marine microbial thiotrophic ectosymbioses - HYDRA-Institute

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2727_C04.fm Page 96 Wednesday, June 30, 2004 12:00 PM 96 J. Ott, M. Bright & S. Bulgheresi In many cases, however, they appear ectosymbiotically, attached to the body surface of their eukaryote host, such as in flagellates, ciliates, Nematoda (Stilbonematinae), and in certain Annelida (Alvinellidae) and Arthropoda (Ott 1996, Polz & Cavanaugh 1996). This review summarises our knowledge about these ectosymbioses. Ectosymbioses differ from endosymbioses in many respects: the microbes are largely exposed to ambient conditions, although the eukaryote host is responsible for the position within gradients of environmental variables. Moreover, substances produced by the host may modify the environment and physiology of the bacterial partner. The animal hosts appear less modified than is the case in endosymbioses, and in most cases, the relationship to nonsymbiotic relatives can be traced with confidence. Rarely is a particular ectosymbiosis characteristic for taxa higher than genera. Although morphological modifications in conjunction with the symbiotic way of life are present in practically all ectosymbioses, they never reach the extent found in endosymbioses. In some cases the partners may be separated and kept alive at least for some time. These characteristics allow us to make inferences on how these symbioses originated, something that is extremely difficult to do in highly evolved endosymbioses. In many thiotrophic symbioses where the method of transmission has been clarified, there is no evidence of vertical transmission from parents to offspring. Apparently, the symbionts must be acquired in each generation, most probably from the free-living bacterial community in the respective habitat. The mechanisms of recognition, attachment, and internalisation of the microbial partner are still unclear. Thiobiotic habitats Hydrothermal Vents Hydrothermal springs are found in all oceans along the central rift valley of mid-oceanic ridges. Here, sea water percolates through the newly formed crust several kilometres deep. When it comes in contact and reacts with hot rocks near the underlying magma chamber it undergoes profound chemical changes (Alt 1995, Von Damm 1995). Most importantly sulphate is reduced to sulphide, the water becomes anoxic and the concentrations of heavy metals increase dramatically. The heated and chemically altered fluid then rises and flows warm (a few degrees above ambient deepwater temperatures) to extremely hot (350–400˚C) from cracks in the basaltic rocks covering the floor of the rift valley or seeps through sediments. Mineral precipitates may form chimneys dozens of metres high, from which the hydrothermal fluid emanates as black clouds coloured by precipitating metal sulphides (Goldfarb et al. 1983). Chemolithoautotrophic bacteria and Archaea already grow in the chemical gradients within the conduits in the basaltic rocks (Karl et al. 1980). Where the hydrothermal fluid is injected into the oxygen-containing, cold, deep-sea water a profusion of microbial production occurs on the surface of rocks and sediments. Most spectacular, however, is the animal life around the hydrothermal vents, which solely depends on the production of the chemolithoautotrophic microbes (Van Dover 2000). Whereas many animals are suspension feeders or simply graze the microbial turf, others live in symbiosis with special kinds of bacteria. Hydrothermal vents are unpredictable environments, where fluid flows may vary on short temporal scales (Johnson et al. 1988). Successful survival strategies here include associations either with mobile animals that may follow gradients or with large sessile organisms that provide the necessary milieu for the bacteria. Both endo- and ectosymbioses are found in these bizarre environments. The most prominent examples are the vestimentiferan tube worms, bivalves such as Calyptogena spp. and Bathymodiolus spp., and the shrimp Rimicaris spp. Hydrothermal vents are not restricted to the deep sea but also occur in shallow water in conjunction with volcanism. None of the few shallow hydrothermal vents studied so far, however, showed such a highly specialised fauna (Dando et al. 1995).
2727_C04.fm Page 97 Wednesday, June 30, 2004 12:00 PM Marine Microbial Thiotrophic Ectosymbioses 97 Cold seeps Wherever the sea sediments are subjected to pressure, pore fluid is squeezed from the interstices and seeps from the surface. This seepage may occur under a variety of tectonic forces: in accretion prisms formed during subduction of one lithospheric plate under another, at the margin of mud volcanoes, in places where salt diapirs rise through continental margin sediments, or in connection with hydrocarbon seeps. The expelled fluids differ chemically from the surrounding sea water. They are anoxic and may contain methane or sulphide, hydrocarbons, or high salt concentrations, but not the high heavy metal concentrations typical for hydrothermal vents (Suess et al. 1987). Flow speeds are generally low but steady and sulphide concentrations are often at the detection limit near the sediment surface. In contrast to the vents, the sulphide here is of biological origin, essentially having been produced by microbial sulphate reduction (Carney 1994). Symbiotic biota associated with cold seeps include vestimentiferan and frenulate tube worms, clams and mussels among the macrofauna, and stilbonematid nematodes among the meiofauna. Some of the mussels contain both thiotrophic and methanotrophic endosymbionts, sometimes within the same bacteriocyte (Fisher 1990). Methanotrophs are also found in the frenulate Siboglinum poseidoni (Schmaljohann & Flügel 1987). Shallow sheltered sediments This is by far the largest thiotrophic habitat. It extends from intertidal sand and mudflats, marsh and mangrove sediments, over essentially all of the shelf sediments, to dysoxic basins and upperslope sediments. It occurs under an oxic surface layer of variable thickness, ranging from a few millimetres to several centimetres, from which it is separated by a chemocline – the redox potential discontinuity layer (RPD) (Fenchel & Riedl 1970). Within the RPD, electron acceptors for the oxidation of organic material change in sequence from oxygen to nitrate, ferric iron, manganese and sulphate. Bacterial sulphate reduction produces sulphide in the deeper layers. Upward diffusion of sulphide leads to its oxidation and a variety of microbes use the free energy of this oxidation process for carbon fixation (Jørgensen 1989). Since sediment layers containing sulphide may be separated from those containing the best electron acceptor (oxygen) by several millimetres to centimetres, microorganisms are at a disadvantage when the sulphide/oxygen gradient is weak. Some of the larger sulphur bacteria such as Beggiatoa and especially the giant spaghetti bacterium Thioploca are mobile enough to bridge the gap (Gallardo 1977). Similar to what has been observed for hot vents and cold seeps, bacteria have succeeded in finding hosts that provide them with both oxygen and sulphide. Among the macrofauna, several families of bivalves, such as the Lucinidae, Thyasiridae, and Solemyidae, have species containing sulphur-oxidising chemoautotrophic bacteria in their gills (Allen 1958, Southward 1986). In those sediments with interstitial spaces, a variety of protists and meiofauna animals have symbiotic bacteria, either as endosymbionts (catenulid flatworms, phallodrilid oligochaetes, nematodes of the genus Astomonema) (Giere 1996) or as ectosymbionts (ciliates, stilbonematid nematodes) (Ott 1996). Recently, a number of flagellates living in the soft sediment of a dysoxic basin have been described to harbour potentially chemoautotrophic ectosymbionts (Buck et al. 2000, Bernhard et al. 2000). Macrophyte debris In shallow waters the debris originating from marsh and mangrove plants, algae, or sea grass may accumulate (Fenchel 1970, Mann 1976). The decomposition of this organic matter creates sulphidic habitats of various spatial and temporal extents. Mangrove peat is a relatively stable substratum having internal sulphide concentrations of up to 4 mM (McKee 1993). Diffusion of sulphide into the overlying water creates a few-millimetre-thick sulphidic boundary layer, whereby sulphide flux is highest in recently disturbed patches on the peat surface (Ott et al. 1998). Loose macrophyte
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