94
Verena TUNNICLIFFE et al.
populations include the normal deep sea, the seafloor,
and sediments underlying it.
Symbioses
A great deal of organic-matter synthesis occurs in symbiotic associations between bacteria and invertebrate
hosts, in which the chemosynthetic symbionts convert
carbon dioxide into organic matter which nourishes
themselves and their hosts. Vestimentiferan and bivalve
symbioses in seep environments are dependent on
aerobic oxidation of sulphide or methane. There
are three general models for the functioning of the
commonest forms of host–symbiont associations in
reducing environments: vestimentiferan tube worms,
vesicomyid clams, and bathymodiolid mussels (Fisher,
1990). The most integrated symbiosis occurs in the
tube worms, which have no mouth or digestive
system and are entirely reliant on their symbiotic
bacteria for nutrition. Pogonophora are all dependent
on symbiotic chemoautotrophic bacteria. Evidence
for sulphide-fuelled chemoautotrophy first came from
studies of the vent tube worm Riftia (Cavanaugh et al.,
1981; Felbeck, 1981). Similar dependence on sulphur
oxidation is known in the cold-seep genera Escarpia
and Lamellibrachia (see Southward et al. (1995) for
review). While no one has examined deep coldseep perviate Pogonophora for chemoautotrophy, it is
worth noting that methanotrophic bacteria are found
in one pogonophore species living at a shallow-water
methane seep (Schmaljohann and Fl¨ ugel, 1987), while
all other perviates investigated use sulphur-oxidizing
(thiotrophic) bacteria. In vestimentiferans, symbionts
are housed in a specialized organ known as the
trophosome. Substrates for microbial metabolism (HS
− ,
CO 2 , O 2 , etc.) are taken up at the branchial plume
and transported to the trophosome in the worm’s
blood by a multiglobin system (Zal et al., 1998).
Some vestimentiferans absorb sulphide through the
tube (Scott and Fisher, 1995).
The vesicomyid clams are filter-feeding animals,
but their digestive tract is highly reduced and they
are unable to survive without a supply of sulphide
for their symbionts. They host their symbionts in the
tissue of their large modified gills. Carbon dioxide
and oxygen diffuse directly into the gills from the
external environment, while the clams take up sulphide
into their blood through the foot, which they extend
into fractures or sediments where dissolved hydrogen
sulphide is available. The mussels also house their
symbionts in gill tissue, but have a functional digestive
system. The best-studied mytilid symbiosis is that
in Bathymodiolus thermophilus from the East Pacific
Rise, which hosts sulphide-oxidizing bacteria. It may
represent a more primitive symbiosis, compared to
the vestifmentiferans or the vesicomyid clams. For
example, it lacks the specific blood proteins for the
binding and transport of sulphide and oxygen that
are found in the vestimentiferans and clams. Unlike
the vesicomyid clams, filtration of particles of organic
matter from the surrounding water appears to provide a
supplement to the mussel’s nutrition (Page et al., 1990),
although the digestive tract is reduced in some species
(Von Cosel and Olu, 1998).
Methanotrophic symbioses are known in mussels
from seeps on the Louisiana Slope (Childress et al.,
1986) and the much deeper Florida Escarpment seeps,
as well as seep sites on the southern part of the
Barbados accretionary prism (Olu et al., 1996b). Some
mussels are known to house sulphide-oxidizing and
methanotrophic symbionts within a single bacteriocyte,
suggesting an ability to exploit both hydrogen sulphide
and methane as energy sources (Fisher, 1997). Nix et al.
(1995) have demonstrated growth rates, when methane
is abundant, to be comparable to those of shallow-water
mussels.
Three other families of bivalves bearing symbionts
are known from reducing habitats in both shallow
and deep water: Families Lucinidae, Solemyidae and
Thyasiridae. They are generally deep burrowers, requiring significant sediment accumulations. More than
20 symbioses, all thiotrophic, have been identified
among the lucinacean bivalves (Families Lucinidae and
Thyasiridae) (Anderson, 1995), and several more have
been described among the solemyids (Fisher, 1990).
Lucinids, present in sediments from the intertidal
zone to the deep-sea, host symbiotic bacteria in their
fleshy gills. Thyasirids are related bivalves which may
represent a more ancestral stage in the association with
symbionts, as the microbes are extracellular and sometimes quite scarce. Dependence on chemoautrophic
symbiosis has not been demonstrated for cold-seep
species belonging to any of these three families (Sibuet
and Olu, 1998).
An unusual methanotrophic symbiosis in a new
species of cladorhizid sponge has been described from
mud-volcano seeps on the Barbados accretionary prism
(Vacelet et al., 1995). While symbiotic bacteria are
common in sponges, this is the first case of an
Verena TUNNICLIFFE et al.
populations include the normal deep sea, the seafloor,
and sediments underlying it.
