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Mineralogical Gradients Associated with Alvinellids at Deep-Sea Hydrothermal Vents

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Mineralogical Gradients Associated with Alvinellids at Deep-Sea Hydrothermal Vents Deep-Sea Research I 50 (2003) 269–280 Mineralogical gradients associated with alvinellids at deep-sea hydrothermal vents Magali Zbindena, Nadine Le Brisb, Philippe Compere" c, Isabelle Martinezd, Francois, Guyote, Francoise, Gailla,* a Laboratoire de Biologie Marine, UMR CNRS 7622, Quai Saint Bernard, 75252 Paris cedex 05, France b Departement! Environnement Profond, IFREMER, BP 70, 29280 Plouzane,! France c Institut de Zoologie, UniversitedeLi! ege," 22 Quai Van Beneden, B-4020 Liege," Belgium d Laboratoire de Geochimie! des Isotopes Stables, IPGP, 4 place Jussieu, 75252 Paris cedex 05, France e Laboratoire de Mineralogie,! LMCP and IPGP, 4 place Jussieu, 75252 Paris cedex 05, France Received 16 November 2001; received in revised form 30 April 2002; accepted 8 November 2002 Abstract Alvinella pompejana and Alvinella caudata live in organic tubes on active sulphide chimney walls at deep-sea hydrothermal vents. These polychaete annelids are exposed to extreme thermal and chemical gradients and to intense mineral precipitation. This work points out that mineral particles associated with Pompeii worm (A. pompejana and A. caudata) tubes constitute useful markers for evaluating the chemical characteristics of their micro-environment. The minerals associated with these worm tubes were analysed on samples recovered from an experimental alvinellid colony, at different locations in the vent fluid–seawater interface. Inhabited tubes from the most upper and lower parts of the colony were analysed by light and electron microscopies, X-ray microanalysis and X-ray diffraction. A change was observed from a Fe–Zn–S mineral assemblage to a Zn–S assemblage at the millimeter scale from the outer to the inner face of a tube. A similar gradient in proportions of minerals was observed at a decimeter scale from the lower to the upper part of the colony. The marcasite/pyrite ratio of iron disulphides also displays a steep decrease along the few millimeters adjacent to the external tube surface. The occurrence of these gradients indicates that the micro- environment within the tube differs from that outside the tube, and suggests that the tube wall acts as an efficient barrier to the external environment. r 2003 Elsevier Science Ltd. All rights reserved. Keywords: Biogeochemistry; Annelids; Tubes; Biomineralisation; Zinc–iron sulphides 1. Introduction polychaete annelids dwelling in organic tubes on smoker walls of deep-sea vents of the East Pacific Alvinella spp. (i.e. A. pompejana and A. cauda- Rise (review in Desbruyeres" et al., 1998). Because ta), the so-called Pompeii worms, are thermophilic of their location on active parts of chimney walls, these organisms are exposed to steep thermo- *Corresponding author. Tel.: +33-1-44-27-30-63; fax: +33- chemical gradients and intense mineral precipita- 1-44-27-52-50. tion. Still, the precise knowledge of the conditions E-mail address: [email protected] (F. Gaill). sustained by Alvinella constitutes one of the most 0967-0637/03/$ - see front matter r 2003 Elsevier Science Ltd. All rights reserved. doi:10.1016/S0967-0637(02)00161-9 270 M. Zbinden et al. / Deep-Sea Research I 50 (2003) 269–280 puzzling questions of deep-sea vent biology scopies, X-ray microanalysis and X-ray diffraction (Chevaldonne! et al., 2000; Pradillon et al., 2001; (XRD). Shillito et al., 2001). Since Alvinella spp. was shown to spend most of the time within its tube (Chevaldonne! and Jollivet, 1993), the conditions 2. Materials and methods prevailing in this micro-environment are of parti- cular interest and, especially, potential differences 2.1. Sample collection between the characteristics of the micro-surround- ing in the inner space delimited by tubes and the An alvinellid colony was collected with the outside conditions have to be examined. This can ‘‘Nautile’’ submersible during the ‘‘HOT 96’’ be approached by chemical characterisation of cruise (91N East Pacific Rise, 2600 m depth). This fluid phases in contact with the inner and outer colony was recovered from a TRAC (Titanium faces of the tube, hereafter called inner and outer Ring for Alvinellid Colonisation, Gaill et al., 1996; medium fluids, respectively. Taylor et al., 1999). The TRAC was deployed for Direct characterisation of the thermal and over 70 days at the top of the M vent smoker, chemical centimeter-scale gradients in the alvinel- initially colonised by alvinellids. This device lid surrounding is expected to provide further clues (Fig. 1) enables collection of the colony that has to address this question. Temperature measure- developed in and around it, preserving its spatial ments and analyses of the chemical conditions structure. Just before recovery, discrete tempera- were performed inside Alvinella spp. tubes with ture measurements were achieved at several points specific sampling and sensing devices (Cary et al., at the bottom