Viruses numerically dominate our oceans; however, we have only just begun to document the diversity, host range and infection dynamics of marine viruses, as well as the subsequent effects of infection on both host cell metabolism and oceanic biogeochemistry. Bacteriophages (that is, phages: viruses that infect bacteria) are highly abundant and are known to play critical roles in bacterial mortality, biogeochemical cycling and horizontal gene transfer. This Review Article summarizes current knowledge of marine viral ecology and highlights the importance of phage particles to the dissolved organic matter pool, as well as the complex interactions between phages and their bacterial hosts. We emphasize the newly recognized roles of phages as puppet masters of their bacterial hosts, where phages are capable of altering the metabolism of infected bacteria through the expression of auxiliary metabolic genes and the redirection of host gene expression patterns. Finally, we propose the 'royal family model' as a hypothesis to describe successional patterns of bacteria and phages over time in marine systems, where despite high richness and significant seasonal differences, only a small number of phages appear to continually dominate a given marine ecosystem. Although further testing is required, this model provides a framework for assessing the specificity and ecological consequences of phage-host dynamics.

https://par.nsf.gov/servlets/purl/10083670

Phage Puppet Masters of the Marine Microbial Realm

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 by viral 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. In this Review, Coleman and colleagues discuss recent advances in understanding the biogeochemical impact of viruses, focusing on how metabolic reprogramming of host cells during viral infection alters the flow of energy and nutrients in aquatic ecosystems.

Metabolic and biogeochemical consequences of viral infection in aquatic ecosystems.

A planetary-scale understanding of the ocean ecosystem, particularly in light of climate change, is crucial. Here, we review the work of Tara Oceans, an international, multidisciplinary project to assess the complexity of ocean life across comprehensive taxonomic and spatial scales. Using a modified sailing boat, the team sampled plankton at 210 globally distributed sites at depths down to 1,000 m. We describe publicly available resources of molecular, morphological and environmental data, and discuss how an ecosystems biology approach has expanded our understanding of plankton diversity and ecology in the ocean as a planetary, interconnected ecosystem. These efforts illustrate how global-scale concepts and data can help to integrate biological complexity into models and serve as a baseline for assessing ecosystem changes and the future habitability of our planet in the Anthropocene epoch. The schooner Tara sailed 140,000 km across the global oceans to sample diverse marine ecosystems and plankton communities. In the Review, members of the Tara Oceans project highlight how resulting data can be used for an integrated understanding of ocean biology.

Tara Oceans: towards global ocean ecosystems biology.

Since the development of methods to quantify transparent exopolymer particles (TEP) 1993, it has been shown that these gel-particles are not only ubiquitous and abundant, but also play a significant role in the biogeochemical cycling of elements and the structuring of food webs. TEP may be quantified either microscopically or colorimetrically. Although data based on measurements using one or other of these methods are not directly comparable, the results are consistent. TEP abundances in fresh and marine waters are in the same range as those of phytoplankton, with peak values occurring during phytoplankton blooms. TEP are very sticky particles that exhibit the characteristics of gels, and consist predominantly of acidic polysaccharides. In marine systems the majority of TEP are formed abiotically from dissolved precursors, which are released by phytoplankton that are either actively growing or are senescent. TEP are also generated during the sloughing of cell surface mucus and the disintegration of colonial matrices. The impact of exopolymers in the creation of microhabitats and in the cycling of trace compounds varies with the state in which the polymers occur, either as particles or as solute slimes. As particles, TEP provide surfaces for the colonization by bacteria and transfer by adsorption, trace solute substances into the particulate pool. As dissolved polymers they are mixed with the water and can neither be filtered nor aggregated. Because of their high abundances, large size and high stickiness, TEP enhance or even facilitate the aggregation of solid, non-sticky particles. They have been found to form the matrices of all marine aggregates investigated to date. By aggregating solid particles, TEP promote the sedimentation of particles, and, because their carbon content is high, their direct contribution to fluxes of carbon into deep water is significant. The direct sedimentation of TEP may represent a mechanism for the selective sequestration of carbon in deep water, because the C:N ratios of TEP lie well above the Redfield ratio. The turnover time of TEP as a result of bacterial degradation appears to range from hours to months, depending on the chemical composition and age of TEP. TEP may also be utilized not only by filter feeders (some protozoans and appendicularian) but TEP-rich microaggregates, consisting of pico- and nano-plankton are also readily grazed by euphausiids, thus permitting the uptake of particles that would otherwise be too small to be grazed directly by euphausiids. This short-circuits food chains and links the microbial food-web to the classical food-web. It is suggested that this expansion of the concept of food webs, linking the microbial loop with an aggregation web will provide a more complete description of particle dynamics. (C) 2002 Elsevier Science Ltd. All rights reserved.

