Cyanobacteria of the Synechococcus and Prochlorococcus genera are important contributors to photosynthetic productivity in the open oceans1-3. Here, using pre-existing metagenomic datasets from the global ocean sampling (GOS) expedition4 as well as from viral biomes5, we show the first evidence for the presence of photosystem I (PSI) genes in genomes of marine viruses that infect these marine cyanobacteria. Recently, core photosystem II (PSII) genes were identified in cyanophages; they were proposed to be functional in photosynthesis and in increasing viral fitness by supplementing the host production of these proteins6-9. The 7 cyanobacterial core PSI genes identified in this study, psaA, B, C, D, E, K and a unique J and F fusion, form a distinctive cluster in cyanophage genomes, suggestive of selection for a distinct function in virus life cycle. The existence of this PSI cluster was confirmed with overlapping and long PCR performed on environmental DNA from the Northern Line Islands. Potentially, the 7 proteins encoded by the viral genes are sufficient to form an intact monomeric PSI complex. Projection of viral predicted peptides on the cyanobacterial PSI crystal structure10 suggested that the viral-PSI components may provide a unique way of funneling reducing power from respiratory and other electron transfer chains to PSI.

Proteorhodopsins (PRs) are light-driven proton pumps that have been found in a variety of marine environments. The goal of this study was to search for PR presence in different freshwater and brackish environments and to explore the diversity of non-marine PR protein. Here, we show that PRs exist in distinctly different aquatic environments, ranging from clear water lakes to peat lakes and in the Baltic Sea. Some of the PRs observed in this study formed unique clades that were not previously observed in marine environments, whereas others were similar to PRs found in non-marine samples of the Global Ocean Sampling (GOS) expedition. Furthermore, the similarity of several PRs isolated from lakes in different parts of the world suggests that these genes are dispersed globally and that they may encode unique functional capabilities enabling successful competition in a wide range of freshwater environments. Phylogenomic analysis of genes found on these GOS scaffolds suggests that some of the freshwater PRs are found in freshwater Flavobacteria and freshwater SAR11-like bacteria.

The aerial surface of plants, the phyllosphere, is colonized by numerous bacteria displaying diverse metabolic properties that enable their survival in this specific habitat. Recently, we reported on the presence of microbial rhodopsin harbouring bacteria on the top of leaf surfaces. Here, we report on the presence of additional bacterial populations capable of harvesting light as a means of supplementing their metabolic requirements. An analysis of six phyllosphere metagenomes revealed the presence of a diverse community of anoxygenic phototrophic bacteria, including the previously reported methylobacteria, as well as other known and unknown phototrophs. The presence of anoxygenic phototrophic bacteria was also confirmed in situ by infrared epifluorescence microscopy. The microscopic enumeration correlated with estimates based on metagenomic analyses, confirming both the presence and high abundance of these microorganisms in the phyllosphere. Our data suggest that the phyllosphere contains a phylogenetically diverse assemblage of phototrophic species, including some yet undescribed bacterial clades that appear to be phyllosphere-unique.

Summary The above-ground surfaces of terrestrial plants, the phyllosphere, comprise the main interface between the terrestrial biosphere and solar radiation. It is estimated to host up to 1026 microbial cells that may intercept part of the photon flux impinging on the leaves. Based on 454-pyrosequencing-generated metagenome data, we report on the existence of diverse microbial rhodopsins in five distinct phyllospheres from tamarisk (Tamarix nilotica), soybean (Glycine max), Arabidopsis (Arabidopsis thaliana), clover (Trifolium repens) and rice (Oryza sativa). Our findings, for the first time describing microbial rhodopsins from non-aquatic habitats, point towards the potential coexistence of microbial rhodopsin-based phototrophy and plant chlorophyll-based photosynthesis, with the different pigments absorbing non-overlapping fractions of the light spectrum.