Communities of T4-like bacteriophages associated with bacteria in Lake Baikal: diversity and biogeography

Lake Baikal phage communities are important for lake ecosystem functioning. Here we describe the diversity of T4-bacteriophage associated with the bacterial fraction of filtered water samples collected from the pelagic zone, coastal zone and shallow bays. Although the study of the diversity of phages for the g23 gene has been carried out at Lake Baikal for more than ten years, shallow bays that comprise a significant part of the lake’s area have been neglected, and this gene has not previously been studied in the bacterial fraction. Phage communities were probed using amplicon sequencing methods targeting the gene of major capsid protein (g23) and compared phylogenetically across sample locations and with sequences previously retrieved from non-bacterial fractions (<0.2 um) and biofilms (non-fractionated). In this study, we examined six water samples, in which 24 to 74 viral OTUs were obtained. The sequences from shallow bays largely differed from those in the pelagic and coastal samples and formed individual subcluster in the UPGMA tree that was obtained from the comparison of phylogenetic distances of g23 sequence sets from various ecosystems, reflecting differences in viral communities depending on the productivity of various sites of Lake Baikal. According to the RefSeq database, from 58.3 to 73% of sequences of each sample had cultivated closest relatives belonging to cyanophages. In this study, for phylogenetic analysis, we chose the closest relatives not only from the RefSeq and GenBank NR databases but also from two marine and one freshwater viromes: eutrophic Osaka Bay (Japan), oligotrophic area of the Pacific Ocean (Station ALOHA) and mesotrophic and ancient Lake Biwa (Japan), which allowed us to more fully compare the diversity of marine and freshwater phages. The identity with marine sequences at the amino acid level ranged from 35 to 80%, and with the sequences from the viral fraction and bacterial one from Lake Biwa—from 35.3 to 98% and from 33.9 to 89.1%, respectively. Therefore, the sequences from marine viromes had a greater difference than those from freshwater viromes, which may indicate a close relationship between freshwater viruses and differences from marine viruses.

Revealing the Viral Community in the Hadal Sediment of the New Britain Trench

Marine viruses are widely distributed and influence matter and energy transformation in ecosystems by modulating hosts’ metabolism. The hadal trenches represent the deepest marine habitat on Earth, for which the viral communities and related biogeochemical functions are least explored and poorly understood. Here, using the sediment samples (8720 m below sea level) collected from the New Britain Trench (NBT), we investigated the viral community, diversity, and genetic potentials in the hadal sediment habitat for the first time by deep shotgun metagenomic sequencing. We found the NBT sediment viral community was dominated by Siphoviridae, Myoviridae, Podoviridae, Mimiviridae, and Phycodnaviridae, which belong to the dsDNA viruses. However, the large majority of them remained uncharacterized. We found the hadal sediment virome had some common components by comparing the hadal sediment viruses with those of hadal aquatic habitats and those of bathypelagic and terrestrial habitats. It was also distinctive in community structure and had many novel viral clusters not associated with the other habitual virome included in our analyses. Further phylogenetic analysis on its Caudovirales showed novel diversities, including new clades specially evolved in the hadal sediment habitat. Annotation of the NBT sediment viruses indicated the viruses might influence microbial hydrocarbon biodegradation and carbon and sulfur cycling via metabolic augmentation through auxiliary metabolic genes (AMGs). Our study filled in the knowledge gaps on the virome of the hadal sediment habitats and provided insight into the evolution and the potential metabolic functions of the hadal sediment virome.

A Review of Marine Viruses in Coral Ecosystem

Coral reefs are among the most biodiverse biological systems on earth. Corals are classified as marine invertebrates and filter the surrounding food and other particles in seawater, including pathogens such as viruses. Viruses act as both pathogen and symbiont for metazoans. Marine viruses that are abundant in the ocean are mostly single-, double stranded DNA and single-, double stranded RNA viruses. These discoveries were made via advanced identification methods which have detected their presence in coral reef ecosystems including PCR analyses, metagenomic analyses, transcriptomic analyses and electron microscopy. This review discusses the discovery of viruses in the marine environment and their hosts, viral diversity in corals, presence of virus in corallivorous fish communities in reef ecosystems, detection methods, and occurrence of marine viral communities in marine sponges.

Viruses—Agents of Change in the Oceans

Viruses are usually thought of as the cause of countless diseases. However, in the oceans, viruses are part of the natural cycle of life and death. This article discusses marine viruses that infect phytoplankton—the tiny micro-algae that form the base of the marine food web and affect Earth’s climate. Through an ongoing “arms race” between viruses and the cells they infect, viruses can promote the evolution of their hosts, and even help their hosts acquire genes that can help them survive. By killing phytoplankton species that become very abundant, viruses can allow other species to grow, promoting biodiversity. Finally, viruses affect global cycles of carbon and other elements, indirectly influencing the climate of our planet.

Viruses infecting a warm water picoeukaryote shed light on spatial co-occurrence dynamics of marine viruses and their hosts

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.

