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------------------------------------O-C-E-A-N-O-L-O-G-IC-A-A-C-T-A-1-98_8_-_N_O~S_P.~~~-Hydrothennal vents
Polychaeta
Bactcria association
Relationships between
the "Pompeii worms"
and their epibiotic bacteria
Sources hydrothennales
Polychètes
Associations bactériennes
Françoise GAILL a, Daniel DESBRUYERES b, Lucien LAUBIER C
a Centre de Biologie Cellulaire, Centre National de la Recherche Scientifique, École Pratique
des Hautes Etudes, 67, rue Maurice Günsbourg, 94200 Ivry-sur-Seine, Fmnce.
b Institut Français de Recherche pour l'Exploitation de la Mer, Centre de Brest, B.P. 337,
29273 Brest, France.
C IFREMER, 66, avenue d'Iéna, 75116 Paris, France.
ABSTRACf
The morphological relationship betwccn the so-callcd "Pompeii worms" (Alvinella caudata
and Alvinella pompejana) and their associatcd bacteria is describcd. Three main
morphological modifications are observcd in Alvinella caudata: segmental division and the
density and size of filarnentous bacteria incrcase in a gmdient manner from the anterior to the
posterior part. Such a gradient does not occur in ALvinella pompejana, which is characterized
by the presence of dorsal expansions associatcd with filamentous bacteria. The underlying
cell epidermis aspects are qui te different as far as bacteria association types are concerned,
espccially in the notopod part of Alvinella caudata. These results permit an overview of the
possible functioning of the biological ensemble constitutcd by the worm, its tube and the
associatcd bacteria.
Oceanol. Acta, 1988. Hydrothermalism, Biology and Ecology Symposium, Paris, 4-7
November, 1985, Proceedings, 147-154.
RÉSUMÉ
Relations entre
épibiontes
les
"vers
de
Pompéi"
et
leurs
bactéries
Les relations morphologiques entre les vers de Pompéi (Alvinella caudata et Alvinella
pompejana) sont décrites. Trois types de modifications morphologiques sont observés chez
Alvinella caudata : une division des segments ; la densité et la taille des bactéries
filamenteuses qui augmentent selon un gradient antéro-postérieur. Un tel gradient n'existe
pas chez Alvinella pompejana qui est caractérisée par la présence d'expansions dorsales
associées à des bactéries filamenteuses. Les aspects de l'épiderme sous-jacent varient suivant
le type d'association bactérienne présent, en particulier ceux de l'épiderme parapodial
d'Alvinella caudata. Ces résultats nous conduisent à présenter une synthèse du
fonctionnement du système biologique constitué par le ver, le tube et ses bactéries associées.
Oceanol. Acta, 1988. Actes du Colloque Hydrothcrmalisme, Biologie ct Écologie, Paris, 47 novembre 1985, 147-154.
INTRODUCTION
diffusers (Dcsbruyères et al., 1985) in zones of activ.e
mixing of hOl, reducing, acidic, mctal-rich fluid and cold,
well-oxygenated scawater. This mixing results in a sharp
horizontal gradient, where the tcmperature changes within
a few decimetres from 200° to 1.8°C. The Pompeii worms
are confincd to the cooler part of the gmdient, betwcen
approximately 20° and 60°C (Dcsbruyères et al., 1982),
The so-called "Pompei worms" (polychaetous annelids)
live on active hydrothermal edifices on the East Pacific
Rise at depths of about 2600 m. They secrete organic
tubes (Vovelle, Gaill, 1986 ; Gaill, Hunt, 1986) on the
peripheral surface of certain chimneys and zinc-sulphide
---------------------------------------------------------------------------------------------147
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F. GAILL, D. DESBRUYÈRES, L. LAUBIER
this being the range of their temperature tolerance defined
as accurately as is possible. A minor portion of the worm,
the branchiae, is positioned at the opening of the tube
bathing in ambient water, whereas the greater portion is
enclosed within the tube these animaIs secrete. The
Pompeü worms comprise two spccies: Alvinella
pompejan a and Alvinella caudata (Desbruyères, Laubier,
1986), primitively considered as two forms of the same
species (Desbruyères, Laubier, 1980).
