270
7 Respiratory Pigments
whereas S. corrugatus has haemoglobin. In Serpula vermicularis, both pigments are present in
the same animal. In this case the blood is greenish-brown with absorption maxima of 605 and
577 nm, corresponding to the a-bands for chlorocruorin and haemoglobin (Table 7.1). There is
about 60 % protein-bound spirographis haem and
40 % protohaem, and as these have as yet proved
impossible to separate, it may be that there is
only one protein present with all the properties of
a typical extracellular annelid pigment and bearing both prosthetic groups on the same molecule
[174, 176].
Coelom cell haemoglobins are found in polychaetes of the families Glyceridae, Terebellidae,
Opheliidae, Capitellidae and Ceratulidae, occurring together with extracellular blood haemoglobin in the terebellids Amphitrite ornata and Thelepus crispus. The coelom cell haemoglobins are all
monomers of about 14 kDa in the terebellids, and
32-kDa dimers in the opheliid Travisia. The erythrocytes of the "blood worm" Glycera dibranchiata
(Glyceridae) contain five to six monomeric haemoglobins of about 17 kDa and at least six globin
chains of the same size; on oxygenation these
form octamers and higher polymers by selfassociation. The monomers M-II and M-IV and
the components Pl, P2 and P3 of the polymer
fraction have been completely sequenced and P4,
P5 and P6 have been partially sequenced. The
five complete sequences include 39 invariant
positions. A further 44 positions are found in all
three polymeric globins but not in the two monomers. In the two monomeric globins, the distal
E7-His is replaced by leucine, which is no longer
able to stabilize the Hb02 by an H-bridge. Some
of the haemoglobins of Glycera and of the larvae
of the non-biting midge genus Chironomus
include conformational isomers with the haem
rotated 180 0 , as has already been described for
vertebrate myoglobins. This isomerism has, of
course, functional consequences [3, 122, 189].
The Glycera haemoglobin has a unique, extremely rapid O2 dissociation (Table 7.5). In
addition to blood and coelom cell haemoglobins,
the annelids also have myoglobins. These are generally monomers with a molecular size of about
16 kDa, although those of Travisia foetida are
dimeric. Dimeric myoglobins are otherwise only
encountered in the molluscs [163].
The coelom cells of the echiurid Urechis caupo
contain several tetrameric haemoglobins and the
muscles possess a monomeric myoglobin. The
haemoglobins show no cooperativity and no Bohr
effect. At least five polypeptides, which differ
only slightly from each other, are detectable in
the haemoglobins, suggesting that U. caupo possesses several very similar globin genes. The
amino acid sequence of globin F-I has been
determined directly and via the cDNA; the chain
of 141 amino acids is ~-like with well-formed D
helices, but shows no more than 20 % sequence
similarity to other globins. The CD1-Phe and the
proximal F8-His are conserved, whereas the distal E7-His is replaced by glutamine. Compared
with human Hb A, only 2 each of the 17 al~l and
the 13 al~2 contacts are present. The subunits are
so arranged in the homotetrameric F-I molecules
that the GIH helices lie at the outer surface of the
molecule and not at the inner surface, as in the
vertebrate haemoglobins. In this respect, F-I
resembles the heterotetrameric haemoglobins of
the mussel family Arcidae (p.271), although the
contacts between the subunits in Urechis and the
Arcidae are very different [117].
The haemoglobins of the echiurid Thalassema
mellita have rather deviant properties. Here,
there are two disulphide-linked dimers and
smaller amounts of a monomer, which in total are
made up from three different polypeptide chains
of 13-16 kDa. One of the dimeric haemoglobins
is a heterodimer having one chain in common
with the monomeric haemoglobin; the other is a
homodimer composed of chains of the remaining
type. The coelom cells and their lysate show
cooperative O2 binding with n = 1.5-1.9, but the
isolated haemoglobin has little cooperativity
(n = 1.0-1.3) [172].
7.2.2 Haemoglobins of the Molluscs
Amongst the molluscs there are various haemoglobin types with characteristic distributions.
High molecular weight extracellular haemoglobins are found only in the aquatic pulmonate
snails of the family Planorbidae; otherwise, the
typical respiratory pigment of the gastropods is
haemocyanin. Mussels of the families Carditidae
and Astartidae have a further type of extracellular haemoglobin. Haemoglobin-containing erythrocytes are found in mussels from at least seven
families, but only a few species of the Arcidae
have been examined in any detail. Myoglobins
are present in the radula and buccal muscles of
the polyplacophores and the gastropods, and in
the shell adductors and foot muscle of the mussels; in fact, intracellular haemoglobins are also
found in the heart and in gill and nerve cells of
some molluscs [163].
