shift in the text (see above section “Series 2: Differences in ΔPO2…” for details).
Mentions: The OECs generated for human and trout blood were used to model O2 release from Hb and tissue O2 delivery. For the human model, a PaO2 of 115 mmHg (labeled “a” on Fig 2A), a PvO2 of 27 mmHg (labeled “v” on Fig 2A), and a physiologically relevant ∆pHa-v of 0.035 were used. All above values correspond to values obtained from previous studies [6,32–35]. The corresponding right-shifted OEC was plotted assuming a constant Bohr coefficient, Φ = -0.35, between 20 and 80% Hb-O2 saturation [4]. For the rainbow trout model, a PaO2 of 110 mmHg was used (labeled “a” on Fig 2B), and PvO2 (labeled “v” on Fig 2B) was estimated from muscle O2 values of 45–47 mmHg, both of which correspond to values obtained in vivo [21]. The OEC curves generated from the current study were used to simulate the various ∆pHa-v for the model and also to accommodate the non-linear Bohr shift known to occur at the different Hb-O2 saturations in teleosts.

Bottom Line: A reduction in pH reduces both Hb-O2 affinity (Bohr effect) and carrying capacity (Root effect).Using known ΔpHa-v and assuming a constant arterial-venous PO2 difference (Pa-vO2), Root effect Hbs can enhance O2 release to the tissues by 73.5% in trout; whereas, the Bohr effect alone is responsible for enhancing O2 release by only 1.3% in humans.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Zoology, University of British Columbia, 6270 University Blvd., Vancouver, BC, V6T 1Z4 Canada; ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, QLD 4811 Australia.

ABSTRACT
The teleost fishes represent over half of all extant vertebrates; they occupy nearly every body of water and in doing so, occupy a diverse array of environmental conditions. We propose that their success is related to a unique oxygen (O2) transport system involving their extremely pH-sensitive haemoglobin (Hb). A reduction in pH reduces both Hb-O2 affinity (Bohr effect) and carrying capacity (Root effect). This, combined with a large arterial-venous pH change (ΔpHa-v) relative to other vertebrates, may greatly enhance tissue oxygen delivery in teleosts (e.g., rainbow trout) during stress, beyond that in mammals (e.g., human). We generated oxygen equilibrium curves (OECs) at five different CO2 tensions for rainbow trout and determined that, when Hb-O2 saturation is 50% or greater, the change in oxygen partial pressure (ΔPO2) associated with ΔpHa-v can exceed that of the mammalian Bohr effect by at least 3-fold, but as much as 21-fold. Using known ΔpHa-v and assuming a constant arterial-venous PO2 difference (Pa-vO2), Root effect Hbs can enhance O2 release to the tissues by 73.5% in trout; whereas, the Bohr effect alone is responsible for enhancing O2 release by only 1.3% in humans. Disequilibrium states are likely operational in teleosts in vivo, and therefore the ΔpHa-v, and thus enhancement of O2 delivery, could be even larger. Modeling with known Pa-vO2 in fish during exercise and hypoxia indicates that O2 release from the Hb and therefore potentially tissue O2 delivery may double during exercise and triple during some levels of hypoxia. 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.

No MeSH data available.


Related in: MedlinePlus