marine microbial thiotrophic ectosymbioses - HYDRA-Institute

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2727_C04.fm Page 106 Wednesday, June 30, 2004 12:00 PM 106 J. Ott, M. Bright & S. Bulgheresi An 8-mm-long Stilbonema majum with a diameter of 60 mm covered by a mucus sheath of 7.5 mm thickness and containing 10 layers of 1.3 ¥ 0.6 mm cocci carries about 21 ¥ 10 6 bacteria. This makes up 22% of the volume of the symbiotic consortium. In Laxus oneistus the density of the upright rods is approximately 3.5 cells mm –2 . A 9-mm-long male with a diameter of 50 mm and an 8-mm-long bacterial coat is covered by 4.5 ¥ 10 6 rods (size 2.1 ¥ 0.6 mm each). This represents 12.3% of the consortium volume. In the genus Eubostrichus, two types of arrangement of the bacteria are found: in E. parasitiferus and several similar undescribed species the bacteria are crescent-shaped nonseptate filaments, 0.6 ¥ 30 mm in size, that are attached to the cuticle with both ends oriented parallel to the worm’s longitudinal axis. About 80 bacteria are arranged in a spiral fashion around the circumference of each worm, giving it the appearance of a rope. In cross section the bacteria appear to form several layers, when, in fact, all bacteria are in contact with the worm surface. A 3-mm-long E. parasitiferus with a diameter of 20 mm carries about 8000 bacteria, which make up only 7% of the volume of the symbiotic consortium, despite their spectacular appearance. In E. dianae the bacteria form up to 120-mm-long and 0.4-mm-thick filaments, which are attached to the cuticle by one end (Figure 6) and form a dense fur-like coat that in live worms appears nicely groomed. With a size similar to that of E. parasitiferus, E. dianae carries 40–60 ¥ 10 3 filaments, contributing substantially (36–44%) to the consortium volume. The dense microbial coat is colonised by additional bacterial epibionts (Polz et al. 1999a). Rimicaris Three morphological types of bacteria have been described from Rimicaris by various authors (Van Dover et al. 1988, Casanova et al. 1993, Gebruk et al. 1993, Polz & Cavanaugh 1995): rods with a diameter from 0.2–0.4 mm and 0.5–3 mm in length and two kinds of filaments, a rare form with a diameter of 0.2–0.5 mm and a common larger form with a diameter of 0.8–3 mm (Figure 14). Several septate filaments grow from a common basal attachment disc and, in the large form, may attain a length of 1.5 mm. The filaments consist of cylindrical cells of approximately the same length as their diameter. These bacteria densely cover the inner surface of the extended carapace and also cover the bacteriophores on the enlarged exopodites of the second maxilla and first maxilliped and on the bases of the thoracic appendages. The rods co-occur with the filaments and are especially abundant in juveniles. They are attached along their whole length to the cuticle of the shrimp. Using a 16S rRNA-specific fluorescent hybridisation probe, Polz & Cavanaugh (1995) demonstrated that all three morphotypes belong to the same phylotype of e-proteobacteria. A number of parasites, but also sulphur bacteria such as Thiovolum sp., are found among the eproteobacteria. Recently, bacteria related to Rimicaris symbionts have been detected with molecular methods in marine anoxic water and sediments (Madrid et al. 2001, Lee et al. 2001). Elemental sulphur within the cells and RuBisCo activity (Gebruk et al. 1993) strongly suggest a thiotrophic nature of the bacteria. Polz & Cavanaugh (1995) estimate that an average shrimp may carry 8.5 ¥ 10 6 bacteria. Mutual benefits The consensus is that the above symbioses are largely nutritional. On one hand, the bacteria provide organic matter from their own primary chemoautotrophic production. On the other hand, the eukaryote partner facilitates access to reduced sulphur compounds and electron acceptors, which may be separated in space and time. Since sulphide is toxic for aerobic metazoans, the idea has been proposed that the bacteria may act as a detoxification mechanism, oxidising sulphide into elemental sulphur and finally to sulphate (Somero et al. 1989). Powell (1989) argued that in