Several polychaetous species inhabit the dcep sea
hydrothermal chimneys, but the Pompeii worms are the
most spectacular with respect to the density of the bacteria
covering their dorsal part (Gaill et al., 1984 a). These
bacteria have bcen described (Gaill et al., 1987;
Desbruyères et al., 1985), but the biological significance
of the bacteria/worm association remains unclear. The
Pompeii worms are devoid of the endosymbiotic
associations (Storch, Gaill, 1986) described and studied in
vestimentiferans (Cavanaugh et al., 1981; Bosch, Grassé,
1984 a, b; Felbeck, 1981) and molluscs (Cavanaugh,
1983; Fiala-Medioni, 1984). They present only epibiotic
bacteria.
The purpose of this study was to determine more precisely
the morphological relationship betwecn the bacteria and
the worm epidermis and to inv~stigate whether the
underlying cell epidermis is modified by the presence of
bacteria associations and, - if so - in what manner.
Answers to these questions would provide some
indications conceming the local environ ment of the animal
and its epidennal reactions, as well as information about
what may be called the process of exosymbyosis.
bifurcatc digitations which are regular in form and
arrangement
In the antcrior region, dorsal segmentary giandular
bourrelets are undivided (Fig. 1), whereas posteriorly they
divide into an increasing number of subsections (Fig. 1
and 2 c, d). Concurrently the non-glandular intersegmentary spaces increasc to a maximum size in the
median region where the glandular bourrelets are not
found. In the caudal region, the intcrsegmentary spaces are
less dilated than in the median region, but are nevertheless
more important than in the anterior region. In these
spaces, bacilli, cocci and filamentous bacteria are
associated with cuticular secretions, forming "cluster-like"
structures (Fig. -l, 2 c, d). These associations are found
along the cntire length of the animal (Fig. 1). However,
the density and dimensions of filamentous bactcria increase
posteriorly (Fig. 1, 2 d). Large filamentous bacteria,
preferentially inserted in the apical portion of posterior
notopods, form a veritable belt, easily visible to the naked
eye (Fig. 2 a).
The epidermis of the animal consists of an epithelium
limited distally by a cuticle (Fig. 3 b) composed of a
network of collagen fibres and bordered by an electrondense epicuticle (Fig. 3 a). The epidermal cells issue
Parapodia transformation
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MATERIAL AND METHODS
1
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Alvinella pompejan a spccimens were collected at 200 50'N
and 109°W with the research submersible Alvin (AprilMay 1979) and at 12°48'N and 103°56'W with the
submersible Cyana (March 1982) at 2600 m depth.
Ultrastructural studics were carried out on pieces of worm
fixed with 0,4 M cacodylate-buffered glutaraldehyde (3%
final concentration) at pH 7,2 and then posl-fixed with
osmium tetroxyde (1 % final concentration), and embedded
in Durcupan and Spurr resins. Thin sections were stained
with aqueous uranyl acetate and lead citrate, and examined
using a Philips EM 201 T E M (Centre de Biologie
Cellulaire, CNRS, Ivry-sur-Seine, France). Scanning
electron microscope observations were made on fixed
samples dehydratcd with ethanol, critical point dried and
sputter-coated with gold mctal. The samples wcre
examined using a Cambridge Sloo SEM (IFREMER,
Centre de Brest, France).
Increase of dorsal glandular torus parceiling
RESULTS
Whereas the cephalic and branchial regions of the two
morphological forros within the species Alvinella are
identical; the posterior sections of the body differ in their
external anatomy, if not in thcir organization.
In the caudata species, there is a gross dccrease in body
diameter from the 49 th to the 54th segment. The
notopodia are elongated in this rcgion and bear four or five
Increase of filamentous bacteria density
~
Figure 1
Diagram comparing morph%gica/ modifications in Alvinella caudata and the associated bacteria densily.
Schéma comparanl les modificaùons morphologiques d'A/vine//a
caudata el la densité des bactéries associées.
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"POMPE" WORMS" AND THEIR EPIBIOTIC BACTERIA
----------------------------------------------------------------------------------------------------Figure 2
A) posterior part of Alvinella caudata: the
notopods present digitations
(1,
2,
3).
