The Generation of Hyperbaric Oxygen Tensions in
Fish
Bernd Pelster
Institut für Zoologie und Limnologie, Universität Innsbruck, A-6020 Innsbruck, Austria
A
erobic metabolism requires a supply of oxygen to the tissues and adequate elimination of acid end products like
carbon dioxide to prevent undue acidification of tissues.
Accordingly, metabolic and ventilatory activities are tightly
coupled in most animals. In addition, the low solubility of oxygen in body fluids is compensated by the presence of respiratory pigments like hemoglobin or hemocyanin, which increase
the oxygen-carrying capacity of blood or hemolymph by one
to two orders of magnitude. The optimal use of these respiratory pigments often requires loading and unloading of the oxygen in a very narrow range of oxygen partial pressures. Furthermore, variations in lifestyle, environmental conditions, and
internal organization require accurate fine-tuning of the oxygen-binding characteristics of the respiratory pigments.
Intensive studies on the structure and functions of the bestknown respiratory pigment, hemoglobin, have revealed a striking flexibility in its intrinsic oxygen-binding characteristics
even among closely related species, caused by replacements
in various amino acid residues of the protein moiety of these
pigments (4). In addition, the hemoglobins may show large
variability in their sensitivity to effectors like protons, organic
phosphates, or bicarbonate, which commonly bind to the
deoxygenated state of the pigment and reduce its oxygen affinity.
An increase in proton concentration decreases the oxygen
affinity of most respiratory pigments (the well-known Bohr
effect). In a large number of fish hemoglobins, however, pH
decrease not only reduces oxygen affinity but also reduces
oxygen-carrying capacity (Fig. 1) (2, 16). At low pH, these
hemoglobins remain partially deoxygenated even in the presence of oxygen partial pressures in excess of 20 kPa (i.e., under
severe hyperoxia). Although some scientists view this as an
extreme form of the Bohr effect, others consider it to be a specific phenomenon with a distinct molecular mechanism. It was
named the “Root effect” after R. W. Root, who first described
this pH-dependent decrease in hemoglobin oxygen-carrying
capacity.
Although the exact molecular mechanism basic to the Root
effect is still debated, it is widely accepted among fish physiologists that the Root effect is required to generate hyperoxic
oxygen partial pressures in the swim bladder and eyes of fish.
These high oxygen partial pressures are necessary to fill the
swim bladder, especially of physoclist fish (whose swim blad-
0886-1714/01 5.00 © 2001 Int. Union Physiol. Sci./Am.Physiol. Soc.
ders are not connected to the esophagus after the embryonic
stage), with gas and to ensure a sufficient oxygen supply to the
retina.
Presence and nature of the Root effect
The presence of a Root effect in blood can be investigated
gasometrically and spectrophotometrically by measuring the
oxygen content or the oxygen saturation, respectively, of blood
or hemoglobin solutions at various pH values. These different
approaches may imply variations in the oxygen partial pressure
used as a reference for 100% oxygenation, which have contributed to controversies about the distribution of the Root
effect. Nevertheless, it is generally accepted that the Root effect
is a peculiarity of teleost fish hemoglobins, although a few
studies have reported it in elasmobranchs and even in amphibians (13). The possible physiological function of the Root effect
in nonteleosts remains obscure and is not dealt with in this
review, which focuses on teleost fishes.
Fish hemoglobins can be separated into electrophoretically
anodic and cathodic components, and the relative distribution
of these hemoglobin components varies from species to
species (17). Although the Root effect is clearly established in
the anodic components, it is absent in cathodic hemoglobins
(13). Accordingly, the magnitude of the Root effect varies from
species to species. In eel or trout, for example, in which ~50%
and ~60%, respectively, of the hemoglobin cannot be oxygenated at low pH, these values match with the fraction of
anodic hemoglobins.
The molecular basis of the Bohr effect is a binding of protons
to specific amino acid residues of the globin chains that results
in extreme stabilization of the low-affinity, deoxygenated conformation (T-state) of the hemoglobin. Consequently, higher
oxygen tensions are required to oxygenate the hemoglobin,
i.e., its oxygen affinity is decreased. On the basis of the concept that the Root effect is distinct from the Bohr effect, it was
proposed that specific amino acid replacements (14) in Root
hemoglobins are implicated in blocking full oxygenation at
low pH even under high oxygen partial pressures.
