540
14 Glycolysis
route was first discovered in 1977 in the heart of
the oyster Crassostrea gigas and is, in fact, of relatively great importance for the mussel heart; it
occurs in other tissues of the molluscs but not at
all in the arthropods [68, 199]. Succinate production from aspartate has also been detected during
hypoxia in heart and skeletal muscle of mammals
and fish. Malate, which is an intermediate of succinate synthesis from glycogen or aspartate, is
found at such high concentrations in the tissues of
several oligochaetes, leeches and the larvae of
non-biting midges that it is a significant substrate
at least during the initial phase of habitatdependent anaerobiosis; the concentration is
14-20 fLmol/g in Eisenia foetida, 30-40 fLmol/g in
Hirudo medicinalis, about 50 fLmol/g in the tubificid Lumbriculus variegatus, and 40-50 fLmol/g in
Chaoborus fiavicans [288].
Activity-dependent anaerobiosis and (natural
or experimental) anoxia can lead to different end
products in the same animal, or even in the same
muscle tissue. The products of the activitydependent process are mainly those of pyruvate
reduction, such as lactate or opine, whereas in the
habitat-dependent process succinate, volatile
fatty acids and alanine are also produced. There
are some well-investigated examples: The mussel
Ensis directus synthesizes octopine during rapid
digging movements but produces mainly strombine, together with succinate, propionate, acetate
and alanine, under anoxic conditions. SpinuncuIus nudus also produces octopine during activitydependent anaerobiosis but synthesizes the products of the succinate pathway together with
strombine during the habitat-dependent process.
The burying action of Are nicol a marin us results in
alanopine but the initial phases of the habitatdependent process produce strombine. Cardium
tuberculatum accumulates octopine in its foot
during fleeing jumps, but produces lactate under
conditions of experimental anoxia [71, 84, 156,
225, 231, 288]. It is of particular interest that different pyruvate reductases are quite often
involved in the two types of anaerobiosis (p. 537).
The accumulation of the acidic end products of
anaerobic glycogenolysis leads to alterations in
the proton balance of the cells and of the whole
animal. One proton arises per carboxyl group
produced, i.e. 1 mol H+ per mol end product,
irrespective of its chemical nature (lactate, opine,
alanine, acetate, propionate); succinate synthesis
yields two protons per mole. This has led to the
hypothesis that the proton stoichiometry of anaerobiosis is independent of the prevailing metabolic pathway [102]. In fact, the situation is complicated by further metabolic processes, and the
proton balance of anaerobiosis may vary greatly
depending upon the substrate consumed and the
end product formed. For example, the number of
protons produced in the succinate-propionate
pathway is lower when aspartate is the substrate
than when glycogen is used. The cleavage of
phosphagen consumes protons, whereas dephosphorylation of MgATp 2 - generates protons; furthermore, the Pi released from phosphagen or
ATP acts as an intracellular buffer. Analysis of the
proton balance of a tissue or of a whole organism
must also take into account the excretion of H+
and NH\ ions [195]. Anoxia occurring in the
presence of enhanced CO2 in the environment
(hypercapnia) leads to increased acidosis [116].
The degree of acidosis is reduced in some animals
by excretion of part of the end products. In this
case, the possibilities for exploiting fully the
remaining energy content of the end products by
oxidation to CO2 and water, or for using them in
gluconeogenesis, are forfeited after the return to
normal conditions. Excretion of lactate is found,
for example, in the crustaceans and also occurs to
a limited extent in the tadpoles of Rana catesbeiana [198]. Many molluscs and annelids secrete
propionate, acetate and sometimes succinate
[103, 105, 187,225]. Another way of reducing
anaerobic acidosis, namely the further metabolism of the acidic end products to ethanol, has
been adopted only by the larvae of the non-biting
midge Chironomus thummi, the free-living nematode Panagrellus redivivus, and the goldfish.
Ethanol is particularly easily disposed of by secretion into the aqueous environment [24,201,276].