Filamentous bacteria are white. d, digitation, f,
filamentous bacteria; p, notopod; s, setae; white
arrow, minerai particles.
B) Aspect of the dilated base of filamentous
bacteria from the notopods. This base is covered
by a portion of cuJicle which recovers
microvillies. e, base of filamentous bacteria; f,
ftlamentous bacteria; m, microvilli.
C) Cluster-like associations in the intersegmentary space (see 3 in fig. 2). a, intersegmentary space; s, subsection of segments.
D) Cluster-like associations in the caudal part
where filamentous bacteria are numerous. f,
ftlamentous bacteria; s, subsection of segments.
A) Partie postérieure d'Alvinella caudata : les
parapodes présentent des digitations (l, 2, 3).
Les bactéries filamenteuses sont blanches. d, digitation; f, filaments bactériens; p, parapode;
s, soie ; flèche blanche, particules minérales.
B) Aspect dilaté de la base des filaments
bactériens des parapodes. Cette base est recouverte d'une portion de cuticule recouvrant les
microvillosités ; e, base des filaments bactériens ; f, bactéries filamenteuses ; m, microvillosités;
C) Associations
en bouquet de l'espace
intersegmentaire (voir 3 sur la fig. 2). a, espace
intersegmentaire ; s, partie de segment segmentée.
D) Associations en bouquet de la partie
postérieure où les bactéries filamenteuses sont
nombreuses. f, bactéries filamenteuses ; s, partie
de segment segmentée.
10wards cellular extensions of microvil1i which traverse
the cuticle perpendicularly (Fig. 3 e). These microvilli
ramify 10wards the epicuticle and their more distal portions
form epicuticular projections or ellipsoidal bodies on the
exterior of the epicuticle (Fig. 3 a). Also, SEM
observations of the surface integument reveal a granular
appearance associated with the presence of epicuticular
projections (Fig. 4 d).
The epithelium in the dorsal intersegmentary zones
consists of a layer of cells overlying a basal lamina. This
tissue is traversed by abundant blood vessels and is
proximal to numerous nerve terminations. The dorsal
epithelium comprises unspecialized cells and mucous cells
which are much less numerous in the dorsal glandular
flanges than in the ventral epithelium; they are absent in
the intersegmentary zone where unspecialized epidermal
cells occur. These cells are characterized by the presence of
Golgi apparatus, an abundance of granular endoplasmic
reticulum and the presence of numerous mitochondria.
Inclusions are present in large numbers in the cytoplasm:
vesicles of all sizes near the cellular apex, lysosomes of
various sizes, and spherulites, small vesicles containing
hererogeneous inaterial (Fig. 3 b). The course of the
plasma membrane in the lateral cellular portions is very
sinuous. Electron-dense accumulations, similar 10
glycogen "rosettes", are visible near the membranous folds
and arounds electron-clear areas (Fig. 4 e). Isolated bacteria
(Gaill et al., 1984 a) are present on the epidermal surface,
sorne of which are inserted at depth in the cuticle
(Fig. 4 d).
The cluster-like associations are very numerous in the
intersegmentary zones. Their presence around the cuticular
pinnules does not modify the general aspect of the
underlying cells in the anterior region of the animal (Fig.
3 d). In contrast, in the caudal region where bacterial
filaments are more numerous, the epidermal cells contain a
large concentration of glycogen vesicles (Fig. 3 e).
Mitochondria are also more numerous but Golgi
apparatus, endoplasmic reticular networks and lysosomes,
signifiers of exchange with the exterior, diminish in
importance. Cellular activity seems rather directed 10wards
storage.
The same type of cellular modifications was observed in
the epidermis of the parapodial digitations of the caudal
region. However, cytoplasmic glycogen is quantitatively
less significant there, whereas "spherocrystals" abound,
and the cytoplasm is dotted with electron-clear zones
--------------------------------------------------------------------------------------------------------149
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F. GAILL, D. DESBRUYÈRES, L. LAUBIER
---------------------------------------------------------------1
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Figure 3
A) Subcuticular bacteria in Alvinella camlala. b,
bacteria; e, epicuticle; f, collagenous fibril; p,
epicuticular projections.
