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Viruses can alter the abundance, evolution, and metabolism of microorganisms in the ocean, playing a key role in water column biogeochemistry and global carbon cycles. Large efforts to measure the contribution of eukaryotic microorganisms (e.g., protists) to the marine food web have been made, yet the in situ activities of the ecologically relevant viruses that infect these organisms are not well characterized. Viruses within the phylum Nucleocytoviricota ("giant viruses") are known to infect a diverse range of ecologically relevant marine protists, yet how these viruses are influenced by environmental conditions remains under-characterized. By employing metatranscriptomic analyses of in situ microbial communities along a temporal and depth-resolved gradient, we describe the diversity of giant viruses at the Southern Ocean Time Series (SOTS), a site within the subpolar Southern Ocean. Using a phylogeny-guided taxonomic assessment of detected giant virus genomes and metagenome-assembled genomes, we observed depth-dependent structuring of divergent giant virus families mirroring dynamic physicochemical gradients in the stratified euphotic zone. Analyses of transcribed metabolic genes from giant viruses suggest viral metabolic reprogramming of hosts from the surface to a 200-m depth. Lastly, using on-deck incubations reflecting a gradient of iron availability, we show that modulating iron regimes influences the activity of giant viruses in the field. Specifically, we show enhanced infection signatures of giant viruses under both iron-replete and iron-limited conditions. Collectively, these results expand our understanding of how the water column's vertical biogeography and chemical surroundings affect an important group of viruses within the Southern Ocean. IMPORTANCE The biology and ecology of marine microbial eukaryotes is known to be constrained by oceanic conditions. In contrast, how viruses that infect this important group of organisms respond to environmental change is less well known, despite viruses being recognized as key microbial community members. Here, we address this gap in our understanding by characterizing the diversity and activity of "giant" viruses within an important region in the sub-Antarctic Southern Ocean. Giant viruses are double-stranded DNA (dsDNA) viruses of the phylum Nucleocytoviricota and are known to infect a wide range of eukaryotic hosts. By employing a metatranscriptomics approach using both in situ samples and microcosm manipulations, we illuminated both the vertical biogeography and how changing iron availability affects this primarily uncultivated group of protist-infecting viruses. These results serve as a foundation for our understanding of how the open ocean water column structures the viral community, which can be used to guide models of the viral impact on marine and global biogeochemical cycling.

The trace metal iron (Fe) controls the diversity and activity of phytoplankton across the surface oceans, a paradigm established through decades of in situ and mesocosm experimental studies. Despite widespread Fe-limitation within high-nutrient, low chlorophyll (HNLC) waters, significant contributions of the cyanobacterium Synechococcus to the phytoplankton stock can be found. Correlations among differing strains of Synechococcus across different Fe-regimes have suggested the existence of Fe-adapted ecotypes. However, experimental evidence of high- versus low-Fe adapted strains of Synechococcus is lacking, and so we investigated the transcriptional responses of microbial communities inhabiting the HNLC, sub-Antarctic region of the Southern Ocean during the Spring of 2018. Analysis of metatranscriptomes generated from on-deck incubation experiments reflecting a gradient of Fe-availabilities reveal transcriptomic signatures indicative of co-occurring Synechococcus ecotypes adapted to differing Fe-regimes. Functional analyses comparing low-Fe and high-Fe conditions point to various Fe-acquisition mechanisms that may allow persistence of low-Fe adapted Synechococcus under Fe-limitation. Comparison of in situ surface conditions to the Fe-titrations indicate ecological relevance of these mechanisms as well as persistence of both putative ecotypes within this region. This Fe-titration approach, combined with transcriptomics, highlights the short-term responses of the in situ phytoplankton community to Fe-availability that are often overlooked by examining genomic content or bulk physiological responses alone. These findings expand our knowledge about how phytoplankton in HNLC Southern Ocean waters adapt and respond to changing Fe supply.

This study examined diel shifts in metabolic functions of Microcystis spp. during a 48-h Lagrangian survey of a toxin-producing cyanobacterial bloom in western Lake Erie in the aftermath of the 2014 Toledo Water Crisis. Transcripts mapped to the genomes of recently sequenced lower Great Lakes Microcystis isolates showed distinct patterns of gene expression between samples collected across day (10:00 h, 16:00 h) and night (22:00 h, 04:00 h). Daytime transcripts were enriched in functions related to Photosystem II (e.g., psbA), nitrogen and phosphate acquisition, cell division (ftsHZ), heat shock response (dnaK, groEL), and uptake of inorganic carbon (rbc, bicA). Genes transcribed during nighttime included those involved in phycobilisome protein synthesis and Photosystem I core subunits. Hierarchical clustering and principal component analysis (PCA) showed a tightly clustered group of nighttime expressed genes, whereas daytime transcripts were separated from each other over the 48-h duration. Lack of uniform clustering within the daytime transcripts suggested that the partitioning of gene expression in Microcystis is dependent on both circadian regulation and physicochemical changes within the environment.

