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Pompeii Worms" Polychètes and Their Epibiotic Bacteria Associations Bactériennes

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Pompeii Worms __------------------------------------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 Relationships between Bactcria association Sources hydrothennales the "Pompeii worms" Polychètes and their epibiotic bacteria 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 les "vers de Pompéi" et leurs bactéries épibiontes 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, 4- 7 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, The so-called "Pompei worms" (polychaetous annelids) well-oxygenated scawater. This mixing results in a sharp live on active hydrothermal edifices on the East Pacific horizontal gradient, where the tcmperature changes within Rise at depths of about 2600 m. They secrete organic a few decimetres from 200° to 1.8°C. The Pompeii worms tubes (Vovelle, Gaill, 1986 ; Gaill, Hunt, 1986) on the are confincd to the cooler part of the gmdient, betwcen peripheral surface of certain chimneys and zinc-sulphide approximately 20° and 60°C (Dcsbruyères et al., 1982), ---------------------------------------------------------------------------------------------- 147 F. GAILL, D. DESBRUYÈRES, L. LAUBIER this being the range of their temperature tolerance defined bifurcatc digitations which are regular in form and as accurately as is possible. A minor portion of the worm, arrangement the branchiae, is positioned at the opening of the tube In the antcrior region, dorsal segmentary giandular bathing in ambient water, whereas the greater portion is bourrelets are undivided (Fig. 1), whereas posteriorly they enclosed within the tube these animaIs secrete. The divide into an increasing number of subsections (Fig. 1 Pompeü worms comprise two spccies: Alvinella and 2 c, d). Concurrently the non-glandular inter­ pompejan a and Alvinella caudata (Desbruyères, Laubier, segmentary spaces increasc to a maximum size in the 1986), primitively considered as two forms of the same median region where the glandular bourrelets are not species (Desbruyères, Laubier, 1980). found. In the caudal region, the intcrsegmentary spaces are Several polychaetous species inhabit the dcep sea less dilated than in the median region, but are nevertheless hydrothermal chimneys, but the Pompeii worms are the more important than in the anterior region. In these most spectacular with respect to the density of the bacteria spaces, bacilli, cocci and filamentous bacteria are covering their dorsal part (Gaill et al., 1984 a). These associated with cuticular secretions, forming "cluster-like" bacteria have bcen described (Gaill et al., 1987; structures (Fig. -l, 2 c, d). These associations are found 1 Desbruyères et al., 1985), but the biological significance along the cntire length of the animal (Fig. 1). However, t of the bacteria/worm association remains unclear. The the density and dimensions of filamentous bactcria increase 1 Pompeii worms are devoid of the endosymbiotic posteriorly (Fig. 1, 2 d). Large filamentous bacteria, , associations (Storch, Gaill, 1986) described and studied in preferentially inserted in the apical portion of posterior 1 vestimentiferans (Cavanaugh et al., 1981; Bosch, Grassé, notopods, form a veritable belt, easily visible to the naked 1 1984 b; Felbeck, 1981) and molluscs (Cavanaugh, eye (Fig. 2 a). a, 1 1983; Fiala-Medioni, 1984). They present only epibiotic The epidermis of the animal consists of an epithelium 1 bacteria. limited distally by a cuticle (Fig. 3 b) composed of a The purpose of this study was to determine more precisely network of collagen fibres and bordered by an electron­ 1 the morphological relationship betwecn the bacteria and dense epicuticle (Fig. 3 a). The epidermal cells issue ~ the worm epidermis and to inv~stigate whether the ! underlying cell epidermis is modified by the presence of Parapodia transformation 1 bacteria associations and, - if so - in what manner. 1 Answers to these questions would provide some co , indications conceming the local environ ment of the animal _\,?-.tf.Jlk\ , and its epidennal reactions, as well as information about ~~~" ! what may be called the process of exosymbyosis. 1 \ 1 MATERIAL AND METHODS 1 f Alvinella pompejan a spccimens were collected at 200 50'N and 109°W with the research submersible Alvin (April­ May 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 Increase of dorsal glandular torus parceiling sputter-coated with gold mctal. The samples wcre examined using a Cambridge Sloo SEM (IFREMER, Centre de Brest, France). RESULTS Whereas the cephalic and branchial regions of the two Increase of filamentous bacteria density morphological forros within the species Alvinella are ~ identical; the posterior sections of the body differ in their Figure 1 external anatomy, if not in thcir organization. Diagram comparing morph%gica/ modifications in Alvinella cau­ r In the caudata species, there is a gross dccrease in body data and the associated bacteria densily. ~ diameter from the 49th to the 54th segment. The Schéma comparanl les modificaùons morphologiques d'A/vine//a f notopodia are elongated in this rcgion and bear four or five caudata el la densité des bactéries associées. ~ ~ ------------------------------------------------------------------------------------------------- " - 148 ~ 1 "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 inter­ segmentary space (see 3 in fig. 2). a, inter­ segmentary 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, di­ gitation; 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 recou­ verte d'une portion de cuticule recouvrant les microvillosités ; e, base des filaments bacté­ riens ; f, bactéries filamenteuses ; m, microvil­ losités; C) Associations en bouquet de l'espace intersegmentaire (voir 3 sur la fig. 2). a, espace intersegmentaire ; s,
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