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The McMurdo Dry Valleys are a cold and arid environment with low biomass relative to most ice- free environments. The ice-covered lakes in the valleys, however, provide a refuge for diverse microbial communities where liquid water persists year-round. Within these lakes, benthic micro- bial assemblages form ornate structures in the absence of burrowing and grazing organisms. In Lake Vanda, the microbial communities create pinnacles with features including tip, web, and ridge ornaments and brown, green, purple, and beige pigmented zones. Bacterial 16S rRNA gene composition differed between lake depths for all sampled features. Within each depth, community composition correlated with the relative distance into the pinnacle and there were also some significant differences between assemblages in certain zones. The bacterial community composi- tion in the zones may reflect how they respond to environmental changes as the mat is buried, altering the internal light environment and affecting 16S rRNA gene assemblages across niches from the surface to the interior. 

ABSTRACT Photosynthetic Cyanobacteria and their descendants are the only known organisms capable of oxygenic photosynthesis. Their metabolism permanently changed the Earth’s surface and the evolutionary trajectory of life, but little is known about their evolutionary history. Genomes of the Gloeobacterales , an order of deeply divergent photosynthetic Cyanobacteria , may hold clues about the evolutionary process. However, there are only three published genomes within this order, and it is difficult to make broad inferences based on such little data. Here, I describe five species within the Gloeobacterales retrieved from publicly available databases and examine their photosynthetic gene content and the environments in which Gloeobacterales genomes and 16S rRNA gene sequences are found. The Gloeobacterales contain reduced photosystems and inhabit cold, wet-rock, and low-light environments. They are likely present in low abundances due to their low growth rate. Future searches for Gloeobacterales should target these environments, and samples should be deeply sequenced to capture the low-abundance taxa. Publicly available databases contain undescribed taxa within the Gloeobacterales . However, searching through all available data with current methods is computationally expensive. Therefore, new methods must be developed to search for these and other evolutionarily important taxa. Once identified, these novel photosynthetic Cyanobacteria will help illuminate the origin and evolution of oxygenic photosynthesis. IMPORTANCE Early branching photosynthetic Cyanobacteria such as the Gloeobacterales may provide clues into the evolutionary history of oxygenic photosynthesis, but there are few genomes or cultured taxa from this order. Five new metagenome-assembled genomes suggest that members of the Gloeobacterales all contain reduced photosystems and lack genes associated with thylakoids and circadian rhythms. Their distribution suggests that they may thrive in environments that are marginal for other species, including wet-rock and cold environments. These traits may aid in the discovery and cultivation of novel species in this clade. 

The evolution of oxygenic photosynthesis was one of the most transformative evolutionary events in Earth’s history, leading eventually to the oxygenation of Earth’s atmosphere and, consequently, the evolution of aerobic respiration. Previous work has shown that the terminal electron acceptors (complex IV) of aerobic respiration likely evolved after the evolution of oxygenic photosynthesis. However, complex I of the respiratory complex chain can be involved in anaerobic processes and, therefore, may have pre-dated the evolution of oxygenic photosynthesis. If so, aerobic respiration may have built upon respiratory chains that pre-date the rise of oxygen in Earth’s atmosphere. The Melainabacteria provide a unique opportunity to examine this hypothesis because they contain genes for aerobic respiration but likely diverged from the Cyanobacteria before the evolution of oxygenic photosynthesis. Here, we examine the phylogenies of translated complex I sequences from 44 recently published Melainabacteria metagenome assembled genomes and genomes from other Melainabacteria, Cyanobacteria, and other bacterial groups to examine the evolutionary history of complex I. We find that complex I appears to have been present in the common ancestor of Melainabacteria and Cyanobacteria, supporting the idea that aerobic respiration built upon respiratory chains that pre-date the evolution of oxygenic photosynthesis and the rise of oxygen. 

Clues to the evolutionary steps producing innovations in oxygenic photosynthesis may be preserved in the genomes of organisms phylogenetically placed between non-photosynthetic Vampirovibrionia (formerly Melainabacteria) and the thylakoid-containing Cyanobacteria. However, only two species with published genomes are known to occupy this phylogenetic space, both within the genus Gloeobacter. Here, we describe nearly complete, metagenome-assembled genomes (MAGs) of an uncultured organism phylogenetically placed near Gloeobacter, for which we propose the name Candidatus Aurora vandensis {Au’ro.ra. L. fem. n. aurora, the goddess of the dawn in Roman mythology; van.de’nsis. N.L. fem. adj. vandensis of Lake Vanda, Antarctica}. The MAG of A. vandensis contains homologs of most genes necessary for oxygenic photosynthesis including key reaction center proteins. Many accessory subunits associated with the photosystems in other species either are missing from the MAG or are poorly conserved. The MAG also lacks homologs of genes associated with the pigments phycocyanoerethrin, phycoeretherin and several structural parts of the phycobilisome. Additional characterization of this organism is expected to inform models of the evolution of oxygenic photosynthesis.