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'Regulation' of Gutless Annelid Ecology by Endosymbiotic Bacteria

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'Regulation' of Gutless Annelid Ecology by Endosymbiotic Bacteria MARINE ECOLOGY PROGRESS SERIES Published January 3 Mar. Ecol. Prog. Ser. 'Regulation' of gutless annelid ecology by endosymbiotic bacteria ' Zoological Institute, University of Hamburg, Martin-Luther-King-Platz 3, D-2000 Hamburg 13, Germany Woods Hole Oceanographic Institution. Coastal Research Lab, Woods Hole, Massachusetts 02543, USA ABSTRACT: In studies on invertebrates from sulphidic environments which exploit reduced substances through symbiosis with bacteria, experimental ecological results are often underrepresented. For such studies the gutless oligochaete Inanidrilus leukodermatus is suitable due to its mobility and local abundance. It contains endosymbiotic sulphur-oxidizing bacteria and inhabits the sediment layers around the redox potential discontinuity (RPD) with access to both microoxic and sulphidic conditions. By experimental manipulation of physico-chemical gradients we have shown that the distribution pattern of these worms directly results from active migrations towards the variable position of the RPD, demonstrating the ecological relevance of the concomitant chemical conditions for these worms. Their distributional behaviour probably helps to optimize metabolic conditions for the endosymbiotic bacteria, coupling the needs of symbiont physiology with host behavioural ecology. The substantial bacterial role in the ecophysiology of the symbiosis was confirmed by biochemical analyses (stable isotope ratios for C and N; assays of lipid and amino acid composition) which showed that a dominant portion of the biochemical fluxes in the symbiosis is bacteria-based. It appears that the distributional and nutritional ecology of the gutless annelids is strongly influenced by their symbiosis with sulphur bacteria. INTRODUCTION (2)Experimental ecology. Inanidrilus leukoderma tus is one of the few members of the sulphide fauna that is Many symbioses between invertebrates and suitable for experimental ecological work due to its chemoautotrophic bacteria have been documented at sufficient size, high mobility, locally rich populations the structural, and to some extent physiological and and its well-documented scientific background (Giere microbiological, levels (for reviews see Cavanaugh & Langheld 1987, Giere 1989). Its symbiotic endobac- 1985, Southward 1987).However, the ecological effects teria are chemoautotrophs which preferentially oxidize resulting from this close partnership between bacteria thiosulphate in order to obtain their metabolic energy. and animal host are generally less recognized. The storage of rich bacterial reserve substances Thiobiotic animals, both meio- and macrobenthic, (polythionates and polyhydroxy butyric acid) makes tend to live around the redox chemocline (Powell & the worms usually appear shiny white (Giere et al. Bright 1981, Powell et al. 1983, Scherer 1985, South- 1988b). Only rarely, i.e. in the oxygenated surface ward 1987, Meyers et al. 1987, 1988, Ott & Novak horizons, are worms greyish-transparent. Hence, the 1989). In this preferred layer they have access to mild position of the worms within the steep chemical gra- concentrations of both reduced sulphur and oxygen. dients of the vertical sand column should have a Initial analyses of populations of the gutless tubificid marked influence on either the production or consump- Inanidrilus (Phallodrilus)leukodermatus by Giere et al. tion of these storage substances which is evidenced by (1982) suggested that this pattern is also found in their appearance as 'white' or 'pale' worms (Giere et al. bacteria-symbiotic annelids from sulphidic sediments. 198813). By manipulation of the oxygen and reduced In this paper we describe the results of 3 different, but sulphur conditions in the sediment it was tested how complementary, approaches to studying the ecological the symbiotic worms adjust to redox and sulphide gra- coupling between endosymbionts and host: dients. A varying supply of reduced sulphur should (1) Field ecology. The distributional ecology of the influence both the appearance of the worms and their worms was determined by further investigation of their distributional pattern. vertical field distribution. (3) Biochemical analysis of the nutritional interac- O Inter-Research/Printed in Germany 288 Mar. Ecol. Prog. Ser. tions between bacterial sym bion ts and annelid host. Manipulation of the redox potential discontinuity The role of the bacterial symbionts as a nutritional (RPD) depth. Migration experiments were designed to source for their gutless hosts is difficult to assess investigate the vertical distribution of worms, allowing because of the intricate structural and physiological the setting of the RPD layer in a given