B) General aspect of the cell epùJermis of
Alvinella caudata. c, cuticle; p, epùJermis.
C) The cell epidermis of the posterior notopods
(Alvinella caudata). b, filamen/ous bacteria; m,
microvilli; s, spherocrystal.
D) The base of a cluster-/ike assocation
(Alvinella caudata). c, cuticle; f, collagenous
fibre; l, lysosome; q, glycogen particles; v,
vacuole.
E) Aspect of the dorsal part of the Pompeii
worm epidermis. c, cuticle; g, glycogen
particles; m, microvilli; n, mitochondria; p, epicuticular projections.
A) Bactéries sous-cuticulaires chez Alvinella caudota. b, bactéries ; e, epicuticule ; f, fibres de
collagène; p, projections épicuticulaires.
B) Aspect général des cellules épidenniques d' AIvinella caudata. c; cuticule; p, épidenne.
C) Les cellules épidenniques des parapodes
postérieurs (Alvinella caudata). b, bactéries mamenteuses ; m, microvillosités ; s, sphérocristal.
D)
Bases des associations en bouquet
(Alvinella caudata). c, cuticule ; f, fibres de collagène; l, lysosome; q, glycogène; v, vacuole.
E) Aspect des cellules épidenniques de la panie
dorsale du ver de Pompéi. c, cuticule ; g, glycogène ; m, microvillosités ; n, mitochondries ;
p, projections épicuticulaires.
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(Fig. 3 c). The exchange surface area of the epidermal cells
and cytoplasm is diminished; microvilli are shorter and
non-branching (Fig. 3 c).
Filamentous bacteria are inserted at depth in the cutic1e of
the parapodial digitations, when they are present (Fig. 2
b). Their dilated discoid bases are covered by a relatively
smOOth portion of cutic1e, as observed by SEM; c1usters
of small-sized spherical elements occasionally surround the
insertions (Fig. 2 b). When the load of filamentous
bacteria becomes too great, the cuticle breaks away in
small flakes until it disappears entirely from sorne areas;
this is apparent in areas still containing impressions of
bacterial insertions on the microvilli. In areas devoid of
cutic1e, the proximal extremity of the filamentous bacteria
is attached to the same microvilli upon which it rests, at
the same time, remaining separated by a network of very
fine fibres (Fig. 3 c). 1EM studies show that shedding of
the cutic1e of the parapodial digitations is progressive; it
gradually undergoes a reduction in thickness, the number
of collagen fibres decreases and the epicutic1e, whose
surface appears smooth under the SEM, separates at the
level of the bacterial insertions.
The general body form of the species Alvinella pompejan a
is thick and regularly attenuated posteriorly. The notopodia
are all similar along the length of the body, with
exception of the two modified anterior segments. The
segmentary glandular bourrelets are evenly subdivided
along the length of the body, except for sorne postbranchial segments. The size of the intersegmentary spaces
increases only slightly from anterior to posterior; c1usterlike associations occur there but in a lesser density than in
Alvinella caudata. Epidermal formations (Fig. 4), unique
in annelid polychaetes, occupy the intersegmentary spaces
on the dorsal side, between the two rows of parapodia and
positioned ventral or dorsal to the notopodia themselves.
Expansions, attaining or surpassing 10 mm in length,
issue from epidermal "cupuliform" structures (Fig. 4 a)
arranged in a single or two altemating rows.
The epidermal "cupuliform" structures are composed of
glandular cells (Fig. 4 a). They are devoid of cutic1e, and
c1ustered microvilli are present at their apex. At the distal
extremity of these microvilli, spherical elements, with the
appearance of mucous secretions (Fig. 4 b), are emitted
and fuse together to form a reticulated mass of a fibrillar
appearance at the periphery (Fig. 4 e). Cellular secretory
activity is revea1ed in numerous vesic1es, well-developed
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"POMPEII WORMS" AND THEIR EPIBIOTIC BACTERIA
DISCUSSION AND CONCLUSIONS
At the base of the expansion, the surface was observed by
SEM to be smooth and consisting, at least exteriorly, of a
"anhyste" substance. Further away from the insertion,
most of this surface coating is broken up, revealing a
shaggy "hirsute" structure composed of more or less
entangled bacterial filaments. A transverse section of the
expansion observed by SEM (Fig. 4 b) showed that the
secretion was distributed in pseudo-concentric layers.
