Potential role of bacterial mats in the nitrogen budget of marine sediments:the case of Thioploca spp.

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The main source of organic matter to estuarine and shelf sediments is the deposition of detrital material from plankton in the water column (Suess 1980). The release of nutrients from the sediments is considered to be regulated (feedback mechanism) by the rate at which organic detritus reaches the bottom, the rate at which this detritus is decon~posed (mainly by heterotrophic bacteria), and the rate at which nutrients released to pore waters are transported to overlying waters by diffusion and bioturbation. Furthermore, the regeneration of nutrients from the sediments of shallow, near-shore marine environments could be supplying more than half of the required nitrogen for primary production (Rowe et al. 1975). However, recent observations (Fossing et al. 1995) suggest that prokaryotic metabolic processes associated with benthic microbial mats of the genus Thioploca could be responsible for converting the most abundant form of new nitrogen (NO3-) into biologically (intracellular) available substrate. This would be an important mechanism for introducing dissolved N into the seabed of the eastern Pacific shelf, representing about a third of the total N input into the sediments, when compared to the input via the rain of detritus and assuming that 10% of the primary production of 9.6 g C n r 2 d-' reaches the botton~. These and other observations (e.g. hydrothermal vents) demand a reassessment of the classic view of the benthic-pelagic coupling in marine systems. Mats of giant filamentous bacteria were first observed off northern Chile under the Peru-Chile Undercurrent (Gallardo 1963). They were later identified from central Chile as being made up of dense populations of Thioploca spp. (Beggiatoaceae) with biomasses of between 10 and 1000 g n1r2, potentially covering more than 40000 km2 of the sea bottom off southern Peru to central Chile (Gallardo 1977). The undercurrent is associated with the Equatorial Subsurface Water (ESSW) and is characterised by high salinity, low oxygen and nutrient-rich waters, which are source waters for wind-driven coastal upwelling that fertilises the Chilean and Peruvian coasts (Wooster & Gilrnartin 1961). The ESSW impinges on the seabed between depths of 50 and 280 m, creating a benthic environment with extended periods of suboxic and anoxic conditions that fluctuate intra-annually and interannually (e.g. with El Nilio) and have a strong influence on the mats' distribution and biomass. The metabolism of these marine bacteria has remained a mystery long after their discovery. An intensive field study of biogeochemical processes in sediments of the continental shelf in central Chile (36 S) was carried out in 1994 through a joint effort between German (Max Planck Institute for Marine Microbiology) and Chilean (University of Concepcion) researchers with the goal of understanding the metabolic pathways of Thioploca spp. Fossing et al. (1995) reported that Thioploca cells are able to concentrate nitrate up to 500 mM in a liquid vacuole that occupies >80% of the cell volume. This vacuole is surrounded by numerous sulphur globules embedded in the cytoplasm. They observed NO3uptake rates by Thioploca of ca 2.1 mm01 m-2 d-l, suggesting that they oxidise hydrogen sulphide using nitrate and behave as sulphide-oxidising denitrifiers. These observations were accompanied by flume studies that show chemotactic response towards nitrate-rich overlying waters with low oxygen conditions (Huettel et al. 1996). The fate of the large NO3pool inside the vacuoles of Thioploca spp, in this area has remained unclear. Thamdrup & Canfield (1996) found that sediment NO3consumption during incubations was not directly coupled to carbon oxidation (i.e. dissimilatory nitrate reduction), suggesting that the NO3consumed may be reduced to NH,' rather than to NZ, which would