Root hemoglobins appear to exhibit marked chain heterogeneity and characteristically show negative cooperativity (the
Hill coefficient is below unity at low pH). Recent molecular
studies suggest that protonation of specific positively charged
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Surprising inventiveness in the molecular interactions in fish hemoglobins that express the Root
effect (decreased oxygen-carrying capacity at low pH) and in metabolic adaptations in swim
bladder gas gland cells and retinal tissues causes local acidification of blood and generates
hyperbaric oxygen tensions that drive oxygen into the swim bladder (regulating buoyancy)
and ensures the oxygen supply to the avascularized retinae.
dence of their hydration and dehydration reactions significantly contributes to differences in the kinetics of the Root-on
and Root-off reactions. Nevertheless, both reactions are completed within <1s, and these differences in the kinetics do not
appear to be of physiological significance.
Physiological importance of the Root effect
residues within the central cleft between the two β-chains
causes a destabilization of the oxygen conformation (R-state) at
low pH (6). Additional amino acid replacements (Table 1)
appear to make the α1β2 switch interface, which is loosened
during oxygenation, particularly stable at low pH, so that Root
hemoglobins can bind oxygen at the high-affinity α-chains
while remaining in the T-state conformation. This ability to
accommodate conformational changes in liganded subunits
while remaining in the T-state is not observed in hemoglobins
showing a normal Bohr effect but no Root effect (3). The
molecular mechanisms hitherto proposed based on single
amino acid exchanges have not been supported by experimental data, and Mazzarella et al. (5) therefore proposed that
more than one amino acid constellation might cause the presence of the Root effect. This might imply that the Root effect
was invented more than once during evolution.
Blood is acidified by secretion of protons into the blood or
through increases in carbon dioxide partial pressure. Reoxygenation of hemoglobin is achieved by alkalinization of the
blood. The kinetics of the Root-on and Root-off reactions are
rather complex because they not only include the chemical
reaction and the diffusion of oxygen but also the transfer of
acid into the blood and erythrocytes and binding of protons to
the hemoglobin (12). Carbonic anhydrase is found in the red
blood cells and is involved in both processes. The pH depen-
Given that the Root effect is switched on by acidification, we
have to address the question of when and where acidification
occurs. Acidification of blood is observed in specific stress situations, such as strenuous exercise, during which the anaerobic production of lactic acid in muscle tissue results in a severe
drop in the pH of venous and even arterial blood. Acidification
of arterial blood, however, reduces the oxygen-carrying capacity of the blood in the gills, where it cannot be fully oxygenated. This would be deleterious in situations in which as
much oxygen as possible is required for muscular contraction.
Intriguing ion transport mechanisms in the membranes of the
erythrocytes ensure that this lactic acidosis is not transferred to
the cytoplasm (11).
A sodium/hydrogen exchanger (NHE) is present in most erythrocytes and is usually involved in osmotic volume regulation. In fish with Root effect hemoglobin, this exchanger is
under β-adrenergic control (β-NHE; Ref. 8). Stimulation of the
β-adrenergic receptor via cAMP as a second messenger and
protein kinase A activates the NHE, which extrudes protons
from the red blood cells and thus alkalinizes the cells and acidifies the blood plasma. Thus intracellular pH of the red blood
cells may even increase under exercise-induced blood acidification.
These considerations show that, physiologically, the Root
effect is not tailored to bring about an overall reduction in oxygen-carrying capacity of the blood. To understand the physiological importance of the Root effect, we therefore turn our
attention to special organs. Only the swim bladder and the eye
of the fish have been identified as organs that rely on the Root
effect. Both organs depend on a buildup of oxygen partial pressures that far exceed the 20 kPa that, under optimal conditions,
can be reached in the gills. In combination with a sophisticated countercurrent arrangement of the vascular system, oxygen unloading via the Root effect allows for the generation of
TABLE 1. Amino acids that are thought to be involved in the expression of the Root effect
α-chain
β-chain
C3
C6
CD2
NA2
EF6
F9
FG1
FG4
H21
HC3
Non-Root effect hemoglobins
Human
Oncorhynchus mykiss HbI
Anguilla anguilla cathodic Hb
Thr
Gln
Ala
Thr
Thr
Val
Pro
Ser
Ser
His
Glu
Glu
Lys
Leu
Lys
Cys
Ala
Asn
Asp
Asn
Glu
His
Phe
Asn
His
Ser
Lys
His
Phe
Phe
Root effect hemoglobins
Oncorhynchus mykiss HbIV
Cyprinus carpio
Notothenia angustata Hb1
Chelodonichtys kumu
Pagothenia bernacchii Hb1
Gln
Gln
Gln
Gln
Gln
Ala
Thr
Thr
Thr
Thr
Ser
Ala
Ser
Thr
Ser
Glu
Glu
Lys
Glu
Glu
Lys
Lys
Ala
Lys
Ala
Ser
Ser
Ser
Ser
Ser
Glu
Glu
Glu
Glu
Glu
His
His
His
His
His
Arg
Arg
Lys
Arg
Lys
His
His
His
His
His
Modified from Ref. 3.