Visualizing active viral infection reveals diverse cell fates in synchronized algal bloom demise

Marine viruses are the most abundant biological entity in the ocean and are considered as major evolutionary drivers of microbial life [C. A. Suttle, Nat. Rev. Microbiol. 5, 801–812 (2007)]. Yet, we lack quantitative approaches to assess their impact on the marine ecosystem. Here, we provide quantification of active viral infection in the bloom forming single-celled phytoplankton Emiliania huxleyi infected by the large virus EhV, using high-throughput single-molecule messenger RNA in situ hybridization (smFISH) of both virus and host transcripts. In natural samples, viral infection reached only 25% of the population despite synchronized bloom demise exposing the coexistence of infected and noninfected subpopulations. We prove that photosynthetically active cells chronically release viral particles through nonlytic infection and that viral-induced cell lysis can occur without viral release, thus challenging major assumptions regarding the life cycle of giant viruses. We could also assess active infection in cell aggregates linking viral infection and carbon export to the deep ocean [C. P. Laber et al., Nat. Microbiol. 3, 537–547 (2018)] and suggest a potential host defense strategy by enrichment of infected cells in sinking aggregates. Our approach can be applied to diverse marine microbial systems, opening a mechanistic dimension to the study of biotic interactions in the ocean.

A Place for Viruses on the Tree of Life

Viruses are ubiquitous. They infect almost every species and are probably the most abundant biological entities on the planet, yet they are excluded from the Tree of Life (ToL). However, there can be no doubt that viruses play a significant role in evolution, the force that facilitates all life on Earth. Conceptually, viruses are regarded by many as non-living entities that hijack living cells in order to propagate. A strict separation between living and non-living entities places viruses far from the ToL, but this may be theoretically unsound. Advances in sequencing technology and comparative genomics have expanded our understanding of the evolutionary relationships between viruses and cellular organisms. Genomic and metagenomic data have revealed that co-evolution between viral and cellular genomes involves frequent horizontal gene transfer and the occasional co-option of novel functions over evolutionary time. From the giant, ameba-infecting marine viruses to the tiny Porcine circovirus harboring only two genes, viruses and their cellular hosts are ecologically and evolutionarily intertwined. When deciding how, if, and where viruses should be placed on the ToL, we should remember that the Tree functions best as a model of biological evolution on Earth, and it is important that models themselves evolve with our increasing understanding of biological systems.

A thermal trade-off between viral production and degradation drives phytoplankton-virus population dynamics

Marine viruses interact with their microbial hosts in dynamic environments shaped by variations in abiotic factors, including temperature. However, the impacts of temperature on viral infection of phytoplankton are not well understood. Here we coupled mathematical modeling with experimental datasets to explore the effect of temperature on three Micromonas-prasinovirus pairs. Our model shows the negative consequences of high temperatures on infection and suggests a temperature-dependent threshold between viral production and degradation. Modeling long-term dynamics in environments with different average temperatures revealed the potential for long-term host-virus coexistence, epidemic free, or habitat loss states. Hence, we generalized our model to global sea surface temperature of present and future seas and show that climate change may influence virus-host dynamics differently depending on the virus-host pair. Our study suggests that temperature-dependent changes in the infectivity of virus particles may lead to shifts in virus-host habitats in warmer oceans, analogous to projected changes in the habitats of macro- and micro-organisms.

Visualizing active viral infection reveals diverse cell fates in synchronized algal bloom demise

SummaryMarine viruses are considered as major evolutionary and biogeochemical drivers of microbial life, through metabolic reprogramming of their host and cell lysis that modulates nutrient cycling1, primary production and carbon export in the oceans2. Despite the fact that viruses are the most abundant biological entities in the marine environment, we still lack mechanistic and quantitative approaches to assess their impact on the marine food webs. Here, we provide the first quantification of active viral infection, during bloom succession of the cosmopolitan coccolithophore Emiliania huxleyi, by subcellular visualization of both virus and host transcripts on a single cell resolution across thousands of cells. Using this novel method, that we coined Virocell-FISH, we revealed that distinct transcriptional states co-exist during the infection dynamics, and that viral infection reached only a quarter of the E. huxleyi population although the bloom demised in a synchronized manner. Through a detailed laboratory time-course infection of E. huxleyi by its lytic large virus EhV, we quantitatively show that metabolically active infected cells chronically release viral particles, and that viral-induced lysis is not systematically accompanied by virion increase, thus challenging major assumptions regarding the life cycle of giant lytic viruses. Using Virocell-FISH, we could further assess in a new resolution, the level of viral infection in cell aggregates, a key ecosystem process that can facilitate carbon export to the deep ocean3. We project that our approach can be applied to diverse marine microbial systems, opening a mechanistic dimension to the study of host-pathogen interactions in the ocean.One Sentence SummaryQuantifying active viral infection in algal blooms

A network-based integrated framework for predicting virus–prokaryote interactions

Metagenomic sequencing has greatly enhanced the discovery of viral genomic sequences; however, it remains challenging to identify the host(s) of these new viruses. We developed VirHostMatcher-Net, a flexible, network-based, Markov random field framework for predicting virus–prokaryote interactions using multiple, integrated features: CRISPR sequences and alignment-free similarity measures ($s_2^*$ and WIsH). Evaluation of this method on a benchmark set of 1462 known virus–prokaryote pairs yielded host prediction accuracy of 59% and 86% at the genus and phylum levels, representing 16–27% and 6–10% improvement, respectively, over previous single-feature prediction approaches. We applied our host prediction tool to crAssphage, a human gut phage, and two metagenomic virus datasets: marine viruses and viral contigs recovered from globally distributed, diverse habitats. Host predictions were frequently consistent with those of previous studies, but more importantly, this new tool made many more confident predictions than previous tools, up to nearly 3-fold more (n &gt; 27 000), greatly expanding the diversity of known virus–host interactions.