Cyanobacterial mats were critical in the evolution of Earth?s chemistry and biology. They have long been recognized as drivers of the ?great oxidation event? (GOE), and may have also perpetuated a prolonged period of intermediate redox state in the early Earth's time period call the Proterozoic. However, the types of cyanobacteria that could have mediated such geochemical transitions are poorly understood because whereas Proterozoic oceans were characterized by low oxygen, stratified and/or fluctuating redox conditions, oxygen is required by most modern cyanobacteria studied to date. Further, traditional tools used for study of microbial mats provide limited information regarding metabolic or physiological diversity of cyanobacteria. In this proposal, the PIs propose an exploratory project that will combine cutting-edge single-cell and community genome sequencing technologies with elemental and isotopic geochemistry to address questions focused on facultatively oxygenic/anoxygenic cyanobacteria dominating modern microbial mats that are excellent analogs of Proterozoic mat ecosystems. This EAGER proposal is motivated by two recent, disparate developments that together provide unique opportunities to investigate metabolically versatile cyanobacteria: (i) discovery of an easily accessible modern mat ecosystem in northern Lake Huron that is a novel analog of Proterozoic geochemistry and biology, and (ii) the advent of new genome sequencing technologies that enable unprecedented insights into uncultivated single cells as well as whole microbial communities.

Broader Impacts: Undergraduate students will conduct the primary research focused on physiology (GVSU) and geochemistry (UM) and a PhD student will lead the genomics effort (UM). The discovery-driven and exploratory nature of this project provides outstanding opportunities for translating research into educational opportunities and public outreach. The PIs will take advantage of video resources (underwater dive footage, microscopic cell separations), time-lapse photography of motility, and recent coverage on the Discovery Channel ( and local news stations to develop multi-media materials (?microbes in motion? and ?laser roundup? movies). These will be integrated into outreach activities at UM and GVSU, and geobiology exhibits at TBNMS?s Visitor Center.

Project Report

Today, we take our well-oxygenated world for granted. But free oxygen was anything but plentiful over the first half of Earth’s 4.5 billion year history. Around 3 billion years ago, cyanobacteria oxygenated Earth, transforming it from a planet that was largely free of O2 into a world with an O2-rich atmosphere and oceans that is habitable for life today. Despite the importance of cyanobacteria in the history of Earth and life, little is known about the cyanobacteria that thrived under the low-O2 conditions that characterized much of their evolutionary history. The goal of this project was to better understand low-O2 adapted cyanobacteria by studying an unusual modern environment that harbors such organisms - submerged sinkholes of northern Lake Huron. Here, brilliant purple cyanobacterial mats thrive in low- O2 groundwater emerging from sinkholes onto the lake floor and provide a readily accessible habitat for exploration. This project resulted in several key outcomes: First, in 8 field expeditions we were able to photographically map and hydrologically characterize the unique high-sulfate, low-oxygen ground water-fed cyanobacterial benthic communities in the Middle Island Sinkhole Second, we showed that sinkhole microbial mats dominated by cyanobacteria are not a net source of oxygen, and that their carbon economy is in near balance. This finding has important implications for understanding the role of cyanobacteria in the evolution of planetary redox chemistry; cyanobacterial mats, which are common in the geologic record, should not necessarily be considered as a source of O2. Third, our project showed that the source of the large amount of carbon-rich sediment buried underneath the cyanobacterial mats is water column phytoplankton and not the overlying cyanobacterial mats. This finding has important implications for the high carbon burial potential of sinkhole ecosystems and opens up new questions about whether the climbing motility of the cyanobacterial filaments have anything to do with the burial of phytoplankton carbon, and the eventual fate of the cyanobacterial mats themselves. Fourth, our work revealed evidence of rapid motility of cyanobacterial filaments (mm in minutes and cm in hours!) that are amongst some of the fastest known for prokaryotes. The ability for rapid horizontal as well as vertical phototaxis may provide them advantages for optimizing light use in variable and low-light sinkhole environments and also enable them to bury water column debris deposited on them into deeper anaerobic sedimentary layers facilitating their preservation. Fifth, our field measurements and experimental studies on sinkhole cyanobacterial photophysiology suggest they optimize their pigment for variable available sunlight by adjusting their photosynthetic efficiency. The ability to adapt rapidly to variable light conditions in submerged sinkholes should be of considerable survival value to these photosynthetically fueled ecosystems on the lake floor. Finally, we have now gathered several lines of evidence that suggest low-oxygen underwater sinkholes in Lake Huron are modern-day refugia for low diversity but functionally versatile microbial ecosystems that serve as analogs of life on early Earth. Collectively, our linked project activities of habitat characterizing, oxygen/carbon tracking, filament behavior/photophysiology studies and genome-sequencing techniques that we have developed will be useful for exploring these and other microbial communities on Earth for novel organisms, physiologies, biogeochemistry, genes and biochemicals that could help us better understand our planet’s past and present - and benefit humanity.

National Science Foundation (NSF)
Division of Earth Sciences (EAR)
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Enriqueta Barrera
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Grand Valley State University
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