7 Respiratory Pigments
whereas S. corrugatus has haemoglobin. In Serpula vermicularis, both pigments are present in
the same animal. In this case the blood is greenish-brown with absorption maxima of 605 and
577 nm, corresponding to the a-bands for chlorocruorin and haemoglobin (Table 7.1). There is
about 60 % protein-bound spirographis haem and
40 % protohaem, and as these have as yet proved
impossible to separate, it may be that there is
only one protein present with all the properties of
a typical extracellular annelid pigment and bearing both prosthetic groups on the same molecule
[174, 176].
Coelom cell haemoglobins are found in polychaetes of the families Glyceridae, Terebellidae,
Opheliidae, Capitellidae and Ceratulidae, occurring together with extracellular blood haemoglobin in the terebellids Amphitrite ornata and Thelepus crispus. The coelom cell haemoglobins are all
monomers of about 14 kDa in the terebellids, and
32-kDa dimers in the opheliid Travisia. The erythrocytes of the "blood worm" Glycera dibranchiata
(Glyceridae) contain five to six monomeric haemoglobins of about 17 kDa and at least six globin
chains of the same size; on oxygenation these
form octamers and higher polymers by selfassociation. The monomers M-II and M-IV and
the components Pl, P2 and P3 of the polymer
fraction have been completely sequenced and P4,
P5 and P6 have been partially sequenced. The
five complete sequences include 39 invariant
positions. A further 44 positions are found in all
three polymeric globins but not in the two monomers. In the two monomeric globins, the distal
E7-His is replaced by leucine, which is no longer
able to stabilize the Hb02 by an H-bridge. Some
of the haemoglobins of Glycera and of the larvae
of the non-biting midge genus Chironomus
include conformational isomers with the haem
rotated 180 0 , as has already been described for
vertebrate myoglobins. This isomerism has, of
course, functional consequences [3, 122, 189].
The Glycera haemoglobin has a unique, extremely rapid O2 dissociation (Table 7.5). In
addition to blood and coelom cell haemoglobins,
the annelids also have myoglobins. These are generally monomers with a molecular size of about
16 kDa, although those of Travisia foetida are
dimeric. Dimeric myoglobins are otherwise only
encountered in the molluscs [163].
The coelom cells of the echiurid Urechis caupo
contain several tetrameric haemoglobins and the
muscles possess a monomeric myoglobin. The
haemoglobins show no cooperativity and no Bohr
effect. At least five polypeptides, which differ
only slightly from each other, are detectable in
the haemoglobins, suggesting that U. caupo possesses several very similar globin genes. The
amino acid sequence of globin F-I has been
determined directly and via the cDNA; the chain
of 141 amino acids is ~-like with well-formed D
helices, but shows no more than 20 % sequence
similarity to other globins. The CD1-Phe and the
proximal F8-His are conserved, whereas the distal E7-His is replaced by glutamine. Compared
with human Hb A, only 2 each of the 17 al~l and
the 13 al~2 contacts are present. The subunits are
so arranged in the homotetrameric F-I molecules
that the GIH helices lie at the outer surface of the
molecule and not at the inner surface, as in the
vertebrate haemoglobins. In this respect, F-I
resembles the heterotetrameric haemoglobins of
the mussel family Arcidae (p.271), although the
contacts between the subunits in Urechis and the
Arcidae are very different [117].
The haemoglobins of the echiurid Thalassema
mellita have rather deviant properties. Here,
there are two disulphide-linked dimers and
smaller amounts of a monomer, which in total are
made up from three different polypeptide chains
of 13-16 kDa. One of the dimeric haemoglobins
is a heterodimer having one chain in common
with the monomeric haemoglobin; the other is a
homodimer composed of chains of the remaining
type. The coelom cells and their lysate show
cooperative O2 binding with n = 1.5-1.9, but the
isolated haemoglobin has little cooperativity
(n = 1.0-1.3) [172].
7.2.2 Haemoglobins of the Molluscs
Amongst the molluscs there are various haemoglobin types with characteristic distributions.
High molecular weight extracellular haemoglobins are found only in the aquatic pulmonate
snails of the family Planorbidae; otherwise, the
typical respiratory pigment of the gastropods is
haemocyanin. Mussels of the families Carditidae
and Astartidae have a further type of extracellular haemoglobin. Haemoglobin-containing erythrocytes are found in mussels from at least seven
families, but only a few species of the Arcidae
have been examined in any detail. Myoglobins
are present in the radula and buccal muscles of
the polyplacophores and the gastropods, and in
the shell adductors and foot muscle of the mussels; in fact, intracellular haemoglobins are also
found in the heart and in gill and nerve cells of
some molluscs [163].