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  1. Abstract

    The biotic and abiotic controls on major shifts in atmospheric oxygen and the persistence of low-oxygen periods over a majority of Earth’s history remain under debate. Explanations of Earth’s stepwise pattern of oxygenation have mostly neglected the effect of changing diel illumination dynamics linked to daylength, which has increased through geological time due to Earth’s rotational deceleration caused by tidal friction. Here we used microsensor measurements and dynamic modelling of interfacial solute fluxes in cyanobacterial mats to investigate the effect of changing daylength on Precambrian benthic ecosystems. Simulated increases in daylength across Earth’s historical range boosted the diel benthic oxygen export, even when the gross photosynthetic production remained constant. This fundamental relationship between net productivity and daylength emerges from the interaction of diffusive mass transfer and diel illumination dynamics, and is amplified by metabolic regulation and microbial behaviour. We found that the resultant daylength-driven surplus organic carbon burial could have shaped the increase in atmospheric oxygen that occurred during the Great and Neoproterozoic Oxidation Events. Our suggested mechanism, which links the coinciding increases in daylength and atmospheric oxygen via enhanced net productivity, reveals a possible contribution of planetary mechanics to the evolution of Earth’s biology and geochemistry.

  2. Free, publicly-accessible full text available November 1, 2023
  3. Bernstein, Hans C. (Ed.)
    ABSTRACT Cyanobacterial mats profoundly influenced Earth’s biological and geochemical evolution and still play important ecological roles in the modern world. However, the biogeochemical functioning of cyanobacterial mats under persistent low-O 2 conditions, which dominated their evolutionary history, is not well understood. To investigate how different metabolic and biogeochemical functions are partitioned among community members, we conducted metagenomics and metatranscriptomics on cyanobacterial mats in the low-O 2 , sulfidic Middle Island sinkhole (MIS) in Lake Huron. Metagenomic assembly and binning yielded 144 draft metagenome assembled genomes, including 61 of medium quality or better, and the dominant cyanobacteria and numerous Proteobacteria involved in sulfur cycling. Strains of a Phormidium autumnale -like cyanobacterium dominated the metagenome and metatranscriptome. Transcripts for the photosynthetic reaction core genes psaA and psbA were abundant in both day and night. Multiple types of psbA genes were expressed from each cyanobacterium, and the dominant psbA transcripts were from an atypical microaerobic type of D1 protein from Phormidium . Further, cyanobacterial transcripts for photosystem I genes were more abundant than those for photosystem II, and two types of Phormidium sulfide quinone reductase were recovered, consistent with anoxygenic photosynthesis via photosystem I in the presence of sulfide. Transcripts indicate active sulfurmore »oxidation and reduction within the cyanobacterial mat, predominately by Gammaproteobacteria and Deltaproteobacteria , respectively. Overall, these genomic and transcriptomic results link specific microbial groups to metabolic processes that underpin primary production and biogeochemical cycling in a low-O 2 cyanobacterial mat and suggest mechanisms for tightly coupled cycling of oxygen and sulfur compounds in the mat ecosystem. IMPORTANCE Cyanobacterial mats are dense communities of microorganisms that contain photosynthetic cyanobacteria along with a host of other bacterial species that play important yet still poorly understood roles in this ecosystem. Although such cyanobacterial mats were critical agents of Earth’s biological and chemical evolution through geological time, little is known about how they function under the low-oxygen conditions that characterized most of their natural history. Here, we performed sequencing of the DNA and RNA of modern cyanobacterial mat communities under low-oxygen and sulfur-rich conditions from the Middle Island sinkhole in Lake Huron. The results reveal the organisms and metabolic pathways that are responsible for both oxygen-producing and non-oxygen-producing photosynthesis as well as interconversions of sulfur that likely shape how much O 2 is produced in such ecosystems. These findings indicate tight metabolic reactions between community members that help to explain the limited the amount of O 2 produced in cyanobacterial mat ecosystems.« less
  4. As we expand the search for life beyond Earth, a water-dominated planet, we turn our eyes to other aquatic worlds. Microbial life found in Earth’s many extreme habitats are considered useful analogs to life forms we are likely to find in extraterrestrial bodies of water. Modern-day benthic microbial mats inhabiting the low-oxygen, high-sulfur submerged sinkholes of temperate Lake Huron (Michigan, USA) and microbialites inhabiting the shallow, high-carbonate waters of subtropical Laguna Bacalar (Yucatan Peninsula, Mexico) serve as potential working models for exploration of extraterrestrial life. In Lake Huron, delicate mats comprising motile filaments of purple-pigmented cyanobacteria capable of oxygenic and anoxygenic photosynthesis and pigment-free chemosynthetic sulfur-oxidizing bacteria lie atop soft, organic-rich sediments. In Laguna Bacalar, lithification by cyanobacteria forms massive carbonate reef structures along the shoreline. Herein, we document studies of these two distinct earthly microbial mat ecosystems and ponder how similar or modified methods of study (e.g., robotics) would be applicable to prospective mat worlds in other planets and their moons (e.g., subsurface Mars and under-ice oceans of Europa). Further studies of modern-day microbial mat and microbialite ecosystems can add to the knowledge of Earth’s biodiversity and guide the search for life in extraterrestrial hydrospheres.
  5. Who’s cooking, who’s cleaning, and who’s got the remote control within the waters blanketing Earth? Anatomically tiny, numerically dominant microbes are the crucial “homemakers” of the watery household. Phytoplankton’s culinary abilities enable them to create food by absorbing sunlight to fix carbon and release oxygen, making microbial autotrophs top-chefs in the aquatic kitchen. However, they are not the only bioengineers that balance this complex household. Ubiquitous heterotrophic microbes including prokaryotic bacteria and archaea (both “bacteria” henceforth), eukaryotic protists, and viruses, recycle organic matter and make inorganic nutrients available to primary producers. Grazing protists compete with viruses for bacterial biomass, whereas mixotrophic protists produce new organic matter as well as consume microbial biomass. When viruses press remote-control buttons, by modifying host genomes or lysing them, the outcome can reverberate throughout the microbial community and beyond. Despite recognition of the vital role of microbes in biosphere housekeeping, impacts of anthropogenic stressors and climate change on their biodiversity, evolution, and ecological function remain poorly understood. How trillions of the smallest organisms in Earth’s largest ecosystem respond will be hugely consequential. By making the study of ecology personal, the “housekeeping” perspective can provide better insights into changing ecosystem structure and function at all scales.