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Anoxic Thermomineral Cave Waters and Bacterial Mats As Habitat for Freshwater Nematodes

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Anoxic Thermomineral Cave Waters and Bacterial Mats As Habitat for Freshwater Nematodes AQUATIC MICROBIAL ECOLOGY Vol. 18: 157-164,1999 hblished August 9 Aquat Microb Ecol I Anoxic thermomineral cave waters and bacterial mats as habitat for freshwater nematodes Wolfgang Riessl,*, Olav ~iere~,Oliver Kohlsl, Serban M. sarbu3 'Max Planck Institute for Marine Microbiology, Celsiusstr. 1. D-28359 Bremen, Germany ZZoological Institute and Zoological Museum. University of Hamburg. Martin-Luther-King-Platz 3, D-20146 Hamburg, Germany 3Department of Biological Sciences, University of Cincinnati, 821-A Rieveschl Hall, Cincinnati, Ohio 45221-0006, USA ABSTRACT: A unique chemoautotrophic system of floating microbial mats was examined in a subter- ranean cave in southern Romania. Oxygen measurements were made with a recently developed tech- nique applying micro-optodes. The oxygen uptake rate of the anoxic and sulfidic cave waters over the atmosphere/water interface was as high as 103.3 i 9.1 mm01 O2 m-2 d-l. Floating microbial mats con- sisting primarily of sulfide oxidizers and fungal mycelia were found to be adapted to reduced oxygen supply and thrived even under strict anoxia. These 2 mm thick mats were inhabited by 5 different spe- cies of nematodes, reaching densities of 9.8 X 106 ind. m-2 Possible alternative pathways for growth of the mats and also for the persistence and reproduction of nematodes under strict anoxic conditions are discussed. KEY WORDS: Microbial mat . Chemoautotrophic . Cave . Nematodes . Anoxia . Optode INTRODUCTION (Fenchel & Finlay 1995), all free-living and parasitic Metazoa seem to need oxygen at least for their repro- The ability to survive in anoxic (and sulfidic) envi- ductive stages (i.e. eggs, larvae) (Barrett 1991). ronments has been reported for many Protozoa and A community of 5 nematode species was discovered Metazoa (Bryant 1991, Giere 1992, Grieshaber et al. thriving within floating microbial mats under com- 1994, Fenchel & Finlay 1995, Hochachka 1997, pletely anoxic, experimental conditions for several Grieshaber & Volkel 1998).In sediments, the question months in a thermomineral sulfide-rich groundwater whether a 'thiobios' exists and how it is to be defined system in Movile Cave, Romania. has been long debated after the first description of the A recently developed, extremely sensitive oxygen sulfide system by Fenchel & Riedl (1970). There is a detector with very high spatial resolution and capable consensus that many taxa can live for extended periods of detecting even traces of oxygen (detection limit of time without oxygen and, thus, are well adapted to 10 ppb, Klimant et al. 1997) was used to confirm com- hypoxia (i.e. exhibit physiological or behavioural plete anoxia. adaptations). But reports regarding Metazoa that live The Movile Cave groundwater system was discov- permanently under anoxic conditions remain circum- ered in 1986 (Lascu 1989). It contains a rich and abun- stantial without detailed experimental proof whether dant community of aquatic and terrestrial inverte- the populations examined were able to temporarily brates isolated from the surface for a considerable take up traces of oxygen by moving within the vertical amount of time (Sarbu & Kane 1995).The subterranean gradients or by extending at least a part of their body ecosystem is based entirely on food produced in situ by into oxic layers or microniches. Thus, the supply of chemoautotrophic microorganisms (Sarbu et al. 1996). some oxygen cannot be excluded (Fenchel & Finlay Sulfur-oxidizing and methane-oxidizing bacteria were 1991, 1995). In contrast to specialized Protozoa identified in samples of water and microbial mats from Movile Cave (Sarbu et al. 1994, 1996, Vlasceanu et al. 1997). O Inter-Research 1999 Aquat Microb Ecol 18: 153-164, 1999 MATERIAL AND METHODS mats on the surface of the lake. In 1992, plexiglass enclosures were set afloat on the surface of the lake to Site. Movile Cave is located in Southern Dobrogea, create artificial air bells (Fig. 2). Openings in their Romania, close to the coastline of the Black Sea and to walls allowed a controlled access of oxygen. Floating the town of Mangalia (Fig. 1). Large subterranean microbial mats developed in those artificial air bells, voids of karst origin host a captive thermomineral sul- whose atmosphere resembled that within the cave's fidic aquifer at depths of 200 m below the surface. In natural air bells. the Mangalia region these waters ascend to the surface Sampling. Biological samples were collected and in along natural faults. They form natural springs and are situ measurements of the physico-chemical parameters found as sulfidic groundwaters in the superficial Sar- of the subterranean environment were performed in matian Limestones (Lascu 1989). Movile Cave and in other sulfide-rich epigean habitats Movile Cave, a 240 m long system of natural cave in April 1994, April 1996, November 1996 and July passages located 20 m under the surface, was discov- 