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Metagenomics of a Microbial Mat

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Metagenomics of a Microbial Mat MBL Microbial Diverstity Course 2012 A mat gone mad – Metagenomics of a microbial mat Thiele, S. Dept. of Molecular Ecology, Max-Planck-Institute for Marine Microbiology, Bremen, Germany Contact: [email protected] Abstract Microbial mats are widely occurring ecosystems of distinct bacterial populations forming different layers in a stacked manner. Within and among these layers, a tight coupling of different metabolic pathways, namely photosynthesis, sulfur metabolism, methane metabolism and nitrogen metabolism have been found. These pathways are tightly coupled over the diurnal cycle, leading to changes in chemical gradients during a days turn. By using chemical analyzes, like microsensor measurements and anion ion-exchange chromatography combined with molecular tools like 454 pyrosequencing and metagenomics, the metabolic pathways within an intertidal microbial mat from the Great Sippewisset Salt Marsh was investigated. Oxygenic photosynthesis was confirmed within the cyanobacterial layer of the mat, while hints for anoxygenic photosynthesis were found throughout the mat. Sulfate reduction as well as sulfite oxidation was predicted throughout the mat, while methane oxidation was only indicated for the uppermost layer (???). In contrast, indications for methanogenesis were not found. Nitrogen fixation, ammonium assimilation, denitrification and DNRA were indicated throughout the microbial mat, while amoA, the marker gene for nitrification was only found in the two uppermost layers. In addition to the prediction of pathways, several marker genes could be assigned to taxonomic information and then compared to data retrieved from 454 pyrosequencing, linking functional features with identity. Thus some light was shed on the microbial communities of microbial mats from the Great Sippewisset Salt Marsh in context of their function in the ecosystem.These findings showed that metagenomics in combination with chemical measurements can be used to answer some of the major questions in microbial ecology. Introduction Laminated microbial ecosystems, widely referred to as microbial mats, are found in various environments, like hot springs (e. g. Ward et al., 1997) or hypersaline ponds (e. g. Sørensen et al., 2005), but also in intertidal sediments, like those found in Great Sippewisset Salt Marsh (Nicholson et al., 1987). Due to different chemical environments, distinct layers are formed by microbial groups with different ecological functions. These layers are tightly linked in their metabolic processes (Fig 1). Due to these processes, different ecological niches are created and colonized by different organisms. Several chemical cycles have been described for microbial mats. Photosynthesis is the main driver of primary production in the upper layers of the mat. Here oxygen is produced by mainly Cyanobacteria, creating an oxic environment. In deeper anoxic layers anoxygenic photosynthesis, by e.g. Green Sulfur Bacteria occurs (Nicholson et al., 1987). Tightly coupled with the oxygen production is the reduction of hydrogen sulfide to sulfate. In the oxygen depleted zone of the mat hydrogen sulfite is produced by sulfate reducing bacteria and gases out into higher layers. Reaching the oxic zone, H2S is oxidized again. This chemical gradient of oxygen and hydrogen sulfite is influenced by the diurnal cycle. During the night, when photosynthesis is intermitted, oxygen is depleted and hydrogen sulfite concentrations increases. During the day the process is reversed by aerobic sulfite oxidation and H2S concentrations decreases (Jørgensen et al., 1979). In addition to the sulfur cycle, also the nitrogen cycle of microbial mats is dependent on the separation of oxic and anoxic layer. In the upper layer nitrogen is fixed, most likely by Cyanobacteria, and the resulting ammonia is either assimilated or nitrified to nitrate. In the anoxic layer, the anaerobe part of the nitrogen cycle takes part. In contrast to anaerobic fixation of N2 (Bonin and Michotey, 2006), Denitrification and Anammox lead to the formation of N2, while dissimilatory nitrate reduction to ammonium (DNRA) and ammonification can produce ammonium (Bonin and Michotey, 2006). Besides sulfur and nitrogen metabolism, the finding of methane production and oxidation in microbial mats added another metabolic pathway (Buckley et al., 2008). Potential methane production rates were found highest at the chemocline between 5 and 10 mm depth in mats from Great Sippewisset Salt Marsh near Cape Cod, Massachusetts, USA. Nevertheless methane production was also found in anoxic and the oxic cyanobaterial layer (Buckley et al., 2008). In contrast to high production, low amounts of methane gas were found at the mat surface, indicating aerobic methane oxidation in the top layer and anaerobic methane oxidation in the deeper layers (Buckley et al., 2008). Fig. 1: Photosynthesis, sulfur