Symbioses
A great deal of organic-matter synthesis occurs in symbiotic associations between bacteria and invertebrate
hosts, in which the chemosynthetic symbionts convert
carbon dioxide into organic matter which nourishes
themselves and their hosts. Vestimentiferan and bivalve
symbioses in seep environments are dependent on
aerobic oxidation of sulphide or methane. There
are three general models for the functioning of the
commonest forms of host–symbiont associations in
reducing environments: vestimentiferan tube worms,
vesicomyid clams, and bathymodiolid mussels (Fisher,
1990). The most integrated symbiosis occurs in the
tube worms, which have no mouth or digestive
system and are entirely reliant on their symbiotic
bacteria for nutrition. Pogonophora are all dependent
on symbiotic chemoautotrophic bacteria. Evidence
for sulphide-fuelled chemoautotrophy first came from
studies of the vent tube worm Riftia (Cavanaugh et al.,
1981; Felbeck, 1981). Similar dependence on sulphur
oxidation is known in the cold-seep genera Escarpia
and Lamellibrachia (see Southward et al. (1995) for
review). While no one has examined deep coldseep perviate Pogonophora for chemoautotrophy, it is
worth noting that methanotrophic bacteria are found
in one pogonophore species living at a shallow-water
methane seep (Schmaljohann and Fl¨ ugel, 1987), while
all other perviates investigated use sulphur-oxidizing
(thiotrophic) bacteria. In vestimentiferans, symbionts
are housed in a specialized organ known as the
trophosome. Substrates for microbial metabolism (HS
− ,
CO 2 , O 2 , etc.) are taken up at the branchial plume
and transported to the trophosome in the worm’s
blood by a multiglobin system (Zal et al., 1998).
Some vestimentiferans absorb sulphide through the
tube (Scott and Fisher, 1995).
The vesicomyid clams are filter-feeding animals,
but their digestive tract is highly reduced and they
are unable to survive without a supply of sulphide
for their symbionts. They host their symbionts in the
tissue of their large modified gills. Carbon dioxide
and oxygen diffuse directly into the gills from the
external environment, while the clams take up sulphide
into their blood through the foot, which they extend
into fractures or sediments where dissolved hydrogen
sulphide is available. The mussels also house their
symbionts in gill tissue, but have a functional digestive
system. The best-studied mytilid symbiosis is that
in Bathymodiolus thermophilus from the East Pacific
Rise, which hosts sulphide-oxidizing bacteria. It may
represent a more primitive symbiosis, compared to
the vestifmentiferans or the vesicomyid clams. For
example, it lacks the specific blood proteins for the
binding and transport of sulphide and oxygen that
are found in the vestimentiferans and clams. Unlike
the vesicomyid clams, filtration of particles of organic
matter from the surrounding water appears to provide a
supplement to the mussel’s nutrition (Page et al., 1990),
although the digestive tract is reduced in some species
(Von Cosel and Olu, 1998).
Methanotrophic symbioses are known in mussels
from seeps on the Louisiana Slope (Childress et al.,
1986) and the much deeper Florida Escarpment seeps,
as well as seep sites on the southern part of the
Barbados accretionary prism (Olu et al., 1996b). Some
mussels are known to house sulphide-oxidizing and
methanotrophic symbionts within a single bacteriocyte,
suggesting an ability to exploit both hydrogen sulphide
and methane as energy sources (Fisher, 1997). Nix et al.
(1995) have demonstrated growth rates, when methane
is abundant, to be comparable to those of shallow-water
mussels.
Three other families of bivalves bearing symbionts
are known from reducing habitats in both shallow
and deep water: Families Lucinidae, Solemyidae and
Thyasiridae. They are generally deep burrowers, requiring significant sediment accumulations. More than
20 symbioses, all thiotrophic, have been identified
among the lucinacean bivalves (Families Lucinidae and
Thyasiridae) (Anderson, 1995), and several more have
been described among the solemyids (Fisher, 1990).
Lucinids, present in sediments from the intertidal
zone to the deep-sea, host symbiotic bacteria in their
fleshy gills. Thyasirids are related bivalves which may
represent a more ancestral stage in the association with
symbionts, as the microbes are extracellular and sometimes quite scarce. Dependence on chemoautrophic
symbiosis has not been demonstrated for cold-seep
species belonging to any of these three families (Sibuet
and Olu, 1998).
An unusual methanotrophic symbiosis in a new
species of cladorhizid sponge has been described from
mud-volcano seeps on the Barbados accretionary prism
(Vacelet et al., 1995). While symbiotic bacteria are
common in sponges, this is the first case of an