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FIGURE 1. An increase in proton concentration decreases hemoglobin oxygen
affinity in most vertebrate hemoglobins (the Bohr effect). In fish blood, an
increase in proton concentration may also induce a decrease in the hemoglobin oxygen-carrying capacity (the Root effect). Because of specific amino acid
replacements in the α- and β-chains, the oxygenated conformation (R-state) of
the Root effect hemoglobins is destabilized at low pH, whereas the α1β2
switch interface in the deoxygenated T-state of the molecule is stabilized,
whereby the hemoglobin molecules cannot be oxygenated at low pH even at
high oxygen partial pressures (PO2). CO2, oxygen content.
hyperbaric oxygen partial pressures of several hundred atmospheres in the swim bladder.
Swim bladder function
FIGURE 2. Lactic acid and carbon dioxide produced by gas gland cells are
released into the blood stream. The increased extracellular proton concentration dehydrates bicarbonate, forming carbon dioxide. In gas gland tissue, this
reaction is catalyzed by membrane-bound carbonic anhydrase. Carbon dioxide diffuses into the red blood cell, where the increase in carbon dioxide partial pressure results in hydration of carbon dioxide, forming bicarbonate and
protons. The increase in intracellular proton concentration initiates the Root
effect, and oxygen is released from the hemoglobin. CA, carbonic anhydrase;
G-6-P, glucose-6-phosphate; Hb, hemoglobin; PPS, pentose phosphate shunt.
cells (9). Sequence data on the B subunit of V-ATPase of eel gas
gland cells has revealed the presence of two isoforms (7). In
mammals, one of these isoforms is found in very few organs,
such as kidney. In kidney cells, its function in association with
acid-base regulation is partially controlled by being inserted or
removed from the membrane. The second V-ATPase B subunit
isoform (brain isoform) can be found in intracellular vesicles of
virtually all cells. If this would be a general model that could
be transferred to the gas gland cells, the kidney isoform of the
B subunit might be involved in acid secretion at basolateral
membranes and the brain isoform may be necessary for the
acidification of lamellar bodies, in which surfactant is stored
before exocytosis.
Thus several mechanisms appear to cause the release of protons in the gas gland. The pH of blood circulating through the
swim bladder of the European eel has been found to be in the
range of 7.5−7.8 when the gas gland cells are inactive. The
blood becomes acidic, with pH values of 6.5−6.6 at times
when the gas gland is active and gas is being secreted into the
swim bladder. The presence of different mechanisms for proton
transfer across the cell membrane may be related to the fact
that the cells must provide for a well-controlled secretion of
protons over this wide range of pH values.
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The swim bladder originates ontogenetically as an outgrowth of the esophagus. Although it is not clear whether it
originally was a buoyancy organ or a structure involved in aerial gas exchange, its homology to the lung is generally
accepted. The teleost swim bladder primarily functions as a
buoyancy organ, and, being flexible, its volume and internal
pressure change with changes in hydrostatic pressure. To retain
neutral buoyancy, teleosts must be able to keep the volume of
the swim bladder constant. This means that gas needs to be
secreted into the bladder while descending and removed while
ascending. Removal of gas occurs by releasing gas bubbles via
the esophagus or by reabsorbing gas along gas partial pressure
gradients in special sections of the swim bladder. The secretion
of gas into the swim bladder is a more complicated phenomenon that includes the release of oxygen from the hemoglobin
via the Root effect. The swim bladder gas consists mainly of
oxygen, carbon dioxide, and inert gases, mainly nitrogen. This
present discussion is limited to the secretion of oxygen, which
is the major constituent. Other gases have been dealt with elsewhere (10, 11).
Although the commonly used term “gas secretion” implies
an active process, swim bladder gas filling occurs by simple
diffusion along partial pressure gradients initiated by the
release of oxygen from the hemoglobin via the Root effect, typically when extracellular pH values fall to ~7.3−7.5 (and intracellular values are ~7.1−7.3). The acidification of the blood
within the swim bladder capillaries is brought about by the
release of acid from the so-called gas gland cells of the swim
bladder epithelium (Fig. 2). These cells are cuboidal or cylindrical and may be lumped together, forming a compact, sometimes multilayered gas gland, or may be spread over the whole
swim bladder epithelium, as in the eel. Gas gland cells show
structural and functional polarity. The apical side, oriented
toward the swim bladder lumen, is characterized by a few
small microvilli. The basal side, facing the blood vessels, shows
extensive membrane foldings. In contrast to most other cells
that carry out active transport, gas gland cells apparently are
not equipped with a large complement of mitochondria.
