Publications by authors named "Steven Wilhelm"

107 Publications

Elevated pH Conditions Associated With spp. Blooms Decrease Viability of the Cultured Diatom and Natural Diatoms in Lake Erie.

Front Microbiol 2021 24;12:598736. Epub 2021 Feb 24.

Department of Microbiology, The University of Tennessee, Knoxville, Knoxville, TN, United States.

Cyanobacterial Harmful Algal Blooms (CyanoHABs) commonly increase water column pH to alkaline levels ≥9.2, and to as high as 11. This elevated pH has been suggested to confer a competitive advantage to cyanobacteria such as . Yet, there is limited information regarding the restrictive effects bloom-induced pH levels may impose on this cyanobacterium's competitors. Due to the pH-dependency of biosilicification processes, diatoms (which seasonally both precede and proceed blooms in many fresh waters) may be unable to synthesize frustules at these pH levels. We assessed the effects of pH on the ecologically relevant diatom , and on a Lake Erie diatom community . assays revealed monocultures exhibited lower growth rates and abundances when cultivated at a starting pH of 9.2 in comparison to pH 7.7. The suppressed growth trends in were exacerbated when co-cultured with at pH conditions and cell densities that simulated a cyanobacteria bloom. Estimates demonstrated a significant decrease in silica (Si) deposition at alkaline pH in both cultures and Lake Erie diatom assemblages, after as little as 48 h of alkaline pH-exposure. These observations indicate elevated pH negatively affected growth rate and diatom silica deposition; in total providing a competitive disadvantage for diatoms. Our observations demonstrate pH likely plays a significant role in bloom succession, creating a potential to prolong summer blooms and constrain diatom fall resurgence.
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http://dx.doi.org/10.3389/fmicb.2021.598736DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7943883PMC
February 2021

Metagenome-Assembled Genome Sequences of Raphidiopsis raciborskii and Planktothrix agardhii from a Cyanobacterial Bloom in Kissena Lake, New York, USA.

Microbiol Resour Announc 2021 Jan 14;10(2). Epub 2021 Jan 14.

Department of Microbiology, University of Tennessee, Knoxville, Tennessee, USA

and are filamentous, potentially toxin-producing cyanobacteria that form nuisance blooms in fresh waters. Here, we report high-quality metagenome-assembled genome sequences of and collected from a bloom in Kissena Lake, New York.
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http://dx.doi.org/10.1128/MRA.01380-20DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7849711PMC
January 2021

Roles of Nutrient Limitation on Western Lake Erie CyanoHAB Toxin Production.

Toxins (Basel) 2021 Jan 9;13(1). Epub 2021 Jan 9.

Institute of Marine Sciences, University of North Carolina at Chapel Hill, Morehead City, NC 28557, USA.

Cyanobacterial harmful algal bloom (CyanoHAB) proliferation is a global problem impacting ecosystem and human health. Western Lake Erie (WLE) typically endures two highly toxic CyanoHABs during summer: a spp. bloom in Maumee Bay that extends throughout the western basin, and a spp. bloom in Sandusky Bay. Recently, the USA and Canada agreed to a 40% phosphorus (P) load reduction to lessen the severity of the WLE blooms. To investigate phosphorus and nitrogen (N) limitation of biomass and toxin production in WLE CyanoHABs, we conducted in situ nutrient addition and 40% dilution microcosm bioassays in June and August 2019. During the June Sandusky Bay bloom, biomass production as well as hepatotoxic microcystin and neurotoxic anatoxin production were N and P co-limited with microcystin production becoming nutrient deplete under 40% dilution. During August, the Maumee Bay bloom produced microcystin under nutrient repletion with slight induced P limitation under 40% dilution, and the Sandusky Bay bloom produced anatoxin under N limitation in both dilution treatments. The results demonstrate the importance of nutrient limitation effects on microcystin and anatoxin production. To properly combat cyanotoxin and cyanobacterial biomass production in WLE, both N and P reduction efforts should be implemented in its watershed.
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http://dx.doi.org/10.3390/toxins13010047DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7828104PMC
January 2021

Tracing the active genetic diversity of Microcystis and Microcystis phage through a temporal survey of Taihu.

PLoS One 2020 28;15(12):e0244482. Epub 2020 Dec 28.

Department of Microbiology, The University of Tennessee, Knoxville, Tennessee, United States of America.

Harmful algal blooms are commonly thought to be dominated by a single genus, but they are not homogenous communities. Current approaches, both molecular and culture-based, often overlook fine-scale variations in community composition that can influence bloom dynamics. We combined homology-based searches (BLASTX) and phylogenetics to distinguish and quantify Microcystis host and phage members across a summer season during a 2014 Microcystis- dominated bloom that occurred in Lake Tai (Taihu), China. We found 47 different genotypes of the Microcystis-specific DNA-dependent RNA polymerase (rpoB), which included several morphospecies. Microcystis flos-aquae and Microcystis wesenbergii accounted for ~86% of total Microcystis transcripts, while the more commonly studied Microcystis aeruginosa only accounted for ~7%. Microcystis genotypes were classified into three temporal groups according to their expression patterns across the course of the bloom: early, constant and late. All Microcystis morphospecies were present in each group, indicating that expression patterns were likely dictated by competition driven by environmental factors, not phylogeny. We identified three primary Microcystis-infecting phages based on the viral terminase, including a novel Siphoviridae phage that may be capable of lysogeny. Within our dataset, Myoviridae phages consistent with those infecting Microcystis in a lytic manner were positively correlated to the early host genotypes, while the Siphoviridae phages were positively correlated to the late host genotypes, when the Myoviridae phages express putative genetic markers for lysogeny. The expression of genes in the microcystin-encoding mcy cassette was estimated using mcyA, which revealed 24 Microcystis-specific genotypes that were negatively correlated to the early host genotypes. Of all environmental factors measured, pH best described the temporal shift in the Microcystis community genotypic composition, promoting hypotheses regarding carbon concentration mechanisms and oxidative stress. Our work expounds on the complexity of HAB events, using a well-studied dataset to highlight the need for increased resolution of community dynamics.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0244482PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7769430PMC
March 2021

Episodic Decrease in Temperature Increases Gene Transcription and Cellular Microcystin in Continuous Cultures of PCC 7806.

