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

Abstract

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.

Sedimentary pyrite sulfur isotope compositions preserve signatures of the surface microbial mat environment in sediments underlying low‐oxygen cyanobacterial mats

“…In July 2016, much of the sediment–water interface (SWI) of the Middle Island Sinkhole (MIS) was dominated with surface coverings that were similar to those described in previous studies (Biddanda et al, 2006, 2015; Kinsman‐Costello et al, 2017; Nold et al, 2010, 2013; Ruberg et al, 2008; Snider et al, 2017; Voorhies et al, 2012): purple mats, gray sediment lacking cohesive mat, and intermittently observed white patches. We chose to focus on the two most commonly observed surface coverings to study diurnal δ 34 S patterns in porewater sulfide in 2016: the purple mats and gray sediment with diffuse mat at the SWI (i.e., gray mats) as two common end‐member environments (Figure 2).…”

“…Density stratification inhibits mixing with the overlying water, resulting in low‐oxygen (~2–4 mg/L) waters overlying the sediment–water interface (SWI; Ruberg et al, 2008). Light penetration to the SWI supports a dynamic microbial mat ecosystem (Biddanda et al, 2006, 2015; Grim, 2019; Kinsman‐Costello et al, 2017; Nold et al, 2010; Snider et al, 2017; Voorhies et al, 2012, 2016).…”

Novel Large Sulfur Bacteria in the Metagenomes of Groundwater-Fed Chemosynthetic Microbial Mats in the Lake Huron Basin

“…We shotgun sequenced white microbial mat communities that are bathed in similar groundwater at two contrasting locations: the library fountain in the town of Alpena, Michigan ( Figure 1A ; Snider et al, 2017 ) and the Isolated Sinkhole, which is submerged at a water depth of 93 m in Lake Huron ( Figure 1B ; Biddanda et al, 2006 ). The emerging groundwater at these two sites is sourced from the same Silurian-Devonian aquifer and has similar conductivity and chemistry ( Biddanda et al, 2012 ).…”

“…Groundwater seeps in this area also occur in sinkholes on land and at the Alpena County Library fountain, where an artesian well draws groundwater from the same aquifers that feed the sinkholes ( Snider et al, 2017 ). The fountain consists of a lower basin that has brown cyanobacterial mats and an upper basin that has white chemosynthetic mats.…”

“…The fountain consists of a lower basin that has brown cyanobacterial mats and an upper basin that has white chemosynthetic mats. A complete description of the fountain site is provided in Snider et al (2017) . Major differences in microbial mat habitat between this site and the Isolated Sinkhole include the following: (i) the fountain is exposed to direct sunlight, (ii) groundwater at the fountain is in closer contact with atmospheric oxygen but does not interact with lake water as at Isolated Sinkhole, (iii) mats in the fountain have no underlying sediment as at Isolated Sinkhole, (iv) the rate of water flow at the fountain is higher than at the Isolated Sinkhole.…”