Seeking sunlight: rapid phototactic motility of filamentous mat-forming cyanobacteria optimize photosynthesis and enhance carbon burial in Lake Huron’s submerged sinkholes

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.

Groundwater shapes sediment biogeochemistry and microbial diversity in a submerged Great Lake sinkhole

“…It seems that the chemical environment established by venting groundwater in the MIS allows microbial mat communities to establish, in part by relieving grazing pressure due to low dissolved oxygen concentrations (Stal, 1995). The MIS microbial mat is capable of high primary production rates (Voorhies et al, 2012), yet underlying sediments largely reflect isotopic characteristics of settling phytoplankton (Nold et al, 2013), implying rapid decomposition of mat biomass prior to burial (Canfield & Des Marais, 1993) and/or significant upward mat motility (Biddanda, McMillan, Long, Snider, & Weinke, 2015) to avoid burial.…”

“…Although microbial mat biomass is often rapidly, and sometimes completely, decomposed before burial (Canfield & Des Marais, 1993), mats likely play direct and indirect roles in establishing and maintaining high-nutrient conditions of underlying sediment material, further enhancing the high-nutrient conditions encouraged by the low-oxygen environment. The mats may play a direct role in sediment nutrient conditions through their motility, which allows them to physically bury organic particles (Biddanda et al, 2015;Stal, 1995). In addition, their extracellular polysaccharide matrix can slow diffusion of nutrient molecules and limit re-suspension of particles into overlying waters (Benjamini & Hochberg, 1995).…”

Versatile photophysiology of compositionally similar cyanobacterial mat communities inhabiting submerged sinkholes of Lake Huron

“…These conditions simultaneously act to de crease the incident angle of oncoming PAR for cyanobacteria on the plants, and cyanobacterial growth on these substrates may promote self-shading. The cyanobacteria can take advantage of these physical features over small scales by rapid phototactic motility (Biddanda et al , 2015. Oxygen is available for those cyanobacteria located on or even near these plants (perhaps in only small amounts), which provides some benefit in the form of respiration.…”

“…For example, the cyanobacterial community in EC was preferentially attached below plants and detrital rafts, receiving a different angle of radiation. The cyanobacterial assemblage in these natural environments, dominated by similar Phormidium sp., has strong phototactic responses (Biddanda et al 2015). On the other hand, cyanobacteria at FT were frequently in direct, high irradiance, with minimal options for phototactic or photoaverse movement.…”

“…1 inset; Biddanda et al 2009). To date, no other studies have analyzed the in vitro pigment content or in situ photosynthetic yield of these microbial mats in the Lake Huron sinkholes (Biddanda et al 2015). Pigment levels (chlorophyll, phycoerythrin and phycocyanin) as well as photosynthetic yield were measured to understand the photophysiology of these microbial systems using both in situ and in vitro studies.…”