Front Microbiol 2020 3;11:601864. Epub 2020 Dec 3.

Department of Microbiology, The University of Tennessee, Knoxville, Knoxville, TN, United States.

Microcystins produced during harmful cyanobacterial blooms are a public health concern. Although patterns are emerging, the environmental cues that stimulate production of microcystin remain confusing, hindering our ability to predict fluctuations in bloom toxicity. In earlier work, growth at cool temperatures relative to optimum (18°C 26°C) was confirmed to increase microcystin quota in batch cultures of NIES-843. Here, we tested this response in PCC 7806 using continuous cultures to examine temporal dynamics and using RNA-sequencing to investigate the physiological nature of the response. A temperature reduction from 26 to 19°C increased microcystin quota ∼2-fold, from an average of ∼464 ag μm cell volume to ∼891 ag μm over a 7-9 d period. Reverting the temperature to 26°C returned the cellular microcystin quota to ∼489 ag μm. Long periods (31-42 d) at 19°C did not increase or decrease microcystin quota beyond that observed at 7-9 d. Nitrogen concentration had little effect on the overall response. RNA sequencing indicated that the decrease in temperature to 19°C induced a classic cold-stress response in PCC 7806, but this operated on a different timescale than the increased microcystin production. Microcystin quota showed a strong 48- to 72-h time-lag correlation to gene expression, but no correlation to concurrent expression. This work confirms an effect of temperature on microcystin quota and extends our understanding of the physiological nature of the response.
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http://dx.doi.org/10.3389/fmicb.2020.601864DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7744600PMC
December 2020

Intermittent disturbance benefits colony size, biomass and dominance of Microcystis in Lake Taihu under field simulation condition.

Harmful Algae 2020 11 10;99:101909. Epub 2020 Oct 10.

Faculty of Resources and Environmental Science, Hubei University, Wuhan 430062, China. Electronic address:

Wind-driven wave disturbance is one of the environmental factors that shapes the formation of Microcystis blooms. Here we present data on the effect of different disturbance modes (continuous vs intermittent disturbances) on colony size, biomass and dominance of Microcystis in Lake Taihu under field conditions. Small submersible pumps were used to simulate different disturbance modes at turbulent dissipation rate (ε) of 2.98 × 10 m s. Our results show that the mean colony sizes of Microcystis in intermittent and continuous disturbance group were 1.94 and 1.23 times that of the control group, respectively. The mean densities of Microcystis in intermittent and continuous disturbance group were 4.23 and 2.91 times that of the control group, respectively. The mean proportion of Microcystis to total algae abundance in control group and continuous disturbance group changed from 78.3% at beginning of the experiment to 4.5% and 9.1% at the end of the experiment. However, the proportion of Microcystis to total algae cells in intermittent disturbance group was 65.7-94.3% during the whole experiment. The results demonstrated intermittent disturbances favored colony morphology, biomass and dominance of Microcystis. Our results suggested that intermittent disturbance benefited the formation of Microcystis bloom and was important in the development of predictive models for toxic cyanobacterial blooms under changing climates in shallow lakes.
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http://dx.doi.org/10.1016/j.hal.2020.101909DOI Listing
November 2020

Structural and Proteomic Studies of the Virus Demonstrate a Global Distribution of Virus-Encoded Carbohydrate Processing.

Front Microbiol 2020 8;11:2047. Epub 2020 Sep 8.

Department of Microbiology, The University of Tennessee, Knoxville, Knoxville, TN, United States.

Viruses modulate the function(s) of environmentally relevant microbial populations, yet considerations of the metabolic capabilities of individual virus particles themselves are rare. We used shotgun proteomics to quantitatively identify 43 virus-encoded proteins packaged within purified Virus (AaV) particles, normalizing data to the per-virion level using a 9.5-Å-resolution molecular reconstruction of the 1900-Å (AaV) particle that we generated with cryogenic electron microscopy. This packaged proteome was used to determine similarities and differences between members of different giant virus families. We noted that proteins involved in sugar degradation and binding (e.g., carbohydrate lyases) were unique to AaV among characterized giant viruses. To determine the extent to which this virally encoded metabolic capability was ecologically relevant, we examined the TARA Oceans dataset and identified genes and transcripts of viral origin. Our analyses demonstrated that putative giant virus carbohydrate lyases represented up to 17% of the marine pool for this function. In total, our observations suggest that the AaV particle has potential prepackaged metabolic capabilities and that these may be found in other giant viruses that are widespread and abundant in global oceans.
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http://dx.doi.org/10.3389/fmicb.2020.02047DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7507832PMC
September 2020

The Complicated and Confusing Ecology of Blooms.

mBio 2020 06 30;11(3). Epub 2020 Jun 30.

Great Lakes Institute for Environmental Research, University of Windsor, Windsor, Ontario, Canada.

Blooms of the toxin-producing cyanobacterium are increasing globally, leading to the loss of ecosystem services, threats to human health, as well as the deaths of pets and husbandry animals. While nutrient availability is a well-known driver of algal biomass, the factors controlling "who" is present in fresh waters are more complicated. possesses multiple strategies to adapt to temperature, light, changes in nutrient chemistry, herbivory, and parasitism that provide a selective advantage over its competitors. Moreover, its ability to alter ecosystem pH provides it a further advantage that helps exclude many of its planktonic competitors. While decades of nutrient monitoring have provided us with the tools to predict the accumulation of phytoplankton biomass, here, we point to factors on the horizon that may inform us why is presently the dominant bloom former in freshwaters around the world.
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http://dx.doi.org/10.1128/mBio.00529-20DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7327167PMC
June 2020

SMRT Sequencing of Paramecium Bursaria Chlorella Virus-1 Reveals Diverse Methylation Stability in Adenines Targeted by Restriction Modification Systems.

