Comparative metagenomic analyses reveal viral-induced shifts of host metabolism towards nucleotide biosynthesis

BACKGROUND: Viral genomes often contain metabolic genes that were acquired from host genomes (auxiliary genes). It is assumed that these genes are fixed in viral genomes as a result of a selective force, favoring viruses that acquire specific metabolic functions. While many individual auxiliary genes were observed in viral genomes and metagenomes, there is great importance in investigating the abundance of auxiliary genes and metabolic functions in the marine environment towards a better understanding of their role in promoting viral reproduction. RESULTS: In this study, we searched for enriched viral auxiliary genes and mapped them to metabolic pathways. To initially identify enriched auxiliary genes, we analyzed metagenomic microbial reads from the Global Ocean Survey (GOS) dataset that were characterized as viral, as well as marine virome and microbiome datasets from the Line Islands. Viral-enriched genes were mapped to a “global metabolism network” that comprises all KEGG metabolic pathways. Our analysis of the viral-enriched pathways revealed that purine and pyrimidine metabolism pathways are among the most enriched pathways. Moreover, many other viral-enriched metabolic pathways were found to be closely associated with the purine and pyrimidine metabolism pathways. Furthermore, we observed that sequential reactions are promoted in pathways having a high proportion of enriched genes. In addition, these enriched genes were found to be of modular nature, participating in several pathways. CONCLUSIONS: Our naïve metagenomic analyses strongly support the well-established notion that viral auxiliary genes promote viral replication via both degradation of host DNA and RNA as well as a shift of the host metabolism towards nucleotide biosynthesis, clearly indicating that comparative metagenomics can be used to understand different environments and systems without prior knowledge of pathways involved

Seasonal and diel patterns of abundance and activity of viruses in the Red Sea

Virus–microbe interactions have been studied in great molecular details for many years in cultured model systems, yielding a plethora of knowledge on how viruses use and manipulate host machinery. Since the advent of molecular techniques and high-throughput sequencing, methods such as cooccurrence, nucleotide composition, and other statistical frameworks have been widely used to infer virus–microbe interactions, overcoming the limitations of culturing methods. However, their accuracy and relevance is still debatable as cooccurrence does not necessarily mean interaction. Here we introduce an ecological perspective of marine viral communities and potential interaction with their hosts, using analyses that make no prior assumptions on specific virus–host pairs. By size fractionating water samples into free viruses and microbes (i.e., also viruses inside or attached to their hosts) and looking at how viral group abundance changes over time along both fractions, we show that the viral community is undergoing a change in rank abundance across seasons, suggesting a seasonal succession of viruses in the Red Sea. We use abundance patterns in the different size fractions to classify viral clusters, indicating potential diverse interactions with their hosts and potential differences in life history traits between major viral groups. Finally, we show hourly resolved variations of intracellular abundance of similar viral groups, which might indicate differences in their infection cycles or metabolic capacities

A novel uncultured marine cyanophage lineage with lysogenic potential linked to a putative marine Synechococcus 'relic' prophage

Marine cyanobacteria are important contributors to primary production in the ocean and their viruses (cyanophages) affect the ocean microbial communities. Despite reports of lysogeny in marine cyanobacteria, a genome sequence of such temperate cyanophages remains unknown although genomic analysis indicate potential for lysogeny in certain marine cyanophages. Using assemblies from Red Sea and Tara Oceans metagenomes, we recovered genomes of a novel uncultured marine cyanophage lineage, which contain, in addition to common cyanophage genes, a phycobilisome degradation protein NblA, an integrase and a split DNA polymerase. The DNA polymerase forms a monophyletic clade with a DNA polymerase from a genomic island in Synechococcus WH8016. The island contains a relic prophage that does not resemble any previously reported cyanophage but shares several genes with the newly identified cyanophages reported here. Metagenomic recruitment indicates that the novel cyanophages are widespread, albeit at low abundance. Here, we describe a novel potentially lysogenic cyanophage family, their abundance and distribution in the marine environment

New Insights into Metabolic Properties of Marine Bacteria Encoding Proteorhodopsins

Proteorhodopsin phototrophy was recently discovered in oceanic surface waters. In an effort to characterize uncultured proteorhodopsin-exploiting bacteria, large-insert bacterial artificial chromosome (BAC) libraries from the Mediterranean Sea and Red Sea were analyzed. Fifty-five BACs carried diverse proteorhodopsin genes, and we confirmed the function of five. We calculate that proteorhodopsin-exploiting bacteria account for 13% of microorganisms in the photic zone. We further show that some proteorhodopsin-containing bacteria possess a retinal biosynthetic pathway and a reverse sulfite reductase operon, employed by prokaryotes oxidizing sulfur compounds. Thus, these novel phototrophs are an unexpectedly large and metabolically diverse component of the marine microbial surface water

Novel Primers Reveal Wider Diversity among Marine Aerobic Anoxygenic Phototrophs

Aerobic anoxygenic phototrophic bacteria (AAnPs) were previously proposed to account for up to 11% of marine bacterioplankton and to potentially have great ecological importance in the world's oceans. Our data show that previously used primers based on the M subunit of anoxygenic photosynthetic reaction center genes (pufM) do not comprehensively identify the diversity of AAnPs in the ocean. We have designed and tested a new set of pufM-specific primers and revealed several new AAnP variants in environmental DNA samples and genomic libraries