We studied the motility of filamentous mat-forming cyanobacteria consisting primarily of Oscillatoria-like cells growing under low-light, low-oxygen, and high-sulfur conditions in Lake Huron’s submerged sinkholes using in situ observations, in vitro measurements and time-lapse microscopy. Gliding movement of the cyanobacterial trichomes (100–10,000 μm long filaments, composed of cells ∼10 μm wide and ∼3 μm tall) revealed individual as well as group-coordinated motility. When placed in a petri dish and dispersed in ground water from the sinkhole, filaments re-aggregated into defined colonies within minutes, then dispersed again. Speed of individual filaments increased with temperature from ∼50 μm min-1 or ∼15 body lengths min-1 at 10°C to ∼215 μm min-1 or ∼70 body lengths min-1 at 35°C – rates that are rapid relative to non-flagellated/ciliated microbes. Filaments exhibited precise and coordinated positive phototaxis toward pinpoints of light and congregated under the light of foil cutouts. Such light-responsive clusters showed an increase in photosynthetic yield – suggesting phototactic motility aids in light acquisition as well as photosynthesis. Once light source was removed, filaments slowly spread out evenly and re-aggregated, demonstrating coordinated movement through inter-filament communication regardless of light. Pebbles and pieces of broken shells placed upon intact mat were quickly covered by vertically motile filaments within hours and became fully buried in the anoxic sediments over 3–4 diurnal cycles – likely facilitating the preservation of falling debris. Coordinated horizontal and vertical filament motility optimize mat cohesion and dynamics, photosynthetic efficiency and sedimentary carbon burial in modern-day sinkhole habitats that resemble the shallow seas in Earth’s early history. Analogous cyanobacterial motility may have played a key role in the oxygenation of the planet by optimizing photosynthesis while favoring carbon burial.

No abstract

During the summers of 2002–2013, we measured rates of carbon metabolism in surface waters of six sites across a land-to-lake gradient from the upstream end of drowned river-mouth Muskegon Lake (ML) (freshwater estuary) to 19 km offshore in Lake Michigan (LM) (a Great Lake). Despite considerable inter-year variability, the average rates of gross production (GP), respiration (R) and net production (NP) across ML (604 ± 58, 222 ± 22 and 381 ± 52 µg C L−1 day−1, respectively) decreased steeply in the furthest offshore LM site (22 ± 3, 55 ± 17 and −33 ± 15 µg C L−1day−1, respectively). Along this land-to-lake gradient, GP decreased by 96 ± 1%, whereas R only decreased by 75 ± 9%, variably influencing the carbon balance along this coastal zone. All ML sites were consistently net autotrophic (mean GP:R = 2.7), while the furthest offshore LM site was net heterotrophic (mean GP:R = 0.4). Our study suggests that pelagic waters of this Great Lakes coastal estuary are net carbon sinks that transition into net carbon sources offshore. Reactive and dynamic estuarine coastal zones everywhere may contribute similarly to regional and global carbon cycles.

Recently discovered submerged sinkholes in Lake Huron are high-sulfur, lowoxygen extreme environments for microbial life. In order to understand the relationship between the physical environment, photophysiology and community composition, we measured the physical conditions, photophysiological indices, and genetic diversity at 3 microbial mat sites bathed in high conductivity groundwater under a natural light gradient during 2012 and 2013. A strong seasonal trend prevailed at all sites, characterized by decreased photosynthetic yield (F v '/F m '; 0.25 to 0.40) during the summer (April to August) and increased yield (0.70 to 0.75) during the winter (November to March). Chlorophyll a content varied seasonally in a similar manner to photosynthetic yield. All sites were dominated by > 80% abundance of one cyanobacterial group, most closely related to Phormidium sp. Phycobilins (phycocyanin and phycoerythrin) were consistently higher in concentration than chlorophyll. Photosynthetic yield was statistically indistinguishable between sites, suggesting that these mat communities are able to acclimate across a wide range of photosynthetically active radiation (PAR). Interestingly, these cyanobacteria carried out oxygenic photosynthesis in the presence of in vitro H 2 S, further suggestive of their versatile photophysiologies under variable redox conditions. Collectively, our study provides insight into the adaptive capabilities of cyanobacteria by revealing how they photophysiologically respond to changes in light climate and redox conditions, and are thereby able to inhabit a wide range of physico-chemical environments. Such versatile physiologies may have enabled their ancestors to thrive across a range of habitats on early Earth.