horizon of a sand interactions between the symbiotic partners (Giere & column. Perspex tubes (diam. 2.6 cm, length 15 cm) Langheld 1987). Analysis of biochemical composition were filled with reduced, gray sand or oxygenated, and measurement of stable isotope ratios (C and N) can white sand, and a sharp redox-cline was set up at a give indications on the relevance of bacterial given horizon. The bottom and top of each core was chemoautotrophy for the diet of the worms (Conway & covered with nylon gauze (10 to 20 pm mesh size).After McDowell Capuzzo 1990a). insertion of 20 active, undamaged worms into a chosen 3 cm layer, the cores were placed in a small glass tank which contained a reduced sediment layer at the bot- MATERIALS AND METHODS tom and an oxygenated surface. The top of the tube rose above the sediment and aerated seawater was Most field and experimental studies were done in allowed to flow around it. summer 1989 in the laboratories of the Bermuda As a generalized indication for oxygenated or Aquarium, Museum and Zoo, close to the sample sta- reduced conditions (Giere et al. 1988a) in the experi- tion in Flatts Inlet, the narrow passage from the sea to mental cores, redox values were recorded in every 3 cm Harrington Sound, Bermuda. We obtained fresh layer when fractionating the sediment core at the end worms, original sand and seawater directly from the of each experimental run (mostly after 72 h). By subse- sampling site. All samples were taken by SCUBA quent careful decantation of the 5 resulting subsamples divers from depths between 2 and 4 m. Data from (about 16 cm3 each) the new position of the worms was vertical cores taken with essentially identical methods evaluated (retrieval rate mostly 90 to 100%) and at the same location during former stays in Bermuda recorded with respect to the monitored redox value. A are included in the results and discussion. few cores from first experiments in 1986 were included Vertical cores from the sublittoral sediment in Flatts in the evaluation. Regrettably, within the time avail- Inlet (Bermuda) were taken by SCUBA divers to study able, not all experiments could be based on sufficient the microdistribution of the worms in relation to the numbers of replicates for reliable statistical evaluation pore water conditions (perspex corer of 5 cm internal (see 'Results'). diameter and 30 cm length). Cores were subdivided Experimental palelwhite conversion of worms as a immediately after retrieval, and split into 2.5 or 3 cm result of variations in nutrient supply of the symbiotic fractions, the redox values were recorded and the bacteria was performed in small experimental boxes worms quantitatively decanted and counted upon (about 2 cm3) filled with original sediment and water. return to the laboratory. After insertion of 5 worms, each box was capped with Sulphide content in the pore water was measured in nylon gauze of 10 to 20 pm mesh size and implanted 10 vertical series (3 in 1981, 6 in 1986 and 1 in 1989). into the sulphidic or oxic sand layers of the same glass For determination of dissolved sulphide in the natural tanks used for the migration experiments. Average sediment (pH 7.9 to 8.5),undisturbed pore water sam- duration of each experiment was 72 h before the worms ples were collected by divers using small hypodermic were retrieved and their color inspected. Similar exper- syringes (Giere et al. 1982, Howes & Wakeham 1985). iments performed during former stays on Bermuda In 1989, spectrophotometric analysis (modified after were incorporated into the evaluation. Cline 1969) could not be done in Bermuda, conse- Measurement of stable isotope ratios (C and N). Air- quently the sulphide, precipitated by alkaline zinc ace- dried worms, sampled in October 1989 in Bermuda, tate, was filtered through Millipore filters (pore width were analyzed in Woods Hole (for detailed methods see 0.2 pm). These filters were kept in Millipore special Conway et al. 1989). Due to the limited amount of filter jars in the refrigerator until return to the labora- material, each determination was based on one pooled tory where the precipitate was dissolved for further worm population (about 100 specimens); thus, the val- photometric analysis by addition of 5.5 N HC1. Using ues obtained are preliminary. this method the amount of sulphide in the samples may Lipids were analysed chromatographically after con- have been slightly underestimated due to immediate version to fatty acid methyl esters following the oxidation during handling of the syringe, precipitation methodology of Conway & McDowell Capuzzo (1990b). loss and bacterial degradation. The resulting data, The values given here are averages of 3 extractions of therefore, represent conservative values. pooled worms. Porewater for analysis of the amino acids was sam- Amino acid composition of the worms was measured pled by a
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