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Interactions of Metallic Elements and Organisms Within Hydrothermal Vents

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Interactions of Metallic Elements and Organisms Within Hydrothermal Vents Cah. Biol. Mar. (1997) 38 : 43-50 Interactions of metallic elements and organisms within hydrothermal vents Richard P. COSSON and Jean-Paul VIVIER* ISOMER-CNRS-EP 61-Faculté de Pharmacie, 1 rue Gaston Veil 44000 Nantes - France fax: (33) 2 40 41 28 61 - E-mail: [email protected] * Laboratoire ESNM, bât. 14, Université de Rennes I, Avenue du Maréchal Leclerc, 35000 Rennes, France fax: (33) 2 99 28 16 17 - E-mail: [email protected] Abstract: This study investigated the bioaccumulation of trace elements in species living within deep-sea hydrothermal vents. Trace elements were quantified in whole organs known to be involved in exchanges with the surrounding medium or in detoxification processes. The binding of heavy metals to specific metalloproteins was studied as well as their balance within subcellular fractions. Sequestration of trace elements under insoluble forms appears to be the major adaptive pathway for polychaetes. Crustaceans show a high capacity for metallothionein induction, as demonstrated by quantitative analyses. Résumé : Interactions entre éléments métalliques et organismes au niveau des sources hydrothermales océaniques. Le but de notre travail était de mettre en évidence la bioaccumulation des éléments traces chez différentes espèces inféodées aux sources hydrothermales profondes. Ces éléments traces ont été quantifiés dans des organes impliqués dans les échanges avec le milieu environnant ou dans les mécanismes de détoxication. La répartition des métaux entre les fractions subcellu- laires et leur association avec des métalloprotéines spécifiques ont été étudiées. Le stockage des éléments traces sous des formes insolubles semble prédominer chez les polychètes. Les crustacés sont connus pour leur forte capacité à synthétiser des métallothionéines. Cette caractéristique est retrouvée dans cette étude via la quantification de ces protéines chez les crus- tacés hydrothermaux. Keywords : Trace elements, Hydrothermal vents, Alvinellids, Bythograea, Metallothioneins. Introduction intracytoplasmic level of heavy metals (Viarengo and Nott, 1993). Both detoxification mechanisms have been found in Our knowledge of biological communities within deep- hydrothermal vent organisms with high tissue levels of sea hydrothermal vents has progressed considerably since heavy metals (Gaill et al., 1984; Chassard-Bouchaud et al., their discovery (Corliss et al., 1979). In particular, high 1988; Cosson-Mannevy et al., 1986, 1988). Metallo- concentrations of metals within these organisms have been thioneins are low-molecular-weight (6,000 Da) sulphur-rich found to bioaccumulate from vent fluids enriched through proteins clearly implicated in heavy metal detoxification leaching out of magmatic rocks (Edmond and Von Damm, (Cosson et al., 1991; Roesijadi, 1992, 1993), whose highest 1983, 1985). In this context, heavy metal detoxification is concentrations have generally been observed within tissues generally achieved by two major mechanisms: metallic ions or organs characterized by the presence of symbionts. In a are either trapped in insoluble granules or bound to specific recent work, Jeanthon (1991) described several free metalloproteins whose synthesis is triggered by the bacterial strains collected in the vicinity of hydrothermal vents, which are able to accumulate and tolerate heavy Reçu le 8 juillet 1996 ; accepté après révision le 10 juin 1997. metals. However, the implication of bacteria in heavy metal Received 8 July 1996 ; accepted in revised form 10 June 1997. detoxification has not been clearly established. 44 BIOCHEMICAL AND MORPHOLOGICAL DIFFERENCES IN EULALIA Figure 14: Specimens belonging to the proposed species name Eulalia clavigera (Audouin & Milne-Edwards, 1834). A-D Neotype from Saint-Efflam; E, F other specimens from same sample. A: Anterior end, dorsal view. B: parapodium of segment 22, posterior view. C: parapodium of segment 59, posterior view. D: parapodium of segment 108, posterior view. E: anterior end with everted proboscis, ventrolateral view. F: posterior end with anal cirri, dorsal view (right anal cirrus missing). Scale = 1 mm (A, F), 0.5 mm (B-D), or 4 mm (E). Figure 14 : Spécimens attribués à l'espèce proposée Eulalia clavigera (Audouin & Milne-Edwards, 1834). A-D Neotype de Saint- Efflam ; E, F autres spécimens du même échantillon. A : extrémité antérieure, vue dorsale. B : parapode du segment 22 vue postérieure. C : parapode du segment 59, vue postérieure. D : parapode du segment 108, vue postérieure. E : extrémité antérieure avec la trompe sor- tie, vue ventro-latérale. F: extrémité postérieure avec un cirre pygidial, vue dorsale, (le cirre droit manquant). Echelle = 1 mm (A, F), 0.5 mm (B-D) ou 4 mm (E). R. P. COSSON, J.