1998. Several different habitats were screened for the ered in 1986 when an artificial shaft intercepted a sec- presence of meiofauna. Samples of microbial mats with tion of the cave. A small lake in the deep section of their inhabitant fauna and some original water were Movile Cave (Fig. 2) permits access to the lower level collected in Movile Cave in April 1994 and were cul- of the cave, which is partially flooded by thermomin- tured in 50 m1 centrifuge tubes (Sarstedt). The tubes, era1 water and contains several air bells (Sarbu & Kane which were sealed and stored in an air-tight container 1995). in the dark at room temperature, were opened 11 mo The air in the lake room has an oxygen content close later and inspected for living animals. Additional vials to normal epigean air conditions (02:20%, CO2: 1.5%) containing mat material were fixed with buffered whereas in the small adjacent air bells, which can be formaldehyde solution (final concentration approx. reached by divers only, the oxygen content is lower 5 %) immediately after sampling. Nematodes living in and CO2 and methane concentrations are higher (02:7 the dense microbial mat substrate were sorted out and to 10 %, CO2:2 to 3.5 %, CH,: 1 %) (Sarbu & Popa 1992, counted under a dissecting microscope immediately this study, Fig. 2). after return to the Center for Ecological Research, in The specific physico-chemical conditions at the Mangalia. Some specimens were mounted on perma- interface between the thermomineral sulfidic water nent slides (Riemann 1988) and stored for later identi- and the significantly modified atmospheric conditions fication. in the cave's air bells allow the development of floating Mat material from the anoxic artificial air bells was microbial mats which can attain a thickness of 2 to frozen and later processed with the French press tech- 3 mm (Fig. 2). The oxygen-rich atmosphere in the lake nique (American Instruments Co. Inc., Silver Spring, room prevents the development of floating microbial USA) to measure nitrate accumulation within the cells and/or mat. The nitrate measurements were done using a 42C NO-NO2-NO, Analyzer (Thermo Environ- mental Instruments, Reference Method RFNA-1289- 074) (see Braman & Hendrix 1989). Water samples were collected in 5 cm intervals between 5 and 90 cm using 1 m1 syringes to determine the concentration of hydrogen sulfide (total soluble sulfide: HIS, HS-, S2-)in the cave water. The samples were fixed with alkaline zinc-acetate solution and were measured photometrically (Gilboa-Garber 197 1, modified). The chemical composition of the atmos- phere in the lake room and in the artificial air bells was Black determined using a Drager hand pump (accuro) and Sea Drager test tubes for oxygen (no. 6728081), carbon BULGARIA dioxide (no. 8101931) and hydrogen sulfide (no. 6728041). High resolution measurements of oxygen con.centra- tions in the water column were performed in Novem- ber 1996 in the cave lake and in the artificial air bells. A fiber optical microsensor (optode) (Klimant et al. Fig. 1. Location of the cave in Southern Dobrogea in the 1995) was connected to an autonomous electronic sys- southeast of Romania tem (Glud et al. 1999) suitable for the specific demands Riess et al.. N(.matodes in anoxic cave waters 159 Lake room 20 % 0, 0.5-1 % CO, Air bell 2 \ Silt - Current - - - 9, -,"'" "'""'"/.\, CU -r- -.I i- - i- 1- -+ -. Fig. 2. Transect through the cave. Oxygen and CO, contents of the different compartments are given in vol.%. The oxygen mea- suring setup includes a micromanipulator (mi)for accurate positioning of the optodes mounted in diflerent ways. blicrobial mats (ma) only form where oxygen is significantly reduced of the cave environment. This battery powered system calibration of the optode. This function was deter- was used for one of the first in situ measurements mined by adjusting the sensor signal to 9 different oxy- within the frame of an ecological study. gen concentrations (0, 5, 10, 25, 40, 55, 70, 85, 100% air Optode measurements. The principle of fiber optic saturation). Based on this function, the optode was cal- oxygen measurements is luminescence quenching of a ibrated before the nleasurement at 0 and 100% air sat- dye which is sensitive to oxygen. This type of sensor uration. The detection limit for oxygen of 10 ppb (02 was chosen over the traditional Clark-type electrode dissolved in water) can be reduced to 0.5 ppb (or since it does not consume oxygen and thus lacks a stir- 0.1 pM) by using a newly developed dye/matrix sys- ring effect. Additionally optodes have their highest ten1 (Klimant pers. comm., Kiihl & Revsbech in press). sensitivity at low oxygen concentrations (because of a Oxygen profiles in the cave water were measured in non-linear relation between oxygen concentration and the uppermost layers of the lake's open water to deter- optical signal). A 100/140 micrometer silica/silica mine the depth of oxygen penetration into the water graded index fiber material (Radiall, Germany) was column and to calculate oxygen fluxes under normoxic used for the preparation of fiber optical microsensors conditions.
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