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.

Aureococcus anophagefferens forms a model host-virus system with the "giant virus" Kratosvirus quantuckense. Studies to define its ribocell (uninfected) and virocell (virus-infected) forms are needed as these states co-occur during algal blooms. Previously, a link between light-derived energy, virus particle production, and virocell formation was noted. We explored how the time of day (morning, midday, or late day) of virus-host contact shaped virocell ontogeny. In parallel, we explored the dependence on light-derived energy in this mixotrophic plankter by inhibiting photosystem II, testing the role of heterotrophic energy in infection dynamics. Using flow cytometry and photochemical assessments, we examined the physiology of infected cells and controls, and estimated virus particle production. We observed differences between ribocell and virocell response to treatments, including reductions in virus particle production during reduced light duration) and PSII inhibition (i.e. "forced heterotrophy"). This work demonstrates the importance of light in shaping the fate of infected cells and provides insight into factors that constrain in situ blooms. Most significantly, we show that time of the solar day when a virus and host come into contact influences viral particle production, and therefore bloom dynamics; a factor that needs to be considered in bloom modeling work. [ABSTRACT FROM AUTHOR]

Viruses of eukaryotic algae have become an important research focus due to their role(s) in nutrient cycling and top-down control of algal blooms. Omics-based studies have identified a boom of genomic and transcriptional potential among the Nucleocytoviricota, a phylum of large dsDNA viruses which have been shown to infect algal and non-algal eukaryotes. However, little is understood regarding the infection cycle of these viruses, particularly in how they take over a metabolically active host and convert it into a virocell state. Of particular interest are the roles light and the diel cycle play in virocell development. Yet despite such a large proportion of Nucleocytoviricota infecting phototrophs, little work has been done to tie infection dynamics to the presence, and absence, of light. Here, we examined the role of the diel cycle on the physiological and transcriptional state of the pelagophyte Aureococcus anophagefferens while undergoing infection by Kratosvirus quantuckense strain AaV through flow cytometry and differential expression analyses. Our observations demonstrate how infection by the virus interrupts the diel growth and division of this cell strain, and that infection further complicates the system by enhancing export of cell biomass. Furthermore, these analyses reinforce the expectation that viral activity is heavily associated with the diel cycle. [ABSTRACT FROM AUTHOR]

In early August 2014, the municipality of Toledo, OH (USA) issued a 'do not drink' advisory on their water supply directly affecting over 400,000 residential customers and hundreds of businesses (Wilson, 2014). This order was attributable to levels of microcystin, a potent liver toxin, which rose to 2.5μgL-1 in finished drinking water. The Toledo crisis afforded an opportunity to bring together scientists from around the world to share ideas regarding factors that contribute to bloom formation and toxigenicity, bloom and toxin detection as well as prevention and remediation of bloom events. These discussions took place at an NSF- and NOAA-sponsored workshop at Bowling Green State University on April 13 and 14, 2015. In all, more than 100 attendees from six countries and 15 US states gathered together to share their perspectives. The purpose of this review is to present the consensus summary of these issues that emerged from discussions at the Workshop. As additional reports in this special issue provide detailed reviews on many major CHAB species, this paper focuses on the general themes common to all blooms, such as bloom detection, modeling, nutrient loading, and strategies to reduce nutrients.

Viruses, with an estimated abundance of 1031 on Earth, are an important component of soil ecosystems. As obligate parasites that entirely depend on hosts for reproduction and survival, viruses have been linked to microbial community diversity and metabolic activities in soil. Emerging evidence indicates that soil viruses influence a broad-spectrum of processes that sustain soil biodiversity, biogeochemical cycling, fertility, and plant health. Research on soil viruses is in its early stages. Even observational assessments of viral ecology such as abundance, diversity, distribution, life strategies, ecological relevance, and functions, are only just beginning to be revealed. In this review, we summarize the state of knowledge concerning the potential function(s) of soil viruses and how they likely influence microbial community composition, nutrient cycles, and carbon dynamics for example. As major drivers of microbial mortality and functioning across a wide range of spatial and temporal scales, soil viruses appear to be key regulators of cellular metabolism and microbial community properties and as well as biogeochemical processes critical to ecosystem function. We conclude that soil viruses are an indispensable component of soil ecology demanding further investigation. Defining abiotic interactions of viruses within the soil environment, revealing the virus-host interaction networks, and elucidating the roles of soil viruses in carbon and nutrient cycling are but a few of the many aspects of soil viral ecology worthy of future investigation. A more complete view of viral participation in soil food webs in the face of a changing climate will lead to improved management of soil ecosystem services and environmental sustainability. [ABSTRACT FROM AUTHOR]

