Search

The extent of oxygenated environments on the early Earth was much lower than today, and cyanobacteria were critical players in Earth's shift from widespread anoxia to oxygenated surface environments. Extant cyanobacteria that aggregate into cones, tufts and ridges are used to understand the long record of photosynthesis and microbe-mineral interactions during times when oxygen was much lower, i.e., the Archean and the Proterozoic. To better understand the metabolic versatility and physiological properties of these organisms, we examined publicly available genomes of cyanobacteria from modern terrestrial hydrothermal systems and a newly sequenced genome of a cyanobacterium isolated from conical and ridged microbialites that grow in occasionally sulfidic hydrothermal springs in Yellowstone National Park, USA. Phylogenomic analyses reveal that cyanobacteria from globally distributed terrestrial and shallow marine hydrothermal systems form a monophyletic clade within the Cyanobacteria phylum. Comparative genomics of this clade reveals the genetic capacity for oxygenic photosynthesis that uses photosystems I and II, and anoxygenic photosynthesis that uses a putative sulfide quinone reductase to oxidize sulfide and bypass photosystem II. Surprisingly large proportions of the newly sequenced genome from Yellowstone National Park are also dedicated to secondary metabolite production (15.1-15.6%), of which ∼6% can be attributed to antibiotic production and resistance genes. All this may be advantageous to benthic, mat-forming photosynthesizers that have to compete for light and nutrients in sporadically or permanently sulfidic environments, and may have also improved the tolerance of ancient counterparts of these cyanobacteria to sulfidic conditions in benthic communities that colonized the coastal margins in the Archean and the Proterozoic., (Copyright © 2019 Elsevier Inc. All rights reserved.)

Gas release in photic-zone microbialites can lead to preservable morphological biosignatures. Here, we investigate the formation and stability of oxygen-rich bubbles enmeshed by filamentous cyanobacteria. Sub-millimetric and millimetric bubbles can be stable for weeks and even months. During this time, lithifying organic-rich laminae surrounding the bubbles can preserve the shape of bubbles. Cm-scale unstable bubbles support the growth of centimetric tubular towers with distinctly laminated mineralized walls. In environments that enable high photosynthetic rates, only small stable bubbles will be enclosed by a dense microbial mesh, while in deep waters extensive microbial mesh will cover even larger photosynthetic bubbles, increasing their preservation potential. Stable photosynthetic bubbles may be preserved as sub-millimeter and millimeter-diameter features with nearly circular cross-sections in the crests of some Proterozoic conical stromatolites, while centrimetric tubes formed around unstable bubbles provide a model for the formation of tubular carbonate microbialites that are not markedly depleted in (13)C.

Conical stromatolites are thought to be robust indicators of the presence of photosynthetic and phototactic microbes in aquatic environments as early as 3.5 billion years ago. However, phototaxis alone cannot explain the ubiquity of disrupted, curled, and contorted laminae in the crests of many Mesoproterozoic, Paleoproterozoic, and some Archean conical stromatolites. Here, we demonstrate that cyanobacterial production of oxygen in the tips of modern conical aggregates creates contorted laminae and submillimeter-to-millimeter-scale enmeshed bubbles. Similarly sized fossil bubbles and contorted laminae may be present only in the crestal zones of some conical stromatolites 2.7 billion years old or younger. This implies not only that cyanobacteria built Proterozoic conical stromatolites but also that fossil bubbles may constrain the timing of the evolution of oxygenic photosynthesis.