Front Microbiol 2020 19;11:887. Epub 2020 May 19.

Department of Microbiology, The University of Tennessee, Knoxville, Knoxville, TN, United States.

Chloroviruses (family ) infect eukaryotic, freshwater, unicellular green algae. A unique feature of these viruses is an abundance of DNA methyltransferases, with isolates dedicating up to 4.5% of their protein coding potential to these genes. This diversity highlights just one of the long-standing values of the chlorovirus model system; where group-wide epigenomic characterization might begin to elucidate the function(s) of DNA methylation in large dsDNA viruses. We characterized DNA modifications in the prototype chlorovirus, PBCV-1, using single-molecule real time (SMRT) sequencing ( PacBio). Results were compared to total available sites predicted based on DNA sequence alone. SMRT-software detected N6-methyl-adenine (m6A) at GATC and CATG recognition sites, motifs previously shown to be targeted by PBCV-1 DNA methyltransferases M.CviAI and M. AII, respectively. At the same time, PacBio analyses indicated that 10.9% of the PBCV-1 genome had large interpulse duration ratio (ipdRatio) values, the primary metric for DNA modification identification. These events represent 20.6x more sites than can be accounted for by all available adenines in GATC and CATG motifs, suggesting base or backbone modifications other than methylation might be present. To define methylation stability, we cross-compared methylation status of each GATC and CATG sequence in three biological replicates and found ∼81% of sites were stably methylated, while ∼2% consistently lack methylation. The remaining 17% of sites were stochastically methylated. When methylation status was analyzed for both strands of each target, we show that palindromes existed in completely non-methylated states, fully-methylated states, or hemi-methylated states, though GATC sites more often lack methylation than CATG sequences. Given that both sequences are targeted by not just methyltransferases, but by restriction endonucleases that are together encoded by PBCV-1 as virus-originating restriction modification (RM) systems, there is strong selective pressure to modify all target sites. The finding that most instances of non-methylation are associated with hemi-methylation is congruent with observations that hemi-methylated palindromes are resistant to cleavage by restriction endonucleases. However, sites where hemi-methylation is conserved might represent a unique regulatory function for PBCV-1. This study serves as a baseline for future investigation into the epigenomics of chloroviruses and their giant virus relatives.
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http://dx.doi.org/10.3389/fmicb.2020.00887DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7248222PMC
May 2020

Nitrogen flux into metabolites and microcystins changes in response to different nitrogen sources in Microcystis aeruginosa NIES-843.

Environ Microbiol 2020 06 5;22(6):2419-2431. Epub 2020 May 5.

Department of Microbiology, University of Tennessee, Knoxville, TN, USA.

The over-enrichment of nitrogen (N) in the environment has contributed to severe and recurring harmful cyanobacterial blooms, especially by the non-N -fixing Microcystis spp. N chemical speciation influences cyanobacterial growth, persistence and the production of the hepatotoxin microcystin, but the physiological mechanisms to explain these observations remain unresolved. Stable-labelled isotopes and metabolomics were employed to address the influence of nitrate, ammonium, and urea on cellular physiology and production of microcystins in Microcystis aeruginosa NIES-843. Global metabolic changes were driven by both N speciation and diel cycling. Tracing N-labelled nitrate, ammonium, and urea through the metabolome revealed N uptake, regardless of species, was linked to C assimilation. The production of amino acids, like arginine, and other N-rich compounds corresponded with greater turnover of microcystins in cells grown on urea compared to nitrate and ammonium. However, N was incorporated into microcystins from all N sources. The differences in N flux were attributed to the energetic efficiency of growth on each N source. While N in general plays an important role in sustaining biomass, these data show that N-speciation induces physiological changes that culminate in differences in global metabolism, cellular microcystin quotas and congener composition.
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http://dx.doi.org/10.1111/1462-2920.15032DOI Listing
June 2020

Internal Nitrogen Pools Shape the Infection of CCMP 1984 by a Giant Virus.

Front Microbiol 2020 25;11:492. Epub 2020 Mar 25.

Department of Microbiology, College of Arts and Sciences, The University of Tennessee, Knoxville, Knoxville, TN, United States.

The pelagophyte blooms annually in shallow bays around the world, where it is hypothesized to outcompete other phytoplankton in part by using alternative nitrogen sources. The high proportion of natural populations that are infected during the late stages of the bloom suggest viruses cause bloom collapse. We hypothesized that the Aureococcus anophagefferens Virus (AaV) infection cycle would be negatively influenced in cultures acclimated to decreasing external nitrogen conditions, but that the real-time external nitrogen concentration would not influence the infection cycle. Cultures acclimated in concentrations (0.0147 mM; N:P = 0.1225) that showed reduced end point cell abundances, forward scatter (a proxy for size) and red fluorescence (a proxy for chlorophyll ), also produced fewer viruses per cell at a slower rate. Decreasing the external concentration of nitrogen post infection did not alter burst size or time to lysis. These data suggest that the nitrogen used for new viral progeny is present within host cells at the time of infection. Flow cytometric data of an infection cycle showed a reduction in red fluorescence around twelve hours post infection, consistent with degradation of nitrogen-rich chloroplasts during the infection cycle. Using cell and virus quota estimates, we determined that cells had sufficient nitrogen and carbon for the lower ranges of burst sizes determined but did not contain enough phosphorous. Consistent with this observation, expression of nitrate and sugar transporters did not increase in the publicly available transcriptome data of the infection cycle, while several phosphorus transporters were. Our data demonstrate that dynamics of viruses infecting over the course of a bloom is dictated by the host cell state upon infection, which is set by external nutrient supplies.
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http://dx.doi.org/10.3389/fmicb.2020.00492DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7109300PMC
March 2020

The "Neglected Viruses" of : Abundant Transcripts for Viruses Infecting Eukaryotes and Their Potential Role in Phytoplankton Succession.