Transparent exopolymer particles (TEP) in aquatic environments

Giant viruses are remarkable for their large genomes, often rivaling those of small bacteria, and for having genes thought exclusive to cellular life. Most isolated to date infect nonmarine protists, leaving their strategies and prevalence in marine environments largely unknown. Using eukaryotic single-cell metagenomics in the Pacific, we discovered a Mimiviridae lineage of giant viruses, which infects choanoflagellates, widespread protistan predators related to metazoans. The ChoanoVirus genomes are the largest yet from pelagic ecosystems, with 442 of 862 predicted proteins lacking known homologs. They are enriched in enzymes for modifying organic compounds, including degradation of chitin, an abundant polysaccharide in oceans, and they encode 3 divergent type-1 rhodopsins (VirR) with distinct evolutionary histories from those that capture sunlight in cellular organisms. One (VirRDTS) is similar to the only other putative rhodopsin from a virus (PgV) with a known host (a marine alga). Unlike the algal virus, ChoanoViruses encode the entire pigment biosynthesis pathway and cleavage enzyme for producing the required chromophore, retinal. We demonstrate that the rhodopsin shared by ChoanoViruses and PgV binds retinal and pumps protons. Moreover, our 1.65-A resolved VirRDTS crystal structure and mutational analyses exposed differences from previously characterized type-1 rhodopsins, all of which come from cellular organisms. Multiple VirR types are present in metagenomes from across surface oceans, where they are correlated with and nearly as abundant as a canonical marker gene from Mimiviridae Our findings indicate that light-dependent energy transfer systems are likely common components of giant viruses of photosynthetic and phagotrophic unicellular marine eukaryotes.

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A distinct lineage of giant viruses brings a rhodopsin photosystem to unicellular marine predators.

Marine phytoplankton account for approximately half of global primary productivity
 1
 , making their fate an important driver of the marine carbon cycle. Viruses are thought to recycle more than one-quarter of oceanic photosynthetically fixed organic carbon
 2
 , which can stimulate nutrient regeneration, primary production and upper ocean respiration
 2
 via lytic infection and the ‘virus shunt’. Ultimately, this limits the trophic transfer of carbon and energy to both higher food webs and the deep ocean
 2
 . Using imagery taken by the Moderate Resolution Imaging Spectroradiometer (MODIS) onboard the Aqua satellite, along with a suite of diagnostic lipid- and gene-based molecular biomarkers, in situ optical sensors and sediment traps, we show that Coccolithovirus infections of mesoscale (~100 km) Emiliania huxleyi blooms in the North Atlantic are coupled with particle aggregation, high zooplankton grazing and greater downward vertical fluxes of both particulate organic and particulate inorganic carbon from the upper mixed layer. Our analyses captured blooms in different phases of infection (early, late and post) and revealed the highest export flux in ‘early-infected blooms’ with sinking particles being disproportionately enriched with infected cells and subsequently remineralized at depth in the mesopelagic. Our findings reveal viral infection as a previously unrecognized ecosystem process enhancing biological pump efficiency.

Coccolithovirus facilitation of carbon export in the North Atlantic

Emiliania huxleyi produces calcium carbonate (CaCO3 ) coccoliths and transparent exopolymer particles (TEP), sticky, acidic carbohydrates that facilitate aggregation. E. huxleyi's extensive oceanic blooms are often terminated by coccolithoviruses (EhVs) with the transport of cellular debris and associated particulate organic carbon (POC) to depth being facilitated by TEP-bound 'marine snow' aggregates. The dynamics of TEP production and particle aggregation in response to EhV infection are poorly understood. Using flow cytometry, spectrophotometry and FlowCam visualization of alcian blue (AB)-stained aggregates, we assessed TEP production and the size spectrum of aggregates for E. huxleyi possessing different degrees of calcification and cellular CaCO3 :POC mass ratios, when challenged with two EhVs (EhV207 and EhV99B1). FlowCam imaging also qualitatively assessed the relative amount of AB-stainable TEP (i.e., blue:red ratio of each particle). We show significant increases in TEP during early phase EhV207-infection (∼ 24 h) of calcifying strains and a shift towards large aggregates following EhV99B1-infection. We also observed the formation of large aggregates with low blue:red ratios, suggesting that other exopolymer substances contribute towards aggregation. Our findings show the potential for virus infection and the associated response of their hosts to impact carbon flux dynamics and provide incentive to explore these dynamics in natural populations.

Dynamics of transparent exopolymer particle production and aggregation during viral infection of the coccolithophore, Emiliania huxleyi.

Coccolithoviruses (EhVs) are large, double-stranded DNA-containing viruses that infect the single-celled, marine coccolithophore Emiliania huxleyi. Given the cosmopolitan nature and global importance of E. huxleyi as a bloom-forming, calcifying, photoautotroph, E. huxleyi-EhV interactions play a key role in oceanic carbon biogeochemistry. Virally-encoded glycosphingolipids (vGSLs) are virulence factors that are produced by the activity of virus-encoded serine palmitoyltransferase (SPT). Here, we characterize the dynamics, diversity and catalytic production of vGSLs in an array of EhV strains in relation to their SPT sequence composition and explore the hypothesis that they are a determinant of infectivity and host demise. vGSL production and diversity was positively correlated with increased virulence, virus replication rate and lytic infection dynamics in laboratory experiments, but they do not explain the success of less-virulent EhVs in natural EhV communities. The majority of EhV-derived SPT amplicon sequences associated with infected cells in the North Atlantic derived from slower infecting, less virulent EhVs. Our lab-, field- and mathematical model-based data and simulations support ecological scenarios whereby slow-infecting, less-virulent EhVs successfully compete in North Atlantic populations of E. huxleyi, through either the preferential removal of fast-infecting, virulent EhVs during active infection or by having access to a broader host range.

Rebecca Vandzura

Papers

Coccolithovirus facilitation of carbon export in the North Atlantic

Dynamics of transparent exopolymer particle production and aggregation during viral infection of the coccolithophore, Emiliania huxleyi.

Biochemical diversity of glycosphingolipid biosynthesis as a driver of Coccolithovirus competitive ecology