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A Stromatolitic Cyanobacterial Crust in a Mediterranean Stream Optimizes Organic Matter Use

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A Stromatolitic Cyanobacterial Crust in a Mediterranean Stream Optimizes Organic Matter Use AQUATIC MICROBIAL ECOLOGY Vol. 16: 131-141, 1998 Published November 27 Aquat Microb Ecol A stromatolitic cyanobacterial crust in a Mediterranean stream optimizes organic matter use Anna M. Romani, Sergi Sabater* Departament d'Ecologia, Facultat de Biologia, Universitat de Barcelona, Avgda Diagonal 645. E-08028 Barcelona, Spain ABSTRACT: The bedrock of La Solana (NE Spain) stream is a thick calcareous cyanobacterial crust with a layered structure similar to a stromatolite. Different algal patches, which appear along with sea- sonal changes (especially discharge, temperature and light), characterize the stromatolite. This struc- ture has a great capacity for organic matter utilization, as indicated by the high extracellular enzymatic activities (P-glucosidase, P-xylosidase and phosphatase) measured in the stromatolibc algal patches over an annual cycle. However, each patch showed a particular ability in the use of organic matter since a different hydrolytic potential capacity was measured. The highest P-glucosidase and P-xylosi- dase activities were measured in the mixed community (cyanobacterial crust with a sparsely developed overstorey), indicating that the understorey of this stromatolitic crust is highly active. In the Zygnema- Spirogyra community, autotrophic activity might enhance P-glucosidase activity in spring, whilst in the diatom bloom (which appeared in May-June), polysaccharides released by algae and mucilagenous material from the diatom stalks might regulate the ectoenzymatic activities. The adaptation of the Rivu- laria community to oligotrophic condi.tions occurring in summer, autumn and winter is shown by the extremely high phosphatase activity, related to the low phosphorus concentration in stream water. The appearance and progressive substitution of the different patches can be interpreted as the adaptive response to the most available organic matter source, as well as a way of surviving the drastic environ- mental changes characteristic of Mediterranean streams. KEY WORDS: Organic matter . Stromatolite . Ectoenzymatic activities . Bacteria . Algae Mediterranean streams INTRODUCTION cyanobactena living in microbial mats are distributed heterogeneously and change their pigment composi- Microbial mats are dense benthic communities of tion in response to the incident light, temperature, and microorganisms which can give rise to laminated rocks water current (Stal et al. 1985, Hawes 1993, Pinckney known as stromatolites (Stal 1995). Stromatolites are et al. 199513). Cyanobacteria-dominated microbial mat formed through lithification processes such as binding communities are restricted to oligotrophic environ- and trapping of sediment particles, precipitated miner- ments. At high nutrient levels diatoms may be compet- als (e.g.calcite) and accumulation of incompletely min- itive dominants (Pinckney et al. 1995a). eralized organic matter (Chafetz & Buczynski 1992). Microorganisms living in stromatolitic microbial Bacteria, and especially cyanobacteria, play a signifi- mats have high metabolic activities (Cohen & Rosen- cant role in producing stromatolites (Abdelahad & berg 1989). The photoautotrophic and the heterotro- Bazzichelli 1989, Chafetz & Buczynski 1992). Extracel- phic communities of microbial mats are closely linked, lular polysaccharides released by diatoms are also showing high rates of photosynthesis and organic mat- involved (Winsborough & Golubic 1987). Algae and ter utilization (Canfield & Des Marais 1993, Paerl et al. 1993),although a higher production to respiration ratio 'Addressee for correspondence. was observed in a stromatolitic mat (Pinckney et al. E-mail: ssabaterOporthos.bio.ub.es 1995b). O Inter-Research 1998 132 Aquat Microb Ecol 16: 131-141, 1998 Our aim was to investigate organic matter utilization ous basin (Marti et al. 1994).The calcareous bedrock of in a stromatolitic cyanobacterial crust which devel- La Solana is covered by a lithified layer of cyanobacte- oped in a Mediterranean stream. La Solana bedrock ria and diatoms, creating a crusted structure similar to shows distinct patches characterized by different dom- a stromatolitic microbial mat. The distribution of differ- inating groups of taxa which follow a seasonal succes- ent algal patches on the cyanobacterial crust changes sion (Guasch & Sabater 1994). Each algal patch has a during the year, due to variations in discharge and characteristic photosynthetic behaviour (Guasch & light (Guasch & Sabater 1994). High photosynthetic Sabater 1995). We hypothesize that organic matter and respiration rates were observed in La Solana degradation processes may also be particular to each (Guasch & Sabater 1994, 1995), which may require algal patch and that their temporal dynamics in the high rates of heterotrophic carbon utilization. stream are related to different abilities in organic mat- This Mediterranean