Front Microbiol 2020 6;11:338. Epub 2020 Mar 6.

Department of Microbiology, The University of Tennessee, Knoxville, Knoxville, TN, United States.

Drivers of algal bloom dynamics remain poorly understood, but viruses have been implicated as important players. Research addressing bloom dynamics has generally been restricted to the virus-infection of the numerically dominant (i.e. bloom forming) taxa. Yet this approach neglects a broad diversity of viral groups, limiting our knowledge of viral interactions and constraints within these systems. We examined hallmark virus marker genes in metatranscriptomic libraries from a seasonal and spatial survey of a bloom in Lake Tai () China to identify active infections by nucleocytoplasmic large DNA viruses (NCLDVs), RNA viruses, ssDNA viruses, bacteriophage, and virophage. Phylogenetic analyses revealed a diverse virus population with seasonal and spatial variability. We observed disproportionately high expression of markers associated with NCLDVs and ssRNA viruses (consistent with viruses that infect photosynthetic protists) relative to bacteriophage infecting heterotrophic bacteria or cyanobacteria during the height of the bloom event. Under a modified kill-the-winner scheme, we hypothesize viruses infecting protists help suppress the photosynthetic eukaryotic community and allow for the proliferation of cyanobacteria such as . Our observations provide a foundation for a little considered factor promoting algal blooms.
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http://dx.doi.org/10.3389/fmicb.2020.00338DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7067694PMC
March 2020

Exploration of sensory and spinal neurons expressing gastrin-releasing peptide in itch and pain related behaviors.

Nat Commun 2020 03 13;11(1):1397. Epub 2020 Mar 13.

Center for the Study of Itch and Sensory Disorders, Washington University School of Medicine, St. Louis, MO, 63110, USA.

Gastrin-releasing peptide (GRP) functions as a neurotransmitter for non-histaminergic itch, but its site of action (sensory neurons vs spinal cord) remains controversial. To determine the role of GRP in sensory neurons, we generated a floxed Grp mouse line. We found that conditional knockout of Grp in sensory neurons results in attenuated non-histaminergic itch, without impairing histamine-induced itch. Using a Grp-Cre knock-in mouse line, we show that the upper epidermis of the skin is exclusively innervated by GRP fibers, whose activation via optogeneics and chemogenetics in the skin evokes itch- but not pain-related scratching or wiping behaviors. In contrast, intersectional genetic ablation of spinal Grp neurons does not affect itch nor pain transmission, demonstrating that spinal Grp neurons are dispensable for itch transmission. These data indicate that GRP is a neuropeptide in sensory neurons for non-histaminergic itch, and GRP sensory neurons are dedicated to itch transmission.
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http://dx.doi.org/10.1038/s41467-020-15230-yDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7070094PMC
March 2020

Insight Into the Molecular Mechanisms for Microcystin Biodegradation in Lake Erie and Lake Taihu.

Front Microbiol 2019 10;10:2741. Epub 2019 Dec 10.

Department of Microbiology, The University of Tennessee, Knoxville, Knoxville, TN, United States.

Microcystins are potent hepatotoxins that are frequently detected in fresh water lakes plagued by toxic cyanobacteria. Microbial biodegradation has been referred to as the most important avenue for removal of microcystin from aquatic environments. The biochemical pathway most commonly associated with the degradation of microcystin is encoded by the () cassette. The ecological significance of this pathway remains unclear as no studies have examined the expression of these genes in natural environments. Six metatranscriptomes were generated from microcystin-producing blooms and analyzed to assess the activity of this pathway in environmental samples. Seventy-eight samples were collected from Lake Erie, United States/Canada and Lake Tai (), China, and screened for the presence of gene transcripts. Read mapping to the cassette indicated transcripts for these genes were absent, with only 77 of the collective 3.7 billion reads mapping to any part of the cassette. Analysis of the assembled metatranscriptomes supported this, with only distantly related sequences identified as like. These observations were made despite the presence of microcystin and over 500,000 reads mapping to the mcy cassette for microcystin production. Glutathione S-transferases and alkaline proteases have been previously hypothesized to be alternative pathways for microcystin biodegradation, and expression of these genes was detected across space and time in both lakes. While the activity of these alternative pathways needs to be experimentally confirmed, they may be individually or collectively more important than genes in the natural environment. Importantly, the lack of expression could indicate microcystin biodegradation was not occurring in the analyzed samples. This study raises interesting questions about the ubiquity, specificity and locality of microcystin biodegradation, and highlights the need for the characterization of relevant mechanisms in natural communities to understand the fate of microcystin in the environment and risk to public health.
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http://dx.doi.org/10.3389/fmicb.2019.02741DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6914704PMC
December 2019

Influence of light on the infection of Aureococcus anophagefferens CCMP 1984 by a "giant virus".

PLoS One 2020 3;15(1):e0226758. Epub 2020 Jan 3.

Department of Microbiology, University of Tennessee, Knoxville, Tennessee, United States of America.