-P. VIVIER 45 Table 1. Elemental composition of various Polychaetous annelids determined by atomic absorption spectrophotometry. Individuals (rinsed or not) or anatomic parts were pooled. The number of aliquots analysed from the same pool is given (n). The standard deviation (± S.D.) refers to the mean level of analysed aliquots. Elemental levels are expressed as µg.g-1 dry weight. Tableau 1. Composition en éléments de différents annélides polychètes déterminée par spectrophotométrie d'absorption atomique. Les individus entiers (rincés ou non) ou les différentes parties anatomiques ont été groupés. Le nombre d'aliquots analysés à partir des échantillons groupés est indiqué (n). L'écart-type (± S.D.) se rapporte à la moyenne des teneurs des aliquots analysés. Les teneurs en éléments sont exprimées en µg de métal par g de poids sec. Paralvinella Element Alvinella pompejana Alvinella caudata HESIONIDAE POLYNOIDAE grasslei tissue anterior digestive anterior digestive rinsed whole rinsed not rinsed rinsed parts tract parts tract whole bodies whole whole whole (rinsed) plus gut (rinsed) plus gut bodies plus bodies bodies bodies contents contents mucus (n) (2) (3) (2) (1) (2) (3) (3) (3) (3) Cu 189 ±4 577 ± 38 140 ±7 93 108 ±8 73 ±8 116 + 17 1137 ±241 26 ±4 Zn 1103 ±680 16501 ±474 7860 ± 329 7445 13780 ± 765 1552 ±91 5997 ± 347 38602 ±1454 5317 ±131 Cd 22 ±1 18 ± 1 13.7 ± 1.0 8.2 10.3 ± 1 8.6 ±0.5 11.2+ 1.0 38 + 2 6.4 ±0.1 Hg 131 ±11 4.2 ±1.0 89 ±4 7.4 3.6 ±1 73 ±6 4.6 ±1.0 7.4 ± 0.2 4.9 ±0.2 As 3389 ± 103 92 ±2 2288 ± 18 67 81 ±2 1052 ±15 20 + 2 89 ±2 38 ±3 obvious. Hesionids, which are polychaetes not bearing Secondly, as the samples were rinsed, metal-rich particles symbiotic bacteria, are often found on smoker walls, may have been partially washed out from the surface of the whereas polynoids and alvinellids (especially P. grasslei) anterior part but persisted within the digestive tract since the are more abundant within Riftia pachyptila bunches. With worms could not be starved prior to metal analyses. respect to Alvinellids, the zinc level in P. grasslei was lower Compartmentation of metals: Intracellular balance than in other polychaetes, whereas mercury and arsenic (Table 2). levels were high. Juniper et al. (1986) have suggested that Insoluble forms were predominant for copper, zinc and the mucus surrounding the body of P. grasslei plays a role cadmium in all studied body parts. For P. grasslei, ratios of in heavy metal detoxification processes. As we did not cytosolic zinc were higher than those of cytosolic copper, separate mucus from the body, our results may reflect the whereas this was true only for the ventral body wall of occurrence of trapped metallic particles within the mucus. A. pompejana. When cadmium was detected, it was Pompei worms (Alvinella pompejana and A. caudata) associated essentially with insoluble compounds. harbouring epibiotic bacteria were sampled on the smokers. Analysis of the rinsed whole body of A. caudata indicated Association with proteins within the cytosol (Table 3). that metal concentrations were similar to those observed in Tissues of A. pompejana displayed differences the hesionid rinsed pool, except for arsenic and zinc which concerning the balance of soluble copper between heat- had higher levels. These polychaetes, which live very close stable and heat-denaturable compounds. The anterior part to vents, are exposed to a continuous flow of particles from and the ventral body wall exhibited a preferential the precipitation of metallic sulphides in hydrothermal association of cytosolic copper with thermolabile fluids. Essential metals (Cu, Zn) were equally (A. caudata) compounds. Conversely, cytosolic copper was mainly or more abundant (A. pompejana) in the digestive tract (gut associated with heat-stable compounds within the digestive wall and content) than in the anterior part (gills, feeding tract and dorsal body wall of A. pompejana and within all tentacles and first segments), which was directly exposed to studied parts of P. grasslei. Cytosolic zinc and cadmium mineral particles and thus contained more toxic metals (As, (when detected, data not shown) were associated essentially Hg). This condition noted in a previous study (Cosson- with heat-stable compounds for both species. Mannevy et al., 1989) could be explained by two non- Abundance of metallothioneins (Table 4). exclusive hypotheses. First, as pompeii worms are known to The dorsal body wall of A. pompejana, which bears "utilize their retractable grooved buccal tentacles to seize epibiotic bacteria, was classified as the richest MT- food particles and to move them to the mouth" (Desbruyères containing tissue in an earlier study (Cosson-Mannevy et et al., 1985), they may be able to identify and sort the al., 1986). Our findings here show that the ventral body wall particles, thereby discarding toxic metal-rich particles. had an MT level 3 to 6 times as high as that of the other 46 METALS WITHIN VENT ORGANISMS Table 2. Ratios of metal associated with the insoluble compounds within homogenates of alvinellid tissues. Results are expressed as percentages of the total amount of metal in the tissue. n. d.: not determined. Tableau 2. Proportions de métal associé aux composés insolubles dans des homogénats de tissus d'avinellidés. Les résultats sont expri- més en pourcentages de la quantité totale de métal présente dans le tissu analysé.
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