Sheathed fIlamentous bacteria of a slender diameter (0.3
J.Illl) colonize the peripheral internaI portions of the
expansion (Fig. 4 e), whereas larger-sized fIlamentous
bacteria (cells 10 ~ x 1.0 ~) seem to develop around
the distal regions. Bacterial colonization of the expansion
is never central and the bacteria multiply in the
polysaccharide matrix of the expansion (Fig. 4 e). These
expansions are general in AlvineUa pompejana, the same
in small individuals, but they may also be seen in lesser
quantities in AlvineUa caudata within the zone of reduction
of the body diameter (segments 50-65). They remain in
this case limited to segmentary zones latero-dorsal to sorne
segments and at the apex of the terminal digitation of the
notopodia. Nevertheless, the frequency of these structures
in Alvinella caudata is very reduced.
With the exception of particular cases at deep-sea and
coastal hydrothermal vents, bacterial epibioses in the
marine environment have been scantily described.
Cases of epibiosis are, evidently, more widespread in
hydrothermal communities, where practically aIl available
surfaces are heavily colonized by bacteria Jannasch and
Wirsen (1979) described major populations of fIlamentous
bacteria of the periostracum of Calyptogena magnifica and
thick covering of fme filaments attributed to the genera
Hyphomonas or Hyphomicrobium on the shell of the
giant mussel of the Galàpagos vents. Associated with
these fIlaments are curious trichomes, tentatively
attributed to Calothrix, a chemosynthetic cyanobacteria
(Jannasch, Wirsen, 1979). The black abalone, Haliotis
cracherodii, of the White Point infra-littoral hydrothennal
vents, carries on its shell a thick covering of fllamentous
bacteria of the genus Thiothrix (Stein, 1984). A number
of similar cases have also been observed in the patellifonn
gastropods that colonize the tubes of Riftia pachyptila.
.The unavoidable sUSpicion must be that these epibioses
are functionally advantageous, to the point of an actual
Figure 4
A) Dorsal expansion of Alvinella pompejana. c,
cU/icle; g, glandular cells; n, matrix of the dorsal
expansion; p, columnar cells; m, muscles.
B) Cross·section of the dorsal expansion (SEM).
White arrows, filamentous bacteria;
C) Glandular cells which secrete the dorsal expansion
(TEM). e, glandular cells; l, lyso-somes; s,
secretions; v, microvilli; x, mitochon-dria.
D) Insertion of bacteria insük the cU/icle (Alvinel-Ia
caudata) (SEM).
E) Aspect of the matrix of the dorsal expansion
(TEM). n,fibrillar matrix; b, bacteria.
A) Expansion dorsale d' Alvinella pompejana. c,
cuticule; g, cellule glandulaire; n, matrice des expansions dorsales ; p, cellule de soutien ; m, muscles.
B) Coupe transversale d'une expansion dorsale (MEB).
Flèche blanche, bactéries fIlamenteuses.
C) Cellules sécrétrices de l'expansion dorsale (MET).
e, cellule sécrétrice ; l, lysosome ; s, sécré-tions ; v,
microvillosités ; x, mitochondries.
D) Insertion bactérienne dans la cuticule (Alvinel-la
caudata) (MEB).
E) Aspect de la matrice de l'expansion dorsale (ME1).
n, matrice fibrillaire ; b, bactéries.
-----------------------------------------------------------------------------------------------------151
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t=. GAILL, D. DESBRUYËRES, L. LAUBIER
symbiosis in the mutualistic sense of the term. Very
different, without doubt, is the case of bacterial cpibiosis
present on the branchial filaments of limpets from vents
of the Juan de Fuca Ridge. Thcse bacterial filaments are
frequenüy endocytozed by the epithelial cells and then
lysed in cytoplasmic organelles similar to lysosomes (De
Burgh, Singly, 1984). The importance of this process in
the nutrition of the animal is again, however, difficult to
estimate.