Research into marine iron cycles and biogeochemistry has commonly relied on the use of chelators (including siderophores) to manipulate iron bioavailability. To test whether a commonly used chelator, desferrioxamine B (DFB) caused effects beyond changing the iron-status of cells, cultures of the environmentally relevant marine heterotrophic bacterium, Ruegeria pomeroyii, were grown in media with different concentrations of iron and/or DFB, resulting in a gradient of iron availability. To determine how cells responded, transcriptomes were generated for cells from the different treatments and analyzed to determine how cells reacted to these to perturbations. Analyses were also performed to look for cellular responses specific to the presence of DFB in the culture medium. As expected, cells experiencing different levels of iron availability had different transcriptomic profiles. While many genes related to iron acquisition were differentially expressed between treatments, there were many other genes that were also differentially expressed between different sample types, including those related to the uptake and metabolism of other metals as well as genes related to metabolism of other types of molecules like amino acids and carbohydrates. We conclude that while DFB certainly altered iron availability to cells, it also appears to have had a general effect on the homeostasis of other metals as well as influenced metabolic processes outside of metal acquisition. [ABSTRACT FROM AUTHOR]

Since the discovery of the first "giant virus," particular attention has been paid toward isolating and culturing these large DNA viruses through Acanthamoeba spp. bait systems. While this method has allowed for the discovery of plenty novel viruses in the Nucleocytoviricota, environmental -omics-based analyses have shown that there is a wealth of diversity among this phylum, particularly in marine datasets. The prevalence of these viruses in metatranscriptomes points toward their ecological importance in nutrient turnover in our oceans and as such, in depth study into non-amoebal Nucleocytoviricota should be considered a focal point in viral ecology. In this review, we report on Kratosvirus quantuckense (née Aureococcus anophagefferens Virus), an algae-infecting virus of the Imitervirales. Current systems for study in the Nucleocytoviricota differ significantly from this virus and its relatives, and a litany of trade-offs within physiology, coding potential, and ecology compared to these other viruses reveal the importance of K. quantuckense. Herein, we review the research that has been performed on this virus as well as its potential as a model system for algal-virus interactions. [ABSTRACT FROM AUTHOR]

Phosphorus (P) availability frequently limits primary production in lakes, influences the physiology of phytoplankton, shapes community structure, and can stimulate or constrain the formation of cyanobacterial blooms. Given the importance of P, numerous methods are available to assess P stress in phytoplankton communities. Marine phytoplankton are known to substitute sulfolipids for phospholipids in response to P limitation. We asked whether sulfolipid substitution might serve as an additional indicator of P stress in freshwater phytoplankton communities. The question was addressed using cultures of Microcystis aeruginosa, Lake Erie microcosms, and surveys of lipid profiles in Lake Erie during a Microcystis spp. bloom. Peak area response ratios of the intact polar lipids sulfoquinovosyldiacylglycerol (SQDG) to phosphatidylglycerol (PG) were used as the metric of lipid substitution. In cultures of M. aeruginosa NIES‐843, the SQDG : PG ratio increased from ~ 0.9 to ~ 3.3 with decreasing P concentration. In P‐limited communities, the SQDG : PG ratio increased from ~ 6 to ~ 11 after 48 h in microcosm controls, while P amendments reduced the ratio to ~ 3. In Lake Erie surveys, the SQDG : PG ratio ranged from ~ 0.4 to ~ 7.4 and was negatively correlated (Pearson r = −0.62) with total dissolved P. The SQDG : PG ratio was not correlated with concentrations of chlorophyll a, soluble reactive P, or N : P molar ratios. These results demonstrated that M. aeruginosa and Microcystis‐dominated communities remodel lipid profiles in response to P scarcity, providing a potential short‐term, time‐integrated biomarker of nutrient history and P stress in fresh waters. [ABSTRACT FROM AUTHOR]

Climate change is affecting how energy and matter flow through ecosystems, thereby altering global carbon and nutrient cycles. Microorganisms play a fundamental role in carbon and nutrient cycling and are thus an integral link between ecosystems and climate. Here, we highlight a major black box hindering our ability to anticipate ecosystem climate responses: viral infections within complex microbial food webs. We show how understanding and predicting ecosystem responses to warming could be challenging—if not impossible—without accounting for the direct and indirect effects of viral infections on different microbes (bacteria, archaea, fungi, protists) that together perform diverse ecosystem functions. Importantly, understanding how rising temperatures associated with climate change influence viruses and virus-host dynamics is crucial to this task, yet is severely understudied. In this perspective, we (i) synthesize existing knowledge about virus-microbe-temperature interactions and (ii) identify important gaps to guide future investigations regarding how climate change might alter microbial food web effects on ecosystem functioning. To provide real-world context, we consider how these processes may operate in peatlands—globally significant carbon sinks that are threatened by climate change. We stress that understanding how warming affects biogeochemical cycles in any ecosystem hinges on disentangling complex interactions and temperature responses within microbial food webs. [ABSTRACT FROM AUTHOR]