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ABSTRACT The evolution of oxygenic photosynthesis in the Cyanobacteria was one of the most transformative events in Earth history, eventually leading to the oxygenation of Earth’s atmosphere. However, it is difficult to understand how the earliest Cyanobacteria functioned or evolved on early Earth in part because we do not understand their ecology, including the environments in which they lived. Here, we use a cutting-edge bioinformatics tool to survey nearly 500,000 metagenomes for relatives of the taxa that likely bookended the evolution of oxygenic photosynthesis to identify the modern environments in which these organisms live. Ancestral state reconstruction suggests that the common ancestors of these organisms lived in terrestrial (soil and/or freshwater) environments. This restricted distribution may have increased the lag between the evolution of oxygenic photosynthesis and the oxygenation of Earth’s atmosphere.IMPORTANCECyanobacteria generate oxygen as part of their metabolism and are responsible for the rise of oxygen in Earth’s atmosphere over two billion years ago. However, we do not know how long this process may have taken. To help constrain how long this process would have taken, it is necessary to understand where the earliest Cyanobacteria may have lived. Here, we use a cutting-edge bioinformatics tool called branch water to examine the environments where modern Cyanobacteria and their relatives live to constrain those inhabited by the earliest Cyanobacteria. We find that these species likely lived in non-marine environments. This indicates that the rise of oxygen may have taken longer than previously believed. 

ABSTRACT We recovered 57 bacterial metagenome-assembled genomes (MAGs) from benthic microbial mat pinnacles from Lake Vanda, Antarctica. These MAGs provide access to genomes from polar environments and can assist in culturing and utilizing these Antarctic bacteria. 

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. 

Cyanobacteria form diverse communities and are important primary producers in Antarctic freshwater environments, but their geographic distribution patterns in Antarctica and globally are still unresolved. There are however few genomes of cultured cyanobacteria from Antarctica available and therefore metagenome-assembled genomes (MAGs) from Antarctic cyanobacteria microbial mats provide an opportunity to explore distribution of uncultured taxa. These MAGs also allow comparison with metagenomes of cyanobacteria enriched communities from a range of habitats, geographic locations, and climates. However, most MAGs do not contain 16S rRNA gene sequences, making a 16S rRNA gene-based biogeography comparison difficult. An alternative technique is to use large-scale k-mer searching to find genomes of interest in public metagenomes. This paper presents the results of k-mer based searches for 5 Antarctic cyanobacteria MAGs from Lake Fryxell and Lake Vanda, assigned the namesPhormidium pseudopriestleyiFRX01,Microcoleussp. MP8IB2.171,Leptolyngbyasp. BulkMat.35,Pseudanabaenaceae cyanobacteriumMP8IB2.15, andLeptolyngbyaceae cyanobacteriumMP9P1.79 in 498,942 unassembled metagenomes from the National Center for Biotechnology Information (NCBI) Sequence Read Archive (SRA). TheMicrocoleussp. MP8IB2.171 MAG was found in a wide variety of environments, theP. pseudopriestleyiMAG was found in environments with challenging conditions, theLeptolyngbyaceae cyanobacteriumMP9P1.79 MAG was only found in Antarctica, and theLeptolyngbyasp. BulkMat.35 andPseudanabaenaceae cyanobacteriumMP8IB2.15 MAGs were found in Antarctic and other cold environments. The findings based on metagenome matches and global comparisons suggest that these Antarctic cyanobacteria have distinct distribution patterns ranging from locally restricted to global distribution across the cold biosphere and other climatic zones. 