The pelagophyte Aureococcus anophagefferens has caused recurrent brown tide blooms along the northeast coast of the United States since the mid-1980's, and more recently spread to other regions of the globe. These blooms, due to the high cell densities, are associated with severe light attenuation that destroys the sea grass beds which provide the basis for many fisheries. Data collected by transmission electron microscopy, PCR, and metatranscriptomic studies of the blooms, support the hypothesis that large dsDNA viruses play a role in bloom dynamics. While a large (~140 nm) icosahedral virus, with a 371 kbp genome, was first isolated more than a decade ago, the constraints imposed by environmental parameters on bloom infection dynamics by Aureococcus anophagefferens Virus, (AaV) remain unknown. To investigate the role light plays in infection by this virus, we acclimated A. anophagefferens to light intensities of 30 (low), 60 (medium) or 90 μmol photons m-2 s-1 (high) and infected cultures at these irradiance levels. Moreover, we completed light shift experiments where acclimated cultures were exposed to even lower light intensities (0, 5, and 15 μmol photons m-2 s-1) consistent with irradiance found during the peak of the bloom when cell concentrations are highest. The abundance of viruses produced per lytic event (burst size) was lower in the low irradiance acclimated cultures compared to the medium and high acclimated cultures. Transferring infected cultures to more-limiting light availabilities further decreased burst size and increased the length of time it took for cultures to lyse, regardless of acclimation irradiance level. A hypothetical mechanism for the reduced efficiency of the infection cycle in low light due to ribosome biogenesis was predicted from pre-existing transcriptomes. Overall, these studies provide a framework for understanding light effects on infection dynamics over the course of the summer months when A. anophagefferens blooms occur.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0226758PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6941929PMC
April 2020

Metatranscriptomic Analyses of Diel Metabolic Functions During a Bloom in Western Lake Erie (United States).

Front Microbiol 2019 10;10:2081. Epub 2019 Sep 10.

Department of Biological Sciences, Bowling Green State University, Bowling Green, OH, United States.

This study examined diel shifts in metabolic functions of 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 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., ), nitrogen and phosphate acquisition, cell division (), heat shock response (, ), and uptake of inorganic carbon (, ). 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 is dependent on both circadian regulation and physicochemical changes within the environment.
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http://dx.doi.org/10.3389/fmicb.2019.02081DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6746948PMC
September 2019

The Human Cytomegalovirus Chemokine vCXCL-1 Modulates Normal Dissemination Kinetics of Murine Cytomegalovirus .

mBio 2019 06 25;10(3). Epub 2019 Jun 25.

Department of Microbiology, University of Tennessee, Knoxville, Tennessee, USA

Human cytomegalovirus (HCMV) is a betaherpesvirus that is a significant pathogen within newborn and immunocompromised populations. Morbidity associated with HCMV infection is the consequence of viral dissemination. HCMV has evolved to manipulate the host immune system to enhance viral dissemination and ensure long-term survival within the host. The immunomodulatory protein vCXCL-1, a viral chemokine functioning primarily through the CXCR2 chemokine receptor, is hypothesized to attract CXCR2 neutrophils to infection sites, aiding viral dissemination. Neutrophils harbor HCMV ; however, the interaction between vCXCL-1 and the neutrophil has not been evaluated Using the mouse model and mouse cytomegalovirus (MCMV) infection, we show that murine neutrophils harbor and transfer infectious MCMV and that virus replication initiates within this cell type. Utilizing recombinant MCMVs expressing vCXCL-1 from the HCMV strain (Toledo), we demonstrated that vCXCL-1 significantly enhances MCMV dissemination kinetics. Through cellular depletion experiments, we observe that neutrophils impact dissemination but that overall dissemination is largely neutrophil independent. This work adds neutrophils to the list of innate cells (i.e., dendritic and macrophages/monocytes) that contribute to MCMV dissemination but refutes the hypothesis that neutrophils are the primary cell responding to vCXCL-1. An adequate analysis of HCMV's viral chemokine vCXCL-1 has been lacking. Here we generate recombinant MCMVs expressing vCXCL-1 to study vCXCL-1 function using MCMV as a surrogate. We demonstrate that vCXCL-1 increases MCMV dissemination kinetics for both primary and secondary dissemination. Additionally, we provide evidence, that the murine neutrophil is largely a bystander in the mouse's response to vCXCL-1. We confirm the hypothesis that vCXCL-1 is a HCMV virulence factor. Infection of severely immunocompromised mice with MCMVs expressing vCXCL-1 was lethal in more than 50% of infected animals, while all animals infected with parental virus survived during a 12-day period. This work provides needed insights into vCXCL-1 function .
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http://dx.doi.org/10.1128/mBio.01289-19DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6593410PMC
June 2019

One-time nitrogen fertilization shifts switchgrass soil microbiomes within a context of larger spatial and temporal variation.

PLoS One 2019 18;14(6):e0211310. Epub 2019 Jun 18.

Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee, United States of America.

Soil microbiome responses to short-term nitrogen (N) inputs remain uncertain when compared with previous research that has focused on long-term fertilization responses. Here, we examined soil bacterial/archaeal and fungal communities pre- and post-N fertilization in an 8 year-old switchgrass field, in which twenty-four plots received N fertilization at three levels (0, 100, and 200 kg N ha-1 as NH4NO3) for the first time since planting. Soils were collected at two depths, 0-5 and 5-15 cm, for DNA extraction and amplicon sequencing of 16S rRNA genes and ITS regions for assessment of microbial community composition. Baseline assessments prior to fertilization revealed no significant pre-existing divergence in either bacterial/archaeal or fungal communities across plots. The one-time N fertilizations increased switchgrass yields and tissue N content, and the added N was nearly completely removed from the soil of fertilized plots by the end of the growing season. Both bacterial/archaeal and fungal communities showed large spatial (by depth) and temporal variation (by season) within each plot, accounting for 17 and 12-22% of the variation as calculated from the Sq. root of PERMANOVA tests for bacterial/archaeal and fungal community composition, respectively. While N fertilization effects accounted for only ~4% of overall variation, some specific microbial groups, including the bacterial genus Pseudonocardia and the fungal genus Archaeorhizomyces, were notably repressed by fertilization at 200 kg N ha-1. Bacterial groups varied with both depth in the soil profile and time of sampling, while temporal variability shaped the fungal community more significantly than vertical heterogeneity in the soil. These results suggest that short-term effects of N fertilization are significant but subtle, and other sources of variation will need to be carefully accounted for study designs including multiple intra-annual sampling dates, rather than one-time "snapshot" analyses that are common in the literature. Continued analyses of these trends over time with fertilization and management are needed to understand how these effects may persist or change over time.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0211310PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6581249PMC
February 2020

Urea Is Both a Carbon and Nitrogen Source for : Tracking C Incorporation at Bloom pH Conditions.