2727_C04.fm Page 107 Wednesday, June 30, 2004 12:00 PM Marine Microbial Thiotrophic Ectosymbioses 107 meiofauna, due to the small size of the animals, sulphur detoxification could not work and they should be sulphide insensitive. In fact, high concentrations of thioles can be found in the tissues of Stilbonematinae (Hentschel et al. 1999). A certain detoxification may nevertheless be provided, because the bacterial symbionts increase heat tolerance in Stilbonematinae in the presence of simultaneous sulphide stress (Ott 1995). Sulphide detoxification probably occurs in sulphideoxidising bodies in the gills of Rimicaris (Compere et al. 2002) without any involvement of the ectosymbionts. Nutrition The limited success in culturing thiotrophic symbioses has precluded direct evidence that the animals feed on the symbiotic bacteria and may grow with them as their sole food. The presence of bacteria in feeding and digestive vacuoles has been reported for Kentrophoros (Raikov 1971, 1974, Fenchel & Finlay 1989) and Zoothamnium niveum (Bauer-Nebelsick et al. 1996b) and in the gut lumen in several species of Stilbonematinae (Wieser 1959, Ott & Novak 1989, Riemann et al. 2003). In all cases the bacteria have the distinct morphology and fine structure of the respective ectosymbionts and dominate the content of the digestive tract. Transfer of labelled carbon from symbionts to host has been shown for Z. niveum by Rinke (2002) in pulse and chase experiments. Most evidence for a nutritional interaction comes from studies of natural tracers in food chains, such as fatty acids and stable isotopes. High proportions of n-4 fatty acids, which are indicative for a bacterial origin, have been found in tissues of Rimicaris, whereas in the closely related genera Alvinocaris and Mirocaris, n-3 fatty acids characteristic for photosynthetically derived carbon are more abundant (Pond et al. 1997b,c). Muscles of Rimicaris contain n-7 fatty acids, which are closer in d 13 C (–13‰) to the ectosymbionts (–12‰) than to bacteria scraped from hydrothermal chimneys (–21‰) (Rieley et al. 1999). As a relic of its early planktotrophic life, however, Rimicaris contains high levels of polyunsaturated fatty acids in storage compounds (wax esters) in reproductive tissues. These fatty acids are thought to be important for reproduction in Crustacea (Pond et al. 2000, Allen et al. 2001). Gebruk et al. (1993) report d 13 C values for various tissues ranging from –10.5 to –12.5‰, which is similar to values reported for other hydrothermal vent animals. Stilbonematinae have d 13 C of –25.9‰ without and –24.9 to –27.5‰ with their symbionts, whereas nonsymbiotic nematodes and detritus from the same habitat show values of –10.3 and –10.5‰, respectively (Ott et al. 1991). In some cases the biomass of the bacterial symbionts dominates the food availability in the environment (Gebruk et al. 1993, Van Dover 2002). Polz & Cavanaugh (1995) estimated that at a density of 25,000 shrimp m –2 the number of symbiotic bacteria attached to Rimicaris would be 2.1 ¥ 10 11 , which is almost three orders of magnitude higher than the 4.9 ¥ 10 8 bacteria attached to a square meter of sulphide chimney surface. Dependence on a special resource is implied by morphological changes in feeding structures, such as the near disappearance of a functional mouth in Kentrophoros (Foissner 1995) or the reduction in dentition and the weakening and rearrangement of pharynx musculature in the Stilbonematinae (Hoschitz et al. 2001). Fenchel & Finlay (1989) calculated that the bacterial production in Kentrophoros allows a doubling time of the ciliate of 18 h, which is low for a ciliate of this size, but would allow the protozoan to grow with the symbionts as a unique food source. No such data are available for the other symbioses. Zoothamnium niveum, however, can maintain the high growth speed to reach the large size only in the presence of the bacteria. The growth rate and maximum size reached by aposymbiotic colonies reared from macrozooids that had lost their bacteria is only about 10% of those of symbiotic colonies. Stilbonematinae have an extremely low metabolism (Schiemer et al. 1990) and could probably be easily sustained on the production of their bacteria. Note also that the bacteria appear to divide more rapidly on the margin of presumed feeding patches on the nematode cuticle (Polz et al. 1992).
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