Here we describe, the longest microbial time-series analyzed to date using high-resolution 16S rRNA tag pyrosequencing of samples taken monthly over 6 years at a temperate marine coastal site off Plymouth, UK. Data treatment effected the estimation of community richness over a 6-year period, whereby 8794 operational taxonomic units (OTUs) were identified using single-linkage preclustering and 21 130 OTUs were identified by denoising the data. The Alphaproteobacteria were the most abundant Class, and the most frequently recorded OTUs were members of the Rickettsiales (SAR 11) and Rhodobacteriales. This near-surface ocean bacterial community showed strong repeatable seasonal patterns, which were defined by winter peaks in diversity across all years. Environmental variables explained far more variation in seasonally predictable bacteria than did data on protists or metazoan biomass. Change in day length alone explains >65% of the variance in community diversity. The results suggested that seasonal changes in environmental variables are more important than trophic interactions. Interestingly, microbial association network analysis showed that correlations in abundance were stronger within bacterial taxa rather than between bacteria and eukaryotes, or between bacteria and environmental variables.

Whether a small cell, a small genome or a minimal set of chemical reactions with self-replicating properties, simplicity is beguiling. As Leonardo da Vinci reportedly said, ‘simplicity is the ultimate sophistication’. Two diverging views of simplicity have emerged in accounts of symbiotic and commensal bacteria and cosmopolitan free-living bacteria with small genomes. The small genomes of obligate insect endosymbionts have been attributed to genetic drift caused by small effective population sizes (N_e). In contrast, streamlining theory attributes small cells and genomes to selection for efficient use of nutrients in populations where N_e is large and nutrients limit growth. Regardless of the cause of genome reduction, lost coding potential eventually dictates loss of function. Consequences of reductive evolution in streamlined organisms include atypical patterns of prototrophy and the absence of common regulatory systems, which have been linked to difficulty in culturing these cells. Recent evidence from metagenomics suggests that streamlining is commonplace, may broadly explain the phenomenon of the uncultured microbial majority, and might also explain the highly interdependent (connected) behavior of many microbial ecosystems. Streamlining theory is belied by the observation that many successful bacteria are large cells with complex genomes. To fully appreciate streamlining, we must look to the life histories and adaptive strategies of cells, which impose minimum requirements for complexity that vary with niche.

We present an extension of the Minimum Information about any (x) Sequence (MIxS) standard for reporting sequences of uncultivated virus genomes. Minimum Information about an Uncultivated Virus Genome (MIUViG) standards were developed within the Genomic Standards Consortium framework and include virus origin, genome quality, genome annotation, taxonomic classification, biogeographic distribution and in silico host prediction. Community-wide adoption of MIUViG standards, which complement the Minimum Information about a Single Amplified Genome (MISAG) and Metagenome-Assembled Genome (MIMAG) standards for uncultivated bacteria and archaea, will improve the reporting of uncultivated virus genomes in public databases. In turn, this should enable more robust comparative studies and a systematic exploration of the global virosphere.

How microbial communities change over time in response to the environment is poorly understood. Previously a six-year time series of 16S rRNA V6 data from the Western English Channel demonstrated robust seasonal structure within the bacterial community, with diversity negatively correlated with day-length. Here we determine whether metagenomes and metatranscriptomes follow similar patterns. We generated 16S rRNA datasets, metagenomes (1.2 GB) and metatranscriptomes (157 MB) for eight additional time points sampled in 2008, representing three seasons (Winter, Spring, Summer) and including day and night samples. This is the first microbial ‘multi-omic’ study to combine 16S rRNA amplicon sequencing with metagenomic and metatranscriptomic profiling. Five main conclusions can be drawn from analysis of these data: 1) Archaea follow the same seasonal patterns as Bacteria, but show lower relative diversity; 2) Higher 16S rRNA diversity also reflects a higher diversity of transcripts; 3) Diversity is highest in winter and at night; 4) Community-level changes in 16S-based diversity and metagenomic profiles are better explained by seasonal patterns (with samples closest in time being most similar), while metatranscriptomic profiles are better explained by diel patterns and shifts in particular categories (i.e., functional groups) of genes; 5) Changes in key genes occur among seasons and between day and night (i.e., photosynthesis); but these samples contain large numbers of orphan genes without known homologues and it is these unknown gene sets that appear to contribute most towards defining the differences observed between times. Despite the huge diversity of these microbial communities, there are clear signs of predictable patterns and detectable stability over time. Renewed and intensified efforts are required to reveal fundamental deterministic patterns in the most complex microbial communities. Further, the presence of a substantial proportion of orphan sequences underscores the need to determine the gene products of sequences with currently unknown function.

Microbial communities living in the oceans are major drivers of global biogeochemical cycles. With nutrients limited across vast swathes of the ocean, marine microbes eke out a living under constant assault from predatory viruses. Viral concentrations exceed those of their bacterial prey by an order of magnitude in surface water, making these obligate parasites the most abundant biological entities in the ocean. Like the pirates of the 17th and 18th centuries that hounded ships plying major trade and exploration routes, viruses have evolved mechanisms to hijack microbial cells and repurpose their cargo and indeed the vessels themselves to maximise viral propagation. Phenotypic reconfiguration of the host is often achieved through Auxiliary Metabolic Genes – genes originally derived from host genomes but maintained and adapted in viral genomes to redirect energy and substrates towards viral synthesis. In this review, we critically evaluate the literature describing the mechanisms used by bacteriophages to reconfigure host metabolism and to plunder intracellular resources to optimise viral production. We also highlight the mechanisms used when, in challenging environments, a ‘batten down the hatches’ strategy supersedes that of ‘plunder and pillage’. Here, the infecting virus increases host fitness through phenotypic augmentation in order to ride out the metaphorical storm, with a concomitant impact on host substrate uptake and metabolism, and ultimately, their interactions with their wider microbial community. Thus, the traditional view of the virus-host relationship as predator and prey does not fully characterise the variety or significance of the interactions observed. Recent advances in viral metagenomics have provided a tantalising glimpse of novel mechanisms of viral metabolic reprogramming in global oceans. Incorporation of these new findings into global biogeochemical models requires experimental evidence from model systems and major improvements in our ability to accurately predict protein function from sequence data.