In the polychaetes of hydrothermal vents of the East
Pacific Rise, several cases of bacterial epibiosis were
observed in our samplcs collectcd at l3°N. In the
polynoids of the genus Lepidonotopodium, bacteria are
frequenüy present on the brisües of the notopodia and on
the elytra (pettibone, 1984). In llesiolyra bergi, which
colonizes the tubes secreted by Alvinella, the notopodial
brisües serve as a substrate for an abundant covering of
filamentous bacteria. The digestive tract of the Serpulidae
shows numerous epibioses whose functional significance
is againenigmatic (Desbruyères et al., 1985). However,
none of these epibioses possess the characteristics of those
of Alvinella; the exceptional quantitative significance,
diversity of bacterial epibiotic bases, and consistency of
bacterial colonization in aIl individuals observed,
irrespective of their size and segment numbers.
Exarnination of another Alvinellid, Paralvinella grasslei
(Desbruyères, Laubier, 1982), which lives in the same
environment as Alvinella, reveals a very differcnt aspect of
this epibiosis. Although its integument bas a very similar
structure 10 that of Alvinella (Lepescheux, in press),
intersegmentary epibiosis is extrcmely reduced and.
bacterial epibiosis on the parapodia is non-existent.
• Cluster-like assoclauons arc charactcrizcd by their
morphological relationship with the cuticle fibre and the
surrounding mineraI storage which does not exist in the
other types of bacteria association (Gaill et al., 1984 b).
The undcrlying cclI epidermis does not differ from the
other supportive ceUs of the worm. A fcw of these bacteria
can he in contact with the cclI epidermis by the way of the
epicuticular projections. It seems tbat the collagenous
fibres act as a physical substrate which permits the
bacteria to exist in a pcculiar microenvironment where
numerous worm secretions are available.
• The third type of association occurs only in the
pompejana species, and is in direct relationship with the
cell epidermis. The underlying cells differ markedly from
the supportive ceUs in their secretory activity. Bactcria are
inserted in the secretions of the worm without contact
with the cell epidermis.
A single observation suggesLS that the attachment of
bacteria on the cuticle of Alvinella is not a passive
phenomenon comparable to the attachment of bacteria on
an inert submerged surface. The preferential attachment of
bacteria in the intcrsegmentary space on unusual epidermal
secretions leads us to hypothesize an actual mUlualistic
association between the worm and the bacterial epibionts.
In our study, two different reactions of the epidermisof the
Pompeii worms have been established. In the case of the
dorsal intersegmentary spaces, particularly in the posterior
region, the epidermal ceUs play a role in the storage of
organic and mineral compounds. Experiments with in situ
labelling have shown that absorption of low molecular
weight organic compounds takes place in that zone
(Alayse-Danet et al., 1985; 1986). In contrast, at the level
of the parapodial digitations, the cellular exchange surfaces
are rcduced. In that rcgion, Laubier et al. (1983) found
evidence of significant concentrations of sulphur and Gaill
et al. (1984 b) have locatcd, in the lysosomes and
spherocrystals, high concentraûons of seveml mineml
elements: S, As, Zn, Fe, Cu, P and Al.
Results of in situ labelling experiments (Alayse-Danet et
al., 1986) show a weak absorption of dissolved organic
compounds by the epidermis of the parapodial digitations.
Cellular characteristics also show that the uptake is
rcduced where the epidermis stores waste products and
mineraI clements. The nature of these stored materials
indicates that they have bcen translocated from the internal
environment of the animal (Gaill et al., 1984 b), and that
the parapodial digitations and their epibioûc bacteria may
be involved in detoxification processes of the animal
(Cosson et al., 1986). Baross and Deming (1985)
incubatcd a specimen of Alvinella caudata at in situ
temperature and pressure conditions in hydrothermal fluid:
microbial sulphate reduction was evident in an intense
precipitation of sulphur, indicating that the filarnentous
bacteria Lake part in the metabolism of sulphur
compounds.
