ALBERT

Description: Bacterial viruses (phages) are amongst the smallest, most powerful biological entities on Earth. Through infection, phages impact host metabolism, bacterial mortality, and evolution. In the oceans, 20–40% of surface microbes are infected, with 1023 new infections each second. Yet, infections remain virtually uncharacterized, as the available phage isolates underrepresent the diversity of marine phage–host interactions. Additionally, while sequencing efforts reveal “who is there?”, a gap between sequence and function prevents answering “what are they doing?” and “how?”. We have developed new Bacteroidetes and Proteobacteria marine phage–host model systems with which to connect genomes, infection strategies, and functions using both traditional and genome-wide “-omics” experiments. We ask: How do infections by genomically divergent phages compare? Are there links between phage–host genomes and infection strategies? Our findings are as follows. In Bacteroidetes, a phage infecting two nearly identical strains (host38 and host18) under identical conditions is more fit and efficient on host38. By contrast, on host18, it is less fit and, except for phage transcription, it fails at efficiently mastering all stages of the infection: from adsorption through to cell lysis. In Proteobacteria, genomically unrelated podovirus and siphovirus phages infecting the same strain reprogram host metabolisms very differently. Namely, siphovirus-infected cells hardly differ from uninfected and mainly repress energy-consuming processes such as motility and translation. By contrast, podovirus-infected cells greatly differ from uninfected cells in transcription and in uniquely shifting central carbon and energy metabolism. Additionally, the siphovirus is more complementary to the host than the podovirus in %GC, amino acids, and codon usage. We found that phage–host genome complementarity may drive the resource demand and fitness of a phage: the phage most complementary to its host easily accesses intracellular resources, infects with little reprogramming, and accomplishes the largest fitness, which has not previously been shown. Together, this work helps to uncover infection efficiency strategies, and connect genomes with metabolisms in marine phage–host systems.

Description: Ecosystems are controlled by 'bottom-up' (resources) and 'top-down' (predation) forces. Viral infection is now recognized as a ubiquitous top-down control of microbial growth across ecosystems but, at the same time, cell death byviral predation influences, and is influenced by, resource availability. In this Review, we discuss recent advances in understanding the biogeochemical impact of viruses, focusing on how metabolic reprogramming of host cells during lytic viral infection alters the flow of energy and nutrients in aquatic ecosystems. Our synthesis revealed several emerging themes. First, viral infection transforms host metabolism, in part through virus-encoded metabolic genes; the functions performed by these genes appear to alleviate energetic and biosynthetic bottlenecks to viral production. Second, viral infection depends on the physiological state of the host cell and on environmental conditions, which are challenging to replicate in the laboratory. Last, metabolic reprogramming of infected cells and viral lysis alter nutrient cycling and carbon export in the oceans, although the net impacts remain uncertain. This Review highlights the need for understanding viral infection dynamics in realistic physiological and environmental contexts to better predict their biogeochemical consequences.

Description: The marine picoeukaryote Bathycoccus prasinos has been considered a cosmopolitan alga, although recent studies indicate two ecotypes exist, Clade BI (B. prasinos) and Clade BII. Viruses that infect Bathycoccus Clade BI are known (BpVs), but not that infect BII. We isolated three dsDNA prasinoviruses from the Sargasso Sea against Clade BII isolate RCC716. The BII-Vs do not infect BI, and two (BII-V2 and BII-V3) have larger genomes (~210 kb) than BI-Viruses and BII-V1. BII-Vs share ~90% of their proteins, and between 65% to 83% of their proteins with sequenced BpVs. Phylogenomic reconstructions and PolB analyses establish close-relatedness of BII-V2 and BII-V3, yet BII-V2 has 10-fold higher infectivity and induces greater mortality on host isolate RCC716. BII-V1 is more distant, has a shorter latent period, and infects both available BII isolates, RCC716 and RCC715, while BII-V2 and BII-V3 do not exhibit productive infection of the latter in our experiments. Global metagenome analyses show Clade BI and BII algal relative abundances correlate positively with their respective viruses. The distributions delineate BI/BpVs as occupying lower temperature mesotrophic and coastal systems, whereas BII/BII-Vs occupy warmer temperature, higher salinity ecosystems. Accordingly, with molecular diagnostic support, we name Clade BII Bathycoccus calidus sp. nov. and propose that molecular diversity within this new species likely connects to the differentiated host-virus dynamics observed in our time course experiments. Overall, the tightly linked biogeography of Bathycoccus host and virus clades observed herein supports species-level host specificity, with strain-level variations in infection parameters.