stream is subject to drastic sea- ter use. The capacity to break down organic matter sonality, and large fluctuations in discharge (minimum was studied by analyzing potential ectoenzymatic 0 1 SS' in summer, maximum 99.9 1 S-' in autumn) and activities. Extracellular enzymatic hydrolysis of macro- temperature (minimum 0.2OC in winter, maximum molecules is the first step in microbial degradation of 24.1°C in summer) have been observed (Marti et al. macromolecular organic compounds in aquatic envi- 1994, Marti & Sabater 1996).The riparian vegetation is ronments (Marxsen & Witzel 1990, Chr6st 1991). not well developed, with only a sparse canopy. Light is Microbial ectoenzymes (those bound to the cell sur- not limiting, being maximum in summer (maximum face) act outside the cell, converting high-molecular- value of 910 pE m-* S-'). The nutrient content is very weight molecules to low-molecular-weight molecules low, especially for soluble reactive phosphorus (5 to which are readily utilizable by heterotrophic microbes 10 pg 1-l) (Table 1). (Chr6st 1990). We analyzed the ectoenzymatic activi- Sampling. Samples of the stromatolitic crust were ties of P-glucosidase, P-xylosidase and phosphatase of collected monthly from January 1994 to February 1995. each patch monthly during an annual study. These The calcareous cyanobacterial crust is permanent over enzymes are involved in the degradation of polysac- the year and the different algae developing over the charides (cellulose, hemicellulose) and orthophos- crust characterize the visually different algal patches: phoric monoesters which are plant and/or animal poly- the Rivularia community, the Zygnerna-Spirogyra mers originating in rivers from both autochthonous and community, the diatom bloom and the mixed community allochthonous sources. Electron transport was also (Guasch & Sabater 1995). Each patch, consisting of an measured and used as a general estimate of the respi- understorey (the permanent crust) and an overstorey, ratory activity of each stromatolitic patch. was defined when appearing in the stream over more than 10 % of the streambed surface. The algal cover on the stream surface was evaluated by several transects MATERIALS AND METHODS along a 100 m reach. Relative density of algal cover was established from 0 to 100% in the area defined by an Study site. La Solana, located in NE Spain, is an underwater viewer (0.16 m*),which was used to visual- undisturbed second-order stream draining a calcare- ize the relative densities along each transect. Table 1. Physical and chemical characteristics of La Solana stream during the study period. Values are seasonal means, except summer values which correspond to early July, when water was only in small pools. From then until the end of August the stream was totally dry. Values in brackets are the standard deviations of the mean (n = 6 but n = 3 in summer and autumn 1994) Winter Spring Summer Autumn Winter 1994 1994 1994 1994 1995 Discharge (I S' ') l0 (2.1) 12 (3.3) 0 (0) 26 (12) 18 (3.2) Temperature ("C) 0.7 (0.3) l l .6 (3.9) 24.8 (4.6) 8.6 (4.2) 2.9 (2.8) Llght (PE m-2 S-') 140 (35) 496 (301) 710 (387) 188 (122) 112 (27) Conductivity (pS cm-') 470 (16) 400 (23) 606 (53) 405 (48) 408 (l 8) PH 8.3 (0.1) 8.2 (0.1) 7.7 (0.2) 8.0 (0.3) 8.5 (0.6) Oxygen (mg 1-') 10.9 (3.6) 8.0 (3.3) 1.5 (0 8) 11.0 (3.7) 11.8 (0.1) NO3-N (pg I-') 181 (51) 71 (65) 269 (63) 187 (83) 202 (116) NH4-N (pg I-') 35 (1.3) 24 (13) 2939 (1040) 27 (17) 29 (15) SRP (pg I-') 1.6 (0.5) 2.1 (2.6) 65 (51) 4.7 (0.9) 1.3 (1.1) D1N:SRP 465 (214) 764 (1130) 49 (20) 102 (49) 116 (83) DOC (mg 1- l) 1.8 (0.3) 6.9 (5.5) 128 (9.6) 5.7 (2.9) 4.7 (1.0) DIC (mg I-') 62.8 (5.1) 59.6 (4.1) 40.1 (4.8) 47.4 (5.4) 48.0 (3.1) Romani & Sabater: Organic mattt?ruse in cyanobacterial crusts 133 On each sampling date, pieces of each patch (0.5 to ilized stream water were also incubated. After addition 1 cm thick) were placed in sterile glass vials with of 0.05 M glycine buffer, pH 10.4, fluorescence was stream water. Samples were kept cold (on ice) and in measured at 455 nm under 365 nm excitation (Kontron, the dark for transport. Samples from July and August SFM25). 1994 (dry period) were transported wrapped in alu- Primary prod.uction was measured as HI4CO3incor- minium foil. The analyzed samples were approxi- poration. Samples (3 replicates) and formaldehyde- mately 1.1 cm2 in surface area. Samples for chlorophyll killed controls were incubated at 150 PE m-2 S-'. Dark analysis were frozen and kept in the dark until pig- replicates were included. Incubation was perfomed in ment extraction. For bacterial cell counts, samples a shaker for 2 h at ambient stream temperature, inject- were placed in sterile glass vials with 2% formalin. ing 1 pCi of NaH1"C03 into each tube (Sabater & Activity measurements (extracellular enzyme analy- Romani 1996). Radioactivity was measured in a ses, photosynthetic activity and respiratory activity) Packard Tri-carb 1500 liquid scintillation analyser. Pri- were measured on the same day, 2 to 3 h after sam- mary production was only analyzed in the mixed com- pling.
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