The functional significance of the epibioûc bacteria of the
dorsal expansions in Alvinella pompejan a is even more
enigmatic. The extent of this association is unique in
marine invertebrates. These filamentous bacteria are
extracellular but seem LO divide actively in a
polysaccharide substance secreted by the animal. The
incorporation of 3H-Thymidine by the bacteria at the base
of the expansion in in situ experiments confirms this
Sorne epicuticular hacteria are observed in the two
Alvinella species (Fig. 3 a; Gaill et al., 1987) but they are
less numerous than epibiotic ones. This kind of
association has been mentioned in sorne gutless annelids
(Giere, 1981; Richards et al., 1982), and it scems that it is
the second case where such an occurrence is mentioned in
enteric polychaetes (Hausmann, 1982), the polynoids
elytra being apart.
SEM and MET observations show tbat the bacteria
distribution is not a random one. It is more accurate in the
caudata species where three main aspects were pointed out
segmental division, and the density and size of filarnentous
bacteria increase from the anterior to the posterior part in a
gradient manner. Such a gradient does not occur in the
pompejan a species, which is characterizcd by the presence
of dorsal expansions associated with filarnentous bacteria.
The underlying cell epidermis aspects arc quite different
with respect to the bacteria association types (which are
always extracellular), each type having a single morphological relationship with the cclI surface:
• One such type is directly inserted on the cell epidermis
close to the ceU microvilli. This is the case of the
filarnentous bacteria associatcd with Alvinella caudata
parapods. These epidermal parts lack cuticle, and the
activity of the supportive cells as weIl as the exchange
surfaces are reduccd, which suggests a stomge rather than
an exchange activity, even if the bacteria arc direcüy in
contact with the cell microvilli. It is not known whether
the cuticle disappearance is a consequence of bacterial
activity or of cclI activity relatcd to the worm physiology.
152
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"POMPE Il WORMS" AND THEIR EPIBIOTIC BACTERIA
fIlamentous bacteria (Gaill, Hunt, 1986) passes a hot (20°60°), acidic fluid with Iittle dissolved oxygen and a high
concentration of reducing gases and metal species. This
tube is an environment favourable to the multiplication of
chemosynthetic bacteria which provide food for the worm;
food in particulate form (Desbruyères et al., 1983; Baross,
Deming, 1985) collected by the protractile buccal
tentacles, in the form of dissolved organic material
absorbed through the body wall in the dorsal
intersegmentary zones and by the branchiae. However, this
exceptional environment, rich in organic matter, is also
10xic because of its metal content, its low oxygen fugacity
and acidic pH. The Pompeii worms have blood pigments
well adapted to life in such an environment (Terwilliger,
Terwilliger, 1984). The ensemble of fùamentous chemoorganotrophic genera Sphaerotilus, Herpetosiphon .or
Streptothrix may actively participate in the fluid
detoxification. Thus, this appears 10 be a complex
symbiotic association in the mutualistic sense, although
well opened 10 the exterior. The worm provides the carbon
source for the bacteria in the form of respired CÛ2 and
organic material, the bacteria provide particulate and
dissolved organic matter for the worm and, in the case of
. the chemo-organotrophs, participate in detoxification.
hypothesis. (Alayse-Danet et al., 1986). Electron
microscoPIC observations, as weIl as the absence of
incorporation of 14C-bicarbonate lead us 10 surmise a
heterotrophic or mixotrophic metaboIism coupled to the
sulphur cycle, as in bacteria of the genera Thiothrix or
Beggiatoa.
The observations described here, 10gether with the
experimental data (Alayse-Danet et al., 1985; 1986) do not
adequately explain the functional relationship between the
epibiotic bacteria and the Pompeü worm. Nevertheless,
the work of Tuttle et al. (1983) as weIl as the results of
cultures of epibiotic bacteria (Gaill et al., 1986) on
various media (Baross media, Strohl media and the 2216E
media of Oppenheimer and ZoBeIl) show that the
metabolism of this apparent bacterial "community" is very
diverse, ranging from strict chemoautotrophy to
heterotrophy.
Let us now propose an overview of the functioning of the
biological "ensemble" constituted by the worm and its
tube, as well as the tube internaI environment, and the
associated bacteria. Through the tube, intemally lined by
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