Cyanobacteria are renowned as the mediators of Earth's oxygenation. However, little is known about the cyanobacterial communities that flourished under the low-O(2) conditions that characterized most of their evolutionary history. Microbial mats in the submerged Middle Island Sinkhole of Lake Huron provide opportunities to investigate cyanobacteria under such persistent low-O(2) conditions. Here, venting groundwater rich in sulfate and low in O(2) supports a unique benthic ecosystem of purple-colored cyanobacterial mats. Beneath the mat is a layer of carbonate that is enriched in calcite and to a lesser extent dolomite. In situ benthic metabolism chambers revealed that the mats are net sinks for O(2), suggesting primary production mechanisms other than oxygenic photosynthesis. Indeed, (14)C-bicarbonate uptake studies of autotrophic production show variable contributions from oxygenic and anoxygenic photosynthesis and chemosynthesis, presumably because of supply of sulfide. These results suggest the presence of either facultatively anoxygenic cyanobacteria or a mix of oxygenic/anoxygenic types of cyanobacteria. Shotgun metagenomic sequencing revealed a remarkably low-diversity mat community dominated by just one genotype most closely related to the cyanobacterium Phormidium autumnale, for which an essentially complete genome was reconstructed. Also recovered were partial genomes from a second genotype of Phormidium and several Oscillatoria. Despite the taxonomic simplicity, diverse cyanobacterial genes putatively involved in sulfur oxidation were identified, suggesting a diversity of sulfide physiologies. The dominant Phormidium genome reflects versatile metabolism and physiology that is specialized for a communal lifestyle under fluctuating redox conditions and light availability. Overall, this study provides genomic and physiologic insights into low-O(2) cyanobacterial mat ecosystems that played crucial geobiological roles over long stretches of Earth history.
Physicochemical characterization, automated ribosomal intergenic spacer analysis (ARISA) community profiling, and 16S rRNA gene sequencing approaches were used to study bacterial communities inhabiting submerged Lake Huron sinkholes inundated with hypoxic, sulfate-rich groundwater. Photosynthetic cyanobacterial mats on the sediment surface were dominated by Phormidium autumnale, while deeper, organically rich sediments contained diverse and active bacterial communities.Groundwater intrusion is becoming recognized as an important source of nutrients, contaminants, and trace elements in aquatic ecosystems (7). Recent reports regarding marine habitats suggest that groundwater influences nitrogen inputs (29) and may have a significant impact on nutrient dynamics over seasonal (27) and longer (25) time scales. To date, investigations of groundwater effects have focused primarily on marine habitats. To better understand the impact of groundwater intrusion into freshwater habitats, we have been studying submerged sinkholes in the Laurentian Great Lakes.Sinkholes typically develop in areas of terrestrial karst when underground caverns collapse (36). We recently discovered submerged sinkholes that occur beneath the surface of Lake Huron in water up to a depth of 93 m (9, 41). These unique habitats are formed by groundwater dissolution of Paleozoic limestone and marine evaporite sediments in the Michigan Basin (16). Some sinkholes actively release cold, dense groundwater through underwater vents onto the lake floor. The venting groundwater has a lower pH (ϳ7.1), higher specific conductivity (ϳ2.3 mS ⅐ cm Ϫ1 , due to high levels of dissolved sulfate [Ͼ1,000 mg ⅐ liter Ϫ1 ], carbonate, and chloride ions), and lower concentrations of dissolved oxygen (Ͻ0.4 mg ⅐ liter Ϫ1 ) and nitrate than Lake Huron water (2,3,41,42). The intrusion of cold, hypoxic, sulfate-rich groundwater greatly alters the local lake habitat and has a significant impact on the sediment microbial community. Sediments at nearby control sites are sandy, but submerged sinkhole sediments (with carbon accounting for 5 to 35% of the sediment dry weight) are rich in organic matter originating from phytoplankton in the overlying water column
In the northern Great Lakes region, limestone sediments deposited some 400 million ybp during the Devonian era have experienced erosion, creating karst features such as caves and sinkholes. The groundwater chemical constituents of the shallow seas that produced these rock formations now contribute to the formation of a unique physical (sharp density gradients), chemical (dissolved oxygen-depleted, sulfate-rich) and biological (microbe-dominated) environment in a submerged sinkhole near Middle Island in freshwater Lake Huron. A variety of methods including aerial photography, physico-chemical mapping, time series measurements, remotely operated vehicle (ROV) survey, diver observations and bathymetric mapping were employed to obtain a preliminary understanding of sinkhole features and to observe physical interactions of the system's groundwater with Lake Huron. High conductivity ground water of relatively constant temperature hugs the sinkhole floor creating a distinct sub-ecosystem within this Great Lakes ecosystem. Extensive photosynthetic purple cyanobacterial benthic mats that characterize the benthos of this shallow sinkhole were strictly limited to the zone of ground water influence.
Dissolution of the Silurian-Devonian aquifer in the Lake Huron Basin has produced several karst formations in the bedrock (sinkholes), through which groundwater emerges onto the lake floor. During September 2003, we explored a recently discovered submerged sinkhole ecosystem (55 m · 40 m · 1 m) located at a depth of 93 m with a remotely operated vehicle (ROV) equipped with a conductivity-temperature-depth (CTD) system, an acoustic navigational system, a video camera, and a water sampling system. In addition to two morphotypes of benthic mats, a 1-2 m thick visibly cloudy near-bottom nepheloid-like layer (sinkhole plume) with a strong hydrogen sulfide odor prevailed just above the seepage area of clear water. Relative to lake water, water samples collected within the sinkhole plume were characterized by slightly higher (by 4°C) temperatures, very high levels of chloride (up to 175 mg l )1 ) and conductivity (1,700 lS cm
Recent underwater explorations have revealed unique hot spots of biogeochemical activity at several submerged groundwater vents in Lake Huron, the third largest of the Laurentian Great Lakes. Fueled by venting groundwater containing high sulfate and low dissolved oxygen, these underwater ecosystems are characterized by sharp physical and chemical gradients and spectacularly colorful benthic mats that overlie carbon‐rich sediments. Here, typical lake inhabitants such as fish and phytoplankton are replaced by communities dominated by microorganisms: bacteria and archaea that perform unique ecosystem functions. Shallow, sunlit sinkholes are dominated by photosynthetic microorganisms and processes, while food webs in deep aphotic sinkholes are supported primarily by chemosynthesis.
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