Front Microbiol 2019 17;10:1064. Epub 2019 May 17.

Department of Microbiology, The University of Tennessee, Knoxville, Knoxville, TN, United States.

The use of urea as a nitrogenous fertilizer has increased over the past two decades, with urea itself being readily detected at high concentrations in many lakes. Urea has been linked to cyanobacterial blooms as it is a readily assimilated nitrogen (N) - source for cyanobacteria that possess the enzyme urease. We tested the hypothesis that urea may also act as a carbon (C) source to supplemental growth requirements during the alkaline conditions created by dense cyanobacterial blooms, when concentrations of dissolved CO are vanishingly low. High rates of photosynthesis markedly reduce dissolved CO concentrations and drive up pH. This was observed in Lake Erie during the largest bloom on record (2015) over long periods (months) and short periods (days) of time, suggesting blooms experience periods of CO-limitation on a seasonal and daily basis. We used C-urea to demonstrate that axenic cultures of the model toxic cyanobacterium, NIES843, assimilated C at varying environmentally relevant pH conditions directly into a spectrum of metabolic pools during urea hydrolysis. Primarily, C from urea was assimilated into central C metabolism and amino acid biosynthesis pathways, including those important for the production of the hepatotoxin, microcystin, and incorporation into these pathways was at a higher percentage during growth at higher pH. This corresponded to increased growth rates on urea as the sole N source with increasing pH. We propose this ability to incorporate C from urea represents yet another competitive advantage for this cyanobacterium during dense algal blooms.
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http://dx.doi.org/10.3389/fmicb.2019.01064DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6536089PMC
May 2019

Corrigendum: Genome and Environmental Activity of a Virus and Its Virophages.

Front Microbiol 2019 24;10:907. Epub 2019 Apr 24.

Department of Biology, University of Toronto Mississauga, Mississauga, ON, Canada.

[This corrects the article DOI: 10.3389/fmicb.2019.00703.].
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http://dx.doi.org/10.3389/fmicb.2019.00907DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6492039PMC
April 2019

Genome and Environmental Activity of a Virus and Its Virophages.

Front Microbiol 2019 5;10:703. Epub 2019 Apr 5.

Department of Biology, University of Toronto Mississauga, Mississauga, ON, Canada.

Some giant viruses are ecological agents that are predicted to be involved in the top-down control of single-celled eukaryotic algae populations in aquatic ecosystems. Despite an increased interest in giant viruses since the discovery and characterization of and other viral giants, little is known about their physiology and ecology. In this study, we characterized the genome and functional potential of a giant virus that infects the freshwater haptophyte , originally isolated from Lake Ontario. This virus, CpV-BQ2, is a member of the nucleo-cytoplasmic large DNA virus (NCLDV) group and possesses a 437 kb genome encoding 503 ORFs with a GC content of 25%. Phylogenetic analyses of core NCLDV genes place CpV-BQ2 amongst the emerging group of algae-infecting Mimiviruses informally referred to as the "extended ," making it the first virus of this group to be isolated from a freshwater ecosystem. During genome analyses, we also captured and described the genomes of three distinct virophages that co-occurred with CpV-BQ2 and likely exploit CpV for their own replication. These virophages belong to the polinton-like viruses (PLV) group and encompass 19-23 predicted genes, including all of the core PLV genes as well as several genes implicated in genome modifications. We used the CpV-BQ2 and virophage reference sequences to recruit reads from available environmental metatranscriptomic data to estimate their activity in fresh waters. We observed moderate recruitment of both virus and virophage transcripts in samples obtained during blooms in Lake Erie and Lake Tai, China in 2013, with a spike in activity in one sample. Virophage transcript abundance for two of the three isolates strongly correlated with that of the CpV-BQ2. Together, the results highlight the importance of giant viruses in the environment and establish a foundation for future research on the physiology and ecology CpV-BQ2 as a model system for algal Mimivirus dynamics in freshwaters.
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http://dx.doi.org/10.3389/fmicb.2019.00703DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6459981PMC
April 2019

Nutrient stoichiometry shapes microbial coevolution.

Ecol Lett 2019 Jun 29;22(6):1009-1018. Epub 2019 Mar 29.

Department of Biology, Indiana University, Bloomington, IN, 47405, USA.

Coevolution is a force contributing to the generation and maintenance of biodiversity. It is influenced by environmental conditions including the scarcity of essential resources, which can drive the evolution of defence and virulence traits. We conducted a long-term chemostat experiment where the marine cyanobacterium Synechococcus was challenged with a lytic phage under nitrogen (N) or phosphorus (P) limitation. This manipulation of nutrient stoichiometry altered the stability of host-parasite interactions and the underlying mode of coevolution. By assessing the infectivity with > 18 000 pairwise challenges, we documented directional selection for increased phage resistance, consistent with arms-race dynamics while phage infectivity fluctuated through time, as expected when coevolution is driven by negative frequency-dependent selection. The resulting infection networks were 50% less modular under N- versus P-limitation reflecting host-range contraction and asymmetric coevolutionary trajectories. Nutrient stoichiometry affects eco-evolutionary feedbacks in ways that may alter the dynamics and functioning of environmental and host-associated microbial communities.
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http://dx.doi.org/10.1111/ele.13252DOI Listing
June 2019

Cryopreservation of Paramecium bursaria Chlorella Virus-1 during an active infection cycle of its host.

PLoS One 2019 14;14(3):e0211755. Epub 2019 Mar 14.

Department of Microbiology, University of Tennessee, Knoxville, Tennessee, United States of America.

