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Ecological theories posit that heterogeneity in environmental conditions greatly affects community structure and function. However, the degree to which ecological theory developed using plant- and animal-dominated systems applies to microbiomes is unclear. Investigating the metabolic strategies found in microbiomes are particularly informative for testing the universality of ecological theories because microorganisms have far wider metabolic capacity than plants and animals. We used metagenomic analyses to explore the relationships between the energy and physicochemical gradients in Lake Fryxell and the metabolic capacity of its benthic microbiome. Statistical analysis of the relative abundance of metabolic marker genes and gene family diversity shows that oxygenic photosynthesis, carbon fixation, and flavin-based electron bifurcation differentiate mats growing in different environmental conditions. The pattern of gene family diversity points to the likely importance of temporal environmental heterogeneity in addition to resource gradients. Overall, we found that the environmental heterogeneity of photosynthetically active radiation (PAR) and oxygen concentration ([O2]) in Lake Fryxell provide the framework by which metabolic diversity and composition of the community is structured, in accordance with its phylogenetic structure. The organization of the resulting microbial ecosystems are consistent with the maximum power principle and the species sorting model., Competing Interests: The authors have declared that no competing interests exist.

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 as Leptolyngbya sp. BulkMat.35, Pseudanabaenaceae cyanobacterium MP8IB2.15, Microcoleus sp. MP8IB2.171, and Leptolyngbyaceae cyanobacterium MP9P1.79. 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 the Leptolyngbya sp. BulkMat.35 and Leptolyngbyaceae cyanobacterium MP9P1.79 contained kaiB3, a divergent homolog of kaiB.

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.

Closed cryoconite holes (CCHs) are small aquatic ecosystems enclosed in glacier surface ice, and they collectively contribute substantial aquatic habitat to inland Antarctica. We examined the morphology, geochemistry and bacterial diversity of 57 CCHs, spread over seven sites, located on five glaciers, covering a range of latitudes, elevations and distance from open seawater. Isotopes confirmed glacial ice as the initial water source, with water chemistry evolving through freeze concentration and photosynthetic processes to have conductivities ranging from <0.005 to >4 mS cm-1 and pH from <5 to >11. Nitrate concentrations were more elevated in inland, higher altitude sites. Bacterial communities were characterized by Automated Ribosomal Intergenic Spacer Analysis and high-throughput sequencing. The dominant phyla were Cyanobacteria, Bacteroides, Proteobacteria and Actinobacteria. CCH bacterial communities predominantly grouped by geographic location, suggesting initial wind-borne inocula from local and regional sources play a role in structuring assemblages. However, multivariate multiple regression analysis indicated that internal CCH conditions also influenced community structure, particularly the ion content and pH of the liquid water. This highlights the importance of founder bacterial populations, isolation and water chemistry in the evolution of CCH bacterial communities. [ABSTRACT FROM AUTHOR]

Photoautotrophic organisms face extreme conditions in the Polar Regions including permanently low temperatures, freezing, salinity and low nutrient. Certain microalgae and cyanobacteria are able to withstand these conditions and adaptation mechanisms associated with photophysiology play an important part in overcoming challenges created by variation in irradiance under low temperatures. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]

Cyanobacteria-dominated microbial mats in Lake Vanda grow with pinnacles and ridges separated by prostrate mat. Rocks protrude over microbial mats on the lake bottom to create localized, dm-scale gradients in sedimentation and irradiance. The effects of sedimentation on pinnacle and ridge growth were isolated from photosynthetic activity by contrasting growth across microenvironmental gradients. Sedimentation rate was measured as the mass of sand and mud sized sediment in mat that accumulated over 11 years, and the incident light was modeled near and under rocks by reconstructing topography using Structure from Motion techniques. Morphologically diverse pinnacles and ridges were documented in both exposed and sheltered mat microenvironments, in addition to growing downward from the underside of overhanging rocks. Mat that grew with > 40% irradiance under overhangs did not have consistent differences in pinnacle density or ridge abundance as a function of sedimentation rates or irradiance when compared to exposed mat. However, their morphology did change significantly with changes in the direction of incident irradiance. Where irradiance was < 40% ambient or light intersected the mat at very low angles, few pinnacles were present and ridges were preferentially aligned parallel to incident light direction. These observations indicate that pinnacle nucleation and spacing were not strongly influenced by sedimentation but pinnacle and ridge morphology varied in response to directional irradiance. [ABSTRACT FROM AUTHOR]

The evolution of oxygenic photosynthesis was the most important geochemical event in Earth history, causing the Great Oxidation Event (GOE) ~2.4 b.y. ago. However, evidence is mixed as to whether O2 production occurred locally as much as 2.8 b.y. ago, creating O2 oases, or initiated just prior to the GOE. The biogeochemical dynamics of possible O2 oases have been poorly constrained due to the absence of modern analogs. However, cyanobacteria in microbial mats in a perennially anoxic region of Lake Fryxell, Antarctica, create a 1-2 mm O2-containing layer in the upper mat during summer, providing the first known modern analog for formation of benthic O2 oases. In Lake Fryxell, benthic cyanobacteria are present below the oxycline in the lake. Mat photosynthesis rates were slow due to low photon flux rate (1-2 µmol m-2 s-1) under thick ice cover, but photosynthetic O2 production was sufficient to sustain up to 50 µmol O2 L-1, sandwiched between anoxic overlying water and anoxic sediments. We hypothesize that Archean cyanobacteria could have similarly created O2 oases in benthic mats prior to the GOE. Analogous mats may have been at least partly responsible for geological evidence of oxidative weathering prior to the GOE, and habitats such as Lake Fryxell provide natural laboratories where the impact of benthic O2 oases on biogeochemical signatures can be investigated. [ABSTRACT FROM AUTHOR]