and nitrogen cycling in a microbial mat during the diurnal cycle. L. Villanueva, 2011, unpublished. Besides investigation of the methane cycling, the microbial mats of Great Sippewisset Salt Marsh have been subject to research for a long time. It usually consists of a Cyanobacteria dominated green/ brown layer, a pink layer dominated by purple sulfur bacteria, a black layer inhabiting green sulfur bacteria and a gray layer with methylotrophic methanogenes (Nicholson et al., 1987; Imhoff and Pfennig, 2001; Zaar et al., 2003; Buckley et al., 2008). However, most studies were focused on phototrophic organisms and few molecular tools were applied to the system. Here I describe the investigation of photosynthesis and sulfur, nitrogen and methane metabolisms within a microbial mat sampled in 2010. I used metagenomics to approach the metabolic potential of the 5 different layers of the microbial mat. This method, based on culture independent sequencing of environmental DNA, is used to investigate three major questions of microbial ecology. Who is there? What are they doing? How is it compared to other environments? In other words, the taxonomic content of a sample can be analyzed, the functional content of the sample can be explored and results can be compared to other environments (Reviewed e.g. in Wooley et al., 2010). Therefore metagenomics is a powerful tool to test hypothesis based on chemical measurements and explore the metabolic potentials of microbial communities. In this study hypothesis about metabolic pathways were developed based on microsensor measurements and nutrient analyzes. These hypotheses were then tested using the metagenomics approach combined with 454 tag pyrosequencing to determine the taxonomic identity of the key organisms in the different metabolic pathways throughout the 5 layers of the microbial mat. Material & Methods Sampling A microbial mat was collected on the 3rd of July 2012 during day time at low tide in Great Sippewisset Salt Marsh (41°58.599 N/ 70°64.083 W). A 30 mm thick microbial mat was taken from an air exposed area and brought back to the laboratory. The mat displayed 5 distinct layers. A brown layer covering the top of the mat, a green layer from 0-4 mm, a purple layer from 4-6 mm, black layer from 6-12 mm and a thick sand layer on the bottom. The mat was covered with Sea Water Base (SWB) with a pH of ~4.6 for approx. 2 hours after sampling and stored until and during microsensor measurements. An additional mat of ~25 mm thickness was sampled from the same spot on the 17th of July during mid day and stored in ambient water taken from a stream next to the mat. This consisted from 5 layers, showing an aging process of the mats. A very small brown layer was found on the top, followed by a green layer (0-2 mm), a pink layer (2-4 mm), an orange layer (4-6 mm), a black layer (6-9 mm) and a sandy layer (9-25 mm). Microsensor measurements In order to characterize the microbial mats and build hypothesis about the metabolic pathways taking place, I used oxygen, pH and hydrogen sulfite sensors from Unisense (Arrhus, Denmark) to measure depth profiles of both mats during light and dark phases. Light phases were simulated with a 75 W bulb emitting 1300 mE m-2 s-1, while dark phases were measured in darkness. Between the light and dark phase, the mat was allowed to acclimatize for min. 30 minutes in the dark. Depth profiles of the first sampling were obtained in steps of 60 µm starting at the water surface and ending at 2.9 cm depth of the mat. For the second mat similar profiles were done to a depth of 2.5 cm. All sensors were sensitive in a range of 50 µm. Nutrient measurements After both microsensor applications pore water was extracted from all 4 or 5 layers of the mat. I used the microsensor stand to navigate syringes with 26.1 G needles to the specific layers in order to extract 1-1.5 ml of pore water. The water was rinsed according to the protocol for Anion Ion-Exchange Chromatography (IC) and 1:10 dilutions (in water) were analyzed using an ICS2100 (Thermo Fischer, Sunnyvale, USA). Ammonium concentrations of the old mat were measured using a colorimetric assay after Solorzano (Solorzano et al., 1969). Sampling for 454 tag pyrosequencing After microsensor measurements the mat from the 3rd of July was skimmed and sub samples of all layers were used for DNA extraction. I used the MoBio PowerSoil DNA Isolation Kit (MoBio, Carlsbad, CA, USA) for extraction. Amplification of the V6 region of the 16S rRNA was done with universal primers tagged with marker sequences. I used sequences C1-C4. The PCR fot the 16S rRNA V9 region was done using 15 µl of Phusion Master Mix, 2.4 µl DMSO, 0.6 µl Reverse and 0.3 µl Forward Primer (provided by course staff) and 2 µl of template DNA. The PCR was run using a touch down program. Denaturing was done for 5 s at 98°C and elongation for 7 s at 72°C. Annealing was done for 10 s with a touch down step in 10 cycles starting at 68°C and decreasing for 1°C every cycle.
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