Best practices in laboratory culture management often include cryopreservation of microbiota, but this can be challenging with some virus particles. By preserving viral isolates researchers can mitigate genetic drift and laboratory-induced selection, thereby maintaining genetically consistent strains between experiments. To this end, we developed a method to cryopreserve the model, green-alga infecting virus, Paramecium bursaria Chlorella virus 1 (PBCV-1). We explored cryotolerance of the infectivity of this virus particle, whereby freezing without cryoprotectants was found to maintain the highest infectivity (~2.5%). We then assessed the cryopreservation potential of PBCV-1 during an active infection cycle in its Chlorella variabilis NC64A host, and found that virus survivorship was highest (69.5 ± 16.5%) when the infected host is cryopreserved during mid-late stages of infection (i.e., coinciding with virion assembly). The most optimal condition for cryopreservation was observed at 240 minutes post-infection. Overall, utilizing the cell as a vehicle for viral cryopreservation resulted in 24.9-30.1 fold increases in PBCV-1 survival based on 95% confidence intervals of frozen virus particles and virus cryopreserved at 240 minutes post-infection. Given that cryoprotectants are often naturally produced by psychrophilic organisms, we suspect that cryopreservation of infected hosts may be a reliable mechanism for virus persistence in non-growth permitting circumstances in the environment, such as ancient permafrosts.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0211755PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6417706PMC
December 2019

Viral and bacterial community responses to stimulated Fe(III)-bioreduction during simulated subsurface bioremediation.

Environ Microbiol 2019 06 28;21(6):2043-2055. Epub 2019 Mar 28.

Department of Biosystems Engineering and Soil Science, The University of Tennessee, Knoxville, TN, 37996, USA.

The delivery of fermentable substrate(s) to subsurface environments stimulates Fe(III)-bioreduction and achieves detoxification of organic/inorganic contaminants. Although, much research has been conducted on the microbiology of such engineered systems at lab and field scales, little attention has been given to the phage-host interactions and virus community dynamics in these environments. The objective was to determine the responses of soil bacterial communities and viral assemblages to stimulated anaerobic Fe(III)-bioreduction following electron donor (e.g. acetate) addition. Microbial communities, including viral assemblages, were investigated after 60 days of Fe(III)-bioreduction in laboratory-scale columns continuously fed with acetate-amended artificial groundwater. Viral abundances were greatest in the influent section and decreased along the flow path. Acetate availability was important in influencing bacterial diversity, microbial interactions and viral abundance and community composition. The impact of acetate addition was most evident in the influent section of the columns. The increased relative abundance of Fe(III)-reducing bacteria coincided with an increase in viral abundance in areas of the columns exhibiting the most Fe(III) reduction. The genetic composition of viruses in these column sections also differed from the control column and distal sections of acetate-treated columns suggesting viral communities responded to biostimulated Fe(III)-bioreduction.
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http://dx.doi.org/10.1111/1462-2920.14566DOI Listing
June 2019

Spatial and Temporal Variation in Paralytic Shellfish Toxin Production by Benthic in a Freshwater New York Lake.

Toxins (Basel) 2019 01 15;11(1). Epub 2019 Jan 15.

Department of Chemistry, State University of New York College of Environmental Science and Forestry, Syracuse, NY 13210, USA.

Butterfield Lake is a mesotrophic lake in New York State where residents and pets have experienced unexplained health issues. (basionym ) was found at two of 15 sites in Butterfield Lake and analyzed for microcystins, anatoxins, cylindrospermopsins, and paralytic shellfish poisoning toxins (PSTs). Only PSTs and trace levels of anatoxin-a were detected in these samples. This is the first published report of PSTs within a New York State lake. To evaluate the environmental and temporal drivers leading to the observed toxicity, PST content at the two sites was examined in detail. There were distinct differences in the total PST content, filament nutrient, filament chlorophyll, and relationship to environmental drivers between the sites, as well as distinct differences in the total PST content measured using different analytical techniques. A multivariate model containing site, temperature, and filament chlorophyll explained 85% of the variation in PSTs observed over the growing season. This work emphasizes the importance of proper site selection and choice of analytical technique in the development of monitoring programs to protect lake users from the occurrence of benthic cyanobacteria toxins.
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http://dx.doi.org/10.3390/toxins11010044DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6356249PMC
January 2019

Minimum Information about an Uncultivated Virus Genome (MIUViG).

Nat Biotechnol 2019 01 17;37(1):29-37. Epub 2018 Dec 17.

Department of Physiology, Genetics and Microbiology, University of Alicante, Alicante, Spain.

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.
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http://dx.doi.org/10.1038/nbt.4306DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6871006PMC
January 2019

Cylindrospermopsis raciborskii Virus and host: genomic characterization and ecological relevance.

Environ Microbiol 2019 06 25;21(6):1942-1956. Epub 2018 Oct 25.

Department of Microbiology, University of Tennessee, Knoxville, TN, USA.

Cylindrospermopsis (Raphidiopsis) raciborskii is an invasive, filamentous, nitrogen-fixing cyanobacterium that forms frequent blooms in freshwater habitats. While viruses play key roles in regulating the abundance, production and diversity of their hosts in aquatic ecosystems, the role(s) of viruses in the ecology of C. raciborskii is almost unexplored. Progress in this field has been hindered by the absence of a characterized virus-host system in C. raciborskii. To bridge this gap, we sequenced the genome of CrV-01T, a previously isolated cyanosiphovirus, and its host, C. raciborskii strain Cr2010. Analyses suggest that CrV-01T represents a distinct clade of siphoviruses infecting, and perhaps lysogenizing, filamentous cyanobacteria. Its genome contains unique features that include an intact CRISPR array and a 12 kb inverted duplication. Evidence suggests CrV-01T recently gained the ability to infect Cr2010 and recently lost the ability to form lysogens. The cyanobacterial host contains a CRISPR-Cas system with CRISPR spacers matching protospacers within the inverted duplication of the CrV-01T genome. Examination of metagenomes demonstrates that viruses with high genetic identity to CrV-01T, but lacking the inverted duplication, are present in C. raciborskii blooms in Australia. The unique genomic features of the CrV/Cr2010 system offers opportunities to investigate in more detail virus-host interactions in an ecologically important bloom-forming cyanobacterium.
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http://dx.doi.org/10.1111/1462-2920.14425DOI Listing
June 2019

Diversity of Active Viral Infections within the Sphagnum Microbiome.