In many free-living animal species several phases of anaerobiosis may be distinguished during
persistent anoxia. This is to be expected because
substrates such as aspartate are gradually used up
during the time needed for regulation of the
switch from aerobic to anaerobic energy production, and because the accumulation of various
metabolites alters the conditions for further cell
metabolism. In the initial phase, phosphagen is
consumed and aspartate is converted to succinate; during the subsequent reactions, propionate
(and sometimes also acetate) is produced as the
main product [83, 225, 288]. These changes with
time have been especially well investigated in
Arenicola marina. During the first 3 h, the phosphagen phosphotaurocyamine is used up, aspartate is metabolized to succinate and volatile fatty
acids, and pyruvate is metabolized to strombine
and L-alanine; the latter is racemized to a mixture
of L- and D-alanine. After 3 h, glycogen catabol-
14 Glycolysis
route was first discovered in 1977 in the heart of
the oyster Crassostrea gigas and is, in fact, of relatively great importance for the mussel heart; it
occurs in other tissues of the molluscs but not at
all in the arthropods [68, 199]. Succinate production from aspartate has also been detected during
hypoxia in heart and skeletal muscle of mammals
and fish. Malate, which is an intermediate of succinate synthesis from glycogen or aspartate, is
found at such high concentrations in the tissues of
several oligochaetes, leeches and the larvae of
non-biting midges that it is a significant substrate
at least during the initial phase of habitatdependent anaerobiosis; the concentration is
14-20 fLmol/g in Eisenia foetida, 30-40 fLmol/g in
Hirudo medicinalis, about 50 fLmol/g in the tubificid Lumbriculus variegatus, and 40-50 fLmol/g in
Chaoborus fiavicans [288].
Activity-dependent anaerobiosis and (natural
or experimental) anoxia can lead to different end
products in the same animal, or even in the same
muscle tissue. The products of the activitydependent process are mainly those of pyruvate
reduction, such as lactate or opine, whereas in the
habitat-dependent process succinate, volatile
fatty acids and alanine are also produced. There
are some well-investigated examples: The mussel
Ensis directus synthesizes octopine during rapid
digging movements but produces mainly strombine, together with succinate, propionate, acetate
and alanine, under anoxic conditions. SpinuncuIus nudus also produces octopine during activitydependent anaerobiosis but synthesizes the products of the succinate pathway together with
strombine during the habitat-dependent process.
The burying action of Are nicol a marin us results in
alanopine but the initial phases of the habitatdependent process produce strombine. Cardium
tuberculatum accumulates octopine in its foot
during fleeing jumps, but produces lactate under
conditions of experimental anoxia [71, 84, 156,
225, 231, 288]. It is of particular interest that different pyruvate reductases are quite often
involved in the two types of anaerobiosis (p. 537).
The accumulation of the acidic end products of
anaerobic glycogenolysis leads to alterations in
the proton balance of the cells and of the whole
animal. One proton arises per carboxyl group
produced, i.e. 1 mol H+ per mol end product,
irrespective of its chemical nature (lactate, opine,
alanine, acetate, propionate); succinate synthesis
yields two protons per mole. This has led to the
hypothesis that the proton stoichiometry of anaerobiosis is independent of the prevailing metabolic pathway [102]. In fact, the situation is complicated by further metabolic processes, and the
proton balance of anaerobiosis may vary greatly
depending upon the substrate consumed and the
end product formed. For example, the number of
protons produced in the succinate-propionate
pathway is lower when aspartate is the substrate
than when glycogen is used. The cleavage of
phosphagen consumes protons, whereas dephosphorylation of MgATp 2 - generates protons; furthermore, the Pi released from phosphagen or
ATP acts as an intracellular buffer. Analysis of the
proton balance of a tissue or of a whole organism
must also take into account the excretion of H+
and NH\ ions [195]. Anoxia occurring in the
presence of enhanced CO2 in the environment
(hypercapnia) leads to increased acidosis [116].
The degree of acidosis is reduced in some animals
by excretion of part of the end products. In this
case, the possibilities for exploiting fully the
remaining energy content of the end products by
oxidation to CO2 and water, or for using them in
gluconeogenesis, are forfeited after the return to
normal conditions. Excretion of lactate is found,
for example, in the crustaceans and also occurs to
a limited extent in the tadpoles of Rana catesbeiana [198]. Many molluscs and annelids secrete
propionate, acetate and sometimes succinate
[103, 105, 187,225]. Another way of reducing
anaerobic acidosis, namely the further metabolism of the acidic end products to ethanol, has
been adopted only by the larvae of the non-biting
midge Chironomus thummi, the free-living nematode Panagrellus redivivus, and the goldfish.
Ethanol is particularly easily disposed of by secretion into the aqueous environment [24,201,276].
In many free-living animal species several phases of anaerobiosis may be distinguished during
persistent anoxia. This is to be expected because
substrates such as aspartate are gradually used up
during the time needed for regulation of the
switch from aerobic to anaerobic energy production, and because the accumulation of various
metabolites alters the conditions for further cell
metabolism. In the initial phase, phosphagen is
consumed and aspartate is converted to succinate; during the subsequent reactions, propionate
(and sometimes also acetate) is produced as the
main product [83, 225, 288]. These changes with
time have been especially well investigated in
Arenicola marina. During the first 3 h, the phosphagen phosphotaurocyamine is used up, aspartate is metabolized to succinate and volatile fatty
acids, and pyruvate is metabolized to strombine
and L-alanine; the latter is racemized to a mixture
of L- and D-alanine. After 3 h, glycogen catabol-