Recent studies have revealed that this structural polarity is
functionally important. Gas gland cells serve a dual function,
producing surfactant, which is secreted into the swim bladder
lumen via exocytosis (15), and secreting acidic metabolites
into the blood at the basolateral membranes. Acidic metabolites are produced mainly from blood-borne glucose. A large
fraction of this glucose is converted into lactic acid, even
though gas gland cells are usually exposed to hyperoxic conditions. This is possible because these cells do not show a Pasteur effect and thus produce lactate even at an oxygen pressure
of 50 atmospheres. The lactic acid is released into the blood.
Although pharmacological inhibition of lactate transport (using
cinnamate) does not impair the acid release, inhibition of
sodium/hydrogen exchange, anion exchange, or of vacuolar
(V)-ATPase activity significantly reduces acid release from the
The transfer of protons through the cell membrane acidifies
the extracellular fluid. This acid load is transferred into the erythrocyte via the Jacobs-Stewart cycle. Extracellular protons
react with bicarbonate, forming carbon dioxide that diffuses
into the red blood cell, where it is hydrated to bicarbonate and
protons. With an increasing proton concentration within the
red blood cell, the threshold for the Root effect is reached and
oxygen is liberated from the hemoglobin. In swim bladder tissue, the time necessary to complete the whole series of reactions is significantly reduced due to the presence of a membrane-bound carbonic anhydrase in gas gland cells. Although
blood plasma typically is devoid of carbonic anhydrase activity, membrane-bound enzyme rapidly accelerates the equilibrium of the carbon dioxide-bicarbonate reaction in the extracellular fluid (9). The high carbonic anhydrase activity of the
red blood cell reestablishes the intracellular equilibrium of the
bicarbonate-carbon dioxide reaction.
Besides lactic acid, carbon dioxide is produced and released
from gas gland cells and is especially important for the initiation of the Root effect. A comparison of the oxygen consumption and the carbon dioxide production of eel gas gland cells
revealed that most of the carbon dioxide is produced by decarboxylation in the pentose phosphate shunt and that only a
small fraction of the glucose is actually oxidized by aerobic
metabolism (10). This intriguing metabolic design ensures that
the highest carbon dioxide partial pressure is always found in
the gas gland. In contrast to the protons, which cannot penetrate membranes easily and require special, time-consuming
transport mechanisms, carbon dioxide rapidly diffuses from the
gas gland cells into the red blood cells. Thus the carbon dioxide produced ensures a very rapid acidification of the erythrocytes and initiation of the Root effect. The oxygen that has been
liberated from the hemoglobin as blood passes through the gas
gland readily diffuses into the swim bladder lumen along the
partial pressure gradient.
290
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The fish eye
In contrast to most other vertebrates, the retinas of most fish
are not vascularized, and diffusion distances for nutrients and
oxygen to the retina therefore can be more than six times larger
than in primates. Because the retina has a high metabolic
activity, this raises a question about how the necessary oxygen
supply to the retina is secured. Although the situation is far
from understood, obvious parallels exist to the situation in the
swim bladder, and the Root effect appears to be involved. The
vitreous humor of the fish eye is highly oxygenated, and oxygen partial pressure values of 1 atmosphere and higher have
been reported (11, 18). Furthermore, the ophthalmic artery
passes through a countercurrent system, the choroid rete
mirabile, before branching to the choriocapillaris, the capillary
network from which the retina is supplied.
To initiate the Root effect, blood must be acidified in the
choriocapillaris. As with the gas gland tissue, teleost retinal tissue produces lactic acid even in the presence of oxygen. Furthermore, in addition to aerobic glucose oxidation, part of the
glucose is metabolized in the pentose phosphate shunt. Thus,
as in the swim bladder, the retina apparently produces lactic
acid and carbon dioxide, which are released into the blood
stream and initiate the Root effect, and the initial increase in
oxygen partial pressure is subsequently multiplied by back diffusion of oxygen in the countercurrent system of the choroid
rete mirabile (Fig. 3).