Appl Environ Microbiol 2018 12 15;84(23). Epub 2018 Nov 15.

Department of Microbiology, University of Tennessee, Knoxville, Tennessee, USA

-dominated peatlands play an important role in global carbon storage and represent significant sources of economic and ecological value. While recent efforts to describe microbial diversity and metabolic potential of the microbiome have demonstrated the importance of its microbial community, little is known about the viral constituents. We used metatranscriptomics to describe the diversity and activity of viruses infecting microbes within the peat bog. The vegetative portions of six plants were obtained from a peatland in northern Minnesota, and the total RNA was extracted and sequenced. Metatranscriptomes were assembled and contigs were screened for the presence of conserved virus marker genes. Using bacteriophage capsid protein gp23 as a marker for phage diversity, we identified 33 contigs representing undocumented phages that were active in the community at the time of sampling. Similarly, RNA-dependent RNA polymerase and the nucleocytoplasmic large DNA virus (NCLDV) major capsid protein were used as markers for single-stranded RNA (ssRNA) viruses and NCLDV, respectively. In total, 114 contigs were identified as originating from undescribed ssRNA viruses, 22 of which represent nearly complete genomes. An additional 64 contigs were identified as being from NCLDVs. Finally, 7 contigs were identified as putative virophage or polinton-like viruses. We developed co-occurrence networks with these markers in relation to the expression of potential-host housekeeping gene to predict virus-host relationships, identifying 13 groups. Together, our approach offers new tools for the identification of virus diversity and interactions in understudied clades and suggests that viruses may play a considerable role in the ecology of the microbiome.-dominated peatlands play an important role in maintaining atmospheric carbon dioxide levels by modifying conditions in the surrounding soil to favor the growth of over that of other plant species. This lowers the rate of decomposition and facilitates the accumulation of fixed carbon in the form of partially decomposed biomass. The unique environment produced by enriches for the growth of a diverse microbial consortia that benefit from and support the moss's growth, while also maintaining the hostile soil conditions. While a growing body of research has begun to characterize the microbial groups that colonize , little is currently known about the ecological factors that constrain community structure and define ecosystem function. Top-down population control by viruses is almost completely undescribed. This study provides insight into the significant viral influence on the microbiome and identifies new potential model systems to study virus-host interactions in the peatland ecosystem.
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http://dx.doi.org/10.1128/AEM.01124-18DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6238052PMC
December 2018

Viruses of Eukaryotic Algae: Diversity, Methods for Detection, and Future Directions.

Viruses 2018 09 11;10(9). Epub 2018 Sep 11.

The Department of Microbiology, The University of Tennessee, Knoxville, TN 37996, USA.

The scope for ecological studies of eukaryotic algal viruses has greatly improved with the development of molecular and bioinformatic approaches that do not require algal cultures. Here, we review the history and perceived future opportunities for research on eukaryotic algal viruses. We begin with a summary of the 65 eukaryotic algal viruses that are presently in culture collections, with emphasis on shared evolutionary traits (e.g., conserved core genes) of each known viral type. We then describe how core genes have been used to enable molecular detection of viruses in the environment, ranging from PCR-based amplification to community scale "-omics" approaches. Special attention is given to recent studies that have employed network-analyses of -omics data to predict virus-host relationships, from which a general bioinformatics pipeline is described for this type of approach. Finally, we conclude with acknowledgement of how the field of aquatic virology is adapting to these advances, and highlight the need to properly characterize new virus-host systems that may be isolated using preliminary molecular surveys. Researchers can approach this work using lessons learned from the virus system, which is not only the best characterized algal-virus system, but is also responsible for much of the foundation in the field of aquatic virology.
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http://dx.doi.org/10.3390/v10090487DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6165237PMC
September 2018

Seasonal Gene Expression and the Ecophysiological Implications of Toxic Microcystis aeruginosa Blooms in Lake Taihu.

Environ Sci Technol 2018 10 14;52(19):11049-11059. Epub 2018 Sep 14.

Department of Microbiology , University of Tennessee , Knoxville , Tennessee 37996 , United States.

Harmful cyanobacterial blooms represent an increasing threat to freshwater resources globally. Despite increased research, the physiological basis of how the dominant bloom-forming cyanobacteria, Microcystis spp., proliferate and then maintain high population densities through changing environmental conditions is poorly understood. In this study, we examined the transcriptional profiles of the microbial community in Lake Taihu, China at 9 stations sampled monthly from June to October in 2014. To target Microcystis populations, we collected metatranscriptomic data and mapped reads to the M. aeruginosa NIES 843 genome. Our results revealed significant temporal gene expression patterns, with many genes separating into either early or late bloom clusters. About one-third of genes observed from M. aeruginosa were differentially expressed between these two clusters. Conductivity and nutrient availability appeared to be the environmental factors most strongly associated with these temporal gene expression shifts. Compared with the early bloom season (June and July), genes involved in N and P transport, energy metabolism, translation, and amino acid biosynthesis were down-regulated during the later season (August to October). In parallel, genes involved in regulatory functions as well as transposases and the production of microcystin and extracellular polysaccharides were up-regulated in the later season. Our observation indicates an eco-physiological shift occurs within the Microcystis spp. transcriptome as cells move from the rapid growth of early summer to bloom maintenance in late summer and autumn.
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http://dx.doi.org/10.1021/acs.est.8b01066DOI Listing
October 2018