Abstract
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.
Highlights
Over 3 billion years of evolutionary history has endowed cyanobacteria with an arsenal of time-tested structural adaptations and physiological mechanisms enabling them to thrive under environmental extremes (Falkowski et al, 2008; Voorhies et al, 2015)
This action is characterized by mass movement of sections of microbial mat driven by the random motility of individual filaments bending, pushing, and gliding by one another (Hoiczyk, 2000)
The El Cajon Bay (ECB; 0.25–2 m, with mats receiving 50– 90% of sunlight incident at the lake surface) and Middle Island Sinkhole (MIS; ∼23 m, with mats receiving 5–10% of sunlight incident at the lake surface), contain groundwater vents providing habitat for mat-forming cyanobacteria mainly comprised of the genus Oscillatoria and Phormidium (Voorhies et al, 2012)
Summary
Over 3 billion years of evolutionary history has endowed cyanobacteria with an arsenal of time-tested structural adaptations and physiological mechanisms enabling them to thrive under environmental extremes (Falkowski et al, 2008; Voorhies et al, 2015). The cyanobacteria respond to discrete chemical signals, exhibiting chemotactic movement to optimize chemical intake or avoid harmful environments (Chet and Mitchell, 1976) Such dynamic behavior appears to contribute to the unique microbial mat structure and its interactions with the environment. Water, and geologic forces have converged to create underwater sinkholes in Lake Huron supporting prolific microbial mats that resemble life as it may have existed throughout much of Earth’s deep history (Biddanda et al, 2012). Ability of filaments to move at environmentally meaningful rates may confer major advantages to Oscillatoria for closely tracking and acquiring light and limiting nutrients across the diurnally variable light and sharp redox gradients that prevail in submerged sinkhole ecosystems If confirmed, such a motile life strategy by matforming cyanobacteria should have significant collective impact on the biogeochemistry of these lacustrine benthic habitats. High magnification images were obtained by a Nikon eclipse 80i microscope using NIS elements basic Research Software, and photograpahed with a QIClick digital camera (QImaging, Surry, BC, Canada) as described in Voorhies et al (2012)
Sign-in/Register to view highlights & summary Sign-in/Register to access full text options 
Free) 
Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a call