and at the top of the device, with a 1998; Di Meo et al., 1999; Luther III et al., 2001). probe held by the ‘‘Nautile’’ arm. The experi- Up to now, this approach did not reveal differ- mental alvinellid colony was dissected on board in ences between the inner and outer medium fluids. order to collect tube portions from two horizontal The study of minerals associated with inhabited sections of equal height (4 cm) corresponding to Alvinella spp. tubes is an interesting alternative to the uppermost (level 1) and lower (level 2) parts of the direct approach of in situ measurement of the colony (Fig. 1). Level 1 was directly in contact thermal and chemical parameters. Previous studies with the surrounding seawater-vent fluid mixing have provided information about the tube char- zone while level 2 was located at the base of the acteristics (see review in Gaill and Hunt, 1991), but TRAC, which had been directly deployed on the the nature and mineralogy of the associated mineralised surface of the smoker. Collected tubes, mineral particles have not been systematically from which the animals were removed, were fixed investigated. Recently, Zbinden et al. (2001) have in saline formalin and kept in a 701-ethanol shown that mineral particles found within Alvi- solution. Mineral deposits that had grown on the nella spp. tubes exhibit constant composition and TRAC walls and between tubes were also recov- microstructure, suggesting that mineral particles ered from these two sections. may be good indicators of chemical conditions prevailing in the worm’s micro-environment. 2.2. Ash and C/N/S content of the tube The present study is the first to combine compositional and ultrastructural information Some of the tubes from levels 1 and 2 were oven- about mineral deposits within and at the inner dried at 801C for 48 h and weighed with a and outer surfaces of recently secreted Pompeii Sartorius precision balance (10À4 g). They were worm tubes, from different locations at the active further heated for 2 h at 4501C (Ehret oven) and substrate–sea water interface. Samples were col- the ash weighed. Other tubes of each level were lected selectively from experimental alvinellid used for measurements of C/N/S contents. Tubes colonies obtained with a specific device. The were dried in ambient air and ground to powder. mineral particles associated with inhabited tubes For each sample, 3 replicates (about 10 mg dry were analysed by photonic and electron micro- weight) were analysed for total carbon and M. Zbinden et al. / Deep-Sea Research I 50 (2003) 269–280 271 the TRAC from levels 1 and 2 were also dried, ground and analysed. XRD studies were carried out with a Philips PW 1710 diffractometer operated at 40 kV, 30 mA with a Co tube. Spectra were collected between 2Y ¼ 31 and 1001 with 0:04ð2YÞ steps and 20 s per step. A Rietveld refinement program was used for interpreting the multiphase spectra. 2.4. Light and scanning electron microscopies and X-ray microanalysis Tube samples were dehydrated in ethanol and propylene oxide series and then embedded in an epoxy resin (Serlabo). Thick polished sections were obtained with a rotary saw. The sections were progressively thinned to 80 mm by abrasion on sandpaper, then polished on velvet with a 0.3 mm alumina suspension and glued on a glass slide with an epoxy resin (Epotecny, E501). Some of these sections were stained with toluidin blue to show the organic matrix of the tube by light microscopy (with a Nikon Optiphot-pol microscope). The other sections were carbon-coated in a Balzers BAF-400 evaporator prior to energy dispersive X-ray microanalysis (EDX) and observations, achieved in a scanning electron microscope (SEM: JEOL JSM-840A) operating at 20 kV. X-ray microanalysis and elemental mappings were performed in the SEM fitted with a Link Pentafet Fig. 1. (A) Schematic representation of the TRAC (showing the location of the two levels of sampling). Total height of the detector and a Link eXl-10 analyser. TRAC is 15 cm and diameter is 25 cm. (B) Photograph of the TRAC in situ at the top of the smoker. 3. Results nitrogen contents with a Nitrogen Analyser 1500 (Carlo Erba Strumentazione, Milano, Italy). Three 3.1. Macroscopic observations other replicates of the same samples (about 2–3 mg dry weight) were analysed for total (i.e. both In situ observations of the TRAC showed the organic and inorganic) carbon and sulphur con- formation of mineral deposits and the colonisation tents with a carbon–sulphur Determinator CS-125 by alvinellids from the basal part to the top of the (Leco Corporation St-Joseph, MI, USA). The TRAC during the 70 days of deployment. One minimum weight of sample required for one hundred and fifty alvinellids belonging to three analysis was 500 mg. species (Paralvinella grasslei, Alvinella pompejana and Alvinella caudata) were sampled from the 2.3. X-ray diffraction (XRD) device. Since the tubes of the two species of the genus Alvinella cannot be morphologically Tubes of each level were dried in ambient air distinguished from each other, they were consid- and ground to powder.
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