The origin of oxygenic photosynthesis in Cyanobacteria led to the rise of oxygen on Earth ~2.3 billion years ago, profoundly altering the course of evolution by facilitating the development of aerobic respiration and complex multicellular life. Here we report the genomes of 41 uncultured organisms related to the photosynthetic Cyanobacteria (class Oxyphotobacteria), including members of the class Melainabacteria and a new class of Cyanobacteria (class Sericytochromatia) that is basal to the Melainabacteria and Oxyphotobacteria. All members of the Melainabacteria and Sericytochromatia lack photosynthetic machinery, indicating that phototrophy was not an ancestral feature of the Cyanobacteria and that Oxyphotobacteria acquired the genes for photosynthesis relatively late in cyanobacterial evolution. We show that all three classes independently acquired aerobic respiratory complexes, supporting the hypothesis that aerobic respiration evolved after oxygenic photosynthesis.

Molecular surveys of aphotic habitats have indicated the presence of major uncultured lineages phylogenetically classified as members of the Cyanobacteria. One of these lineages has recently been proposed as a nonphotosynthetic sister phylum to the Cyanobacteria, the Melainabacteria, based on recovery of population genomes from human gut and groundwater samples. Here, we expand the phylogenomic representation of the Melainabacteria through sequencing of six diverse population genomes from gut and bioreactor samples supporting the inference that this lineage is nonphotosynthetic, but not the assertion that they are strictly fermentative. We propose that the Melainabacteria is a class within the phylogenetically defined Cyanobacteria based on robust monophyly and shared ancestral traits with photosynthetic representatives. Our findings are consistent with theories that photosynthesis occurred late in the Cyanobacteria and involved extensive lateral gene transfer and extends the recognized functionality of members of this phylum.

Crustose coralline algae (CCA) are key reef-building primary producers that are known to induce the metamorphosis and recruitment of many species of coral larvae. Reef biofilms (particularly microorganisms associated with CCA) are also important as settlement cues for a variety of marine invertebrates, including corals. If rising sea surface temperatures (SSTs) affect CCA and/or their associated biofilms, this may in turn affect recruitment on coral reefs. Herein, we report that the CCA Neogoniolithon fosliei, and its associated microbial communities do not tolerate SSTs of 32 °C, only 2–4 °C above the mean maximum annual SST. After 7 days at 32 °C, the CCA exhibited clear signs of stress, including bleaching, a reduction in maximum quantum yield (F_v/F_m) and a large shift in microbial community structure. This shift at 32 °C involved an increase in Bacteroidetes and a reduction in Alphaproteobacteria, including the loss of the primary strain (with high-sequence similarity to a described coral symbiont). A recovery in F_v/F_m was observed in CCA exposed to 31 °C following 7 days of recovery (at 27 °C); however, CCA exposed to 32 °C did not recover during this time as evidenced by the rapid growth of endolithic green algae. A 50% reduction in the ability of N. fosliei to induce coral larval metamorphosis at 32 °C accompanied the changes in microbiology, pigmentation and photophysiology of the CCA. This is the first experimental evidence to demonstrate how thermal stress influences microbial associations on CCA with subsequent downstream impacts on coral recruitment, which is critical for reef regeneration and recovery from climate-related mortality events.

The classification of life forms into a hierarchical system (taxonomy) and the application of names to this hierarchy (nomenclature) is at a turning point in microbiology. The unprecedented availability of genome sequences means that a taxonomy can be built upon a comprehensive evolutionary framework, a longstanding goal of taxonomists. However, there is resistance to adopting a single framework to preserve taxonomic freedom, and ever increasing numbers of genomes derived from uncultured prokaryotes threaten to overwhelm current nomenclatural practices, which are based on characterised isolates. The challenge ahead then is to reach a consensus on the taxonomic framework and to adapt and scale the existing nomenclatural code, or create a new code, to systematically incorporate uncultured taxa into the chosen framework.

Coral reefs provide habitat for an array of marine invertebrates that host symbiotic microbiomes. Photosynthetic symbionts including Symbiodinium dinoflagellates and diatoms potentially influence the diversity of their host-associated microbiomes by releasing carbon-containing photosynthates and other organic compounds that fuel microbial metabolism. Here we used 16S ribosomal RNA (rRNA) gene amplicon pyrosequencing to characterise the microbiomes of 11 common Great Barrier Reef marine invertebrate species that host photosynthetic symbionts and five taxa in which they are absent. The presence of photosynthetic symbionts influenced the composition but not the species richness, evenness and phylogenetic diversity of invertebrate-associated microbiomes. Invertebrates without photosynthetic symbionts were dominated by Alphaproteobacteria, whereas those hosting photosynthetic symbionts were dominated by Gammaproteobacteria. Interestingly, many microbial species from photosymbiont-bearing invertebrates, including Oceanospirillales spp., Alteromonas spp., Pseudomonas spp., Halomonas spp., are implicated in the metabolism of dimethylsulfoniopropionate (DMSP). DMSP is produced in high concentrations by photosynthetic dinoflagellates and is involved in climate regulation by facilitating cloud formation. Microbiomes correlated with host taxa and replicate individuals from most sampled species grouped in distance-based redundancy analysis of retrieved 16S rRNA gene sequences. This study highlights the complex nature of invertebrate holobionts and confirms the importance of photosynthetic symbionts in structuring marine invertebrate bacterial communities.

Summary: Biotic communities and ecosystem dynamics in terrestrial Antarctica are limited by an array of extreme conditions including low temperatures, moisture and organic matter availability, high salinity, and a paucity of biodiversity to facilitate key ecological processes. Recent studies have discovered that the prokaryotic communities in these extreme systems are highly diverse with patchy distributions. Investigating the physical and biological controls over the distribution and activity of microbial biodiversity in Victoria Land is essential to understanding ecological functioning in this region. Currently, little information on the distribution, structure and activity of soil communities anywhere in Victoria Land are available, and their sensitivity to potential climate change remains largely unknown. We investigated soil microbial communities from low‐ and high‐productivity habitats in an isolated Antarctic location to determine how the soil environment impacts microbial community composition and structure. The microbial communities in Luther Vale, Northern Victoria Land were analysed using bacterial 16S rRNA gene clone libraries and were related to soil geochemical parameters and classical morphological analysis of soil metazoan invertebrate communities. A total of 323 16S rRNA gene sequences analysed from four soils spanning a productivity gradient indicated a high diversity (Shannon–Weaver values > 3) of phylotypes within the clone libraries and distinct differences in community structure between the two soil productivity habitats linked to water and nutrient availability. In particular, members of the Deinococcus / Thermus lineage were found exclusively in the drier, low‐productivity soils, while Gammaproteobacteria of the genus Xanthomonas were found exclusively in high‐productivity soils. However, rarefaction curves indicated that these microbial habitats remain under‐sampled. Our results add to the recent literature suggesting that there is a higher biodiversity within Antarctic soils than previously expected.