Despite the homologies with the swim bladder, an intriguing
twist complicates the situation in the fish eye, since retinal tis-
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FIGURE 3. Blood supply to the fish eye originates from the efferent artery of
the pseudobranch, which in turn receives arterialized blood from the first gill
arch. According to current understanding, blood is titrated in the pseudobranch to a pH value just above that which induces the Root effect. Subsequently, only a small amount of acid needs to be released from the retina to
switch on the Root effect in the choriocapillaris and to liberate oxygen from
the hemoglobin. The resulting increase in oxygen partial pressure induces a
back diffusion of oxygen in the choroid rete mirabile and thus generates high
oxygen partial pressures that are necessary to ensure the oxygen supply to the
avascularized fish retina. O2cap, oxygen carrying capacity. Figure modified
from Ref. 1.
Some of the oxygen will also remain in the blood, and blood
returning from the gas gland tissue travels through the countercurrent system of the rete mirabile with a higher oxygen partial pressure than afferent blood traveling to the gas gland tissue. Given the production and release of carbon dioxide from
the gas gland cells, this also applies to carbon dioxide tensions.
The metabolic activity of gas gland cells thus brings about initial increases in blood oxygen partial pressures and carbon
dioxide partial pressures.
The swim bladder rete mirabile represents a very efficient
countercurrent exchanger. Oxygen and carbon dioxide molecules returning to the venous side of the rete mirabile will therefore diffuse back to the arterial side, resulting in a countercurrent multiplication of the initial increases in oxygen and carbon
dioxide partial pressures. The back diffusion of carbon dioxide
again is of crucial importance for the initiation of the Root effect
within the swim bladder tissue because it results in an acidification of the arterial blood of the rete mirabile, induces the Root
effect, and elevates oxygen partial pressure in the blood supplying the swim bladder tissue. The metabolic activity of gas
gland cells causes further acidification, which enhances the
Root effect and the increase in oxygen partial pressure. Model
calculations demonstrate that this dual acidification, together
with the very efficient countercurrent multiplication of the
increases in blood oxygen partial pressure and blood oxygen
content in the rete mirabile, can readily explain the generation
of oxygen partial pressure values of up to several hundred
atmospheres in swim bladder tissue of deep sea fish (10).
Summary
The Root effect represents an intriguing example of the ecophysiological variability and adaptability of hemoglobin.
Although hyperoxia is deleterious for most tissues, extremely
high oxygen partial pressures must be generated in the swim
bladder and retinae of fish to ensure their proper physiological
function. These high oxygen partial pressure values are generated in a complex system that includes a remarkable capacity
of certain cells to produce and secrete acid metabolites, the
presence of Root effect hemoglobins, and of a rete mirabile.
The rete mirabile is necessary for countercurrent multiplication
but also acts as a barrier to prevent the acid from spreading
through the whole organism. In addition, hormone-induced
acid-base regulation in red blood cells prevents the initiation
of the Root effect during situations of general acidosis, thus
preventing a reduction in hemoglobin oxygen-carrying capacity that would curtail oxygen transport.
I would like to thank Dr. R. Weber for helpful comments on the manuscript.
Parts of this study were financially supported by the Austrian Science Foundation (FWF, P-11837-BIO, and P14174-BIO).
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sue is very sensitive to acidification and acidification down to
pH 6.4 results in blindness. Thus the unavoidable drop in
blood pH associated with the countercurrent concentration of
carbon dioxide must be moderate to avoid an acid-induced
damage of the tissue.
Comparative studies demonstrated that the presence of a
choroid rete mirabile in the eye coincides with the presence of
a pseudobranch (1). This gill-like hemibranch receives arterialized blood from the first gill arch, and the efferent artery gives
rise to the ophthalmic artery. The fish eye thus receives its
blood supply from the pseudobranch. Although the pseudobranch has attracted attention for more than 150 years, its
physiological function remains a mystery. Nevertheless, most
fish physiologists subscribe to the idea that it is implicated in
the oxygen supply to the retina.
It has recently been proposed that the pseudobranch is
equipped with a sensor and titrates the blood to a pH value
just above the value at which the Root effect is initiated (1). In
this way, only a small amount of acid needs to be released to
switch on the Root effect during passage of the choriocapillaris, and the countercurrent concentration of acid, especially
of carbon dioxide, is reduced. This scenario indeed could
build up high oxygen partial pressure values with only a
minor acidification of the blood. In this context, it is important
to keep in mind that, in contrast to the swim bladder, where
the oxygen partial pressure necessary to drive diffusional oxygen transport into the swim bladder lumen increases with
increasing water depth, the choriocapillaris oxygen partial
pressure must only be high enough to meet the oxygen
requirement of the retina. At this point, no further increase in
oxygen partial pressure is necessary. Accordingly, the length
of the capillaries of the choroid rete, which is crucial for the
maximal countercurrent multiplication that can be achieved,
is short compared with the length of capillaries in most swim
bladder retia mirabilia.