Cyanobacteria in polar environments face environmental challenges, including cold temperatures and extreme light seasonality with small diurnal variation, which has implications for polar circadian clocks. However, polar cyanobacteria remain underrepresented in available genomic data, and there are limited opportunities to study their genetic adaptations to these challenges. This paper presents four new Antarctic cyanobacteria metagenome-assembled genomes (MAGs) from microbial mats in Lake Vanda in the McMurdo Dry Valleys in Antarctica. The four MAGs were classified asLeptolyngbyasp. BulkMat.35,Pseudanabaenaceae cyanobacteriumMP8IB2.15,Microcoleussp. MP8IB2.171, andLeptolyngbyaceae cyanobacteriumMP9P1.79. The MAGs contain 2.76 Mbp – 6.07 Mbp, and the bin completion ranges from 74.2–92.57%. Furthermore, the four cyanobacteria MAGs have average nucleotide identities (ANIs) under 90% with each other and under 77% with six existing polar cyanobacteria MAGs and genomes. This suggests that they are novel cyanobacteria and demonstrates that polar cyanobacteria genomes are underrepresented in reference databases and there is continued need for genome sequencing of polar cyanobacteria. Analyses of the four novel and six existing polar cyanobacteria MAGs and genomes demonstrate they have genes coding for various cold tolerance mechanisms and most standard circadian rhythm genes with theLeptolyngbyasp. BulkMat.35 andLeptolyngbyaceae cyanobacteriumMP9P1.79 containedkaiB3, a divergent homolog ofkaiB. 

ABSTRACT The evolution of oxygenic photosynthesis in Cyanobacteria was a transformative event in Earth's history. However, the scientific community disagrees over the duration of the delay between the origin of oxygenic photosynthesis and oxygenation of Earth's atmosphere, with estimates ranging from less than a hundred thousand to more than a billion years, depending on assumptions about rates of oxygen production and fluxes of reductants. Here, we propose a novel ecological hypothesis that a geologically significant delay could have been caused by biomolecular inefficiencies within proto‐Cyanobacteria—ancestors of modern Cyanobacteria—that limited their maximum rates of oxygen production. Consideration of evolutionary processes and genomic data suggest to us that proto‐cyanobacterial primary productivity was initially limited by photosystem instability, oxidative damage, and photoinhibition rather than nutrients or ecological competition. We propose that during the Archean era, cyanobacterial photosystems experienced protracted evolution, with biomolecular inefficiencies initially limiting primary productivity and oxygen production. Natural selection led to increases in efficiency and thus primary productivity through time. Eventually, evolutionary advances produced sufficient biomolecular efficiency that environmental factors, such as nutrient availability, limited primary productivity and shifted controls on oxygen production from physiological to environmental limitations. If correct, our novel hypothesis predicts a geologically significant interval of time between the first local oxygen production and sufficient production for oxygenation of environments. It also predicts that evolutionary rates were likely highly variable due to strong environmental selection pressures and potentially high mutation rates but low competitive interactions. 

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. 

Sulfide inhibits oxygenic photosynthesis by blocking electron transfer between H2O and the oxygen-evolving complex in the D1 protein of Photosystem II. The ability of cyanobacteria to counter this effect has implications for understanding the productivity of benthic microbial mats in sulfidic environments throughout Earth history. In Lake Fryxell, Antarctica, the benthic, filamentous cyanobacterium Phormidium pseudopriestleyi creates a 1–2 mm thick layer of 50 µmol L−1 O2 in otherwise sulfidic water, demonstrating that it sustains oxygenic photosynthesis in the presence of sulfide. A metagenome-assembled genome of P. pseudopriestleyi indicates a genetic capacity for oxygenic photosynthesis, including multiple copies of psbA (encoding the D1 protein of Photosystem II), and anoxygenic photosynthesis with a copy of sqr (encoding the sulfide quinone reductase protein that oxidizes sulfide). The genomic content of P. pseudopriestleyi is consistent with sulfide tolerance mechanisms including increasing psbA expression or directly oxidizing sulfide with sulfide quinone reductase. However, the ability of the organism to reduce Photosystem I via sulfide quinone reductase while Photosystem II is sulfide-inhibited, thereby performing anoxygenic photosynthesis in the presence of sulfide, has yet to be demonstrated. 

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.