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

   https://doi.org/10.3390/toxins13010047  

   Barnard, Malcolm A. ; Chaffin, Justin D. ; Plaas, Haley E. ; Boyer, Gregory L. ; Wei, Bofan ; Wilhelm, Steven W. ; Rossignol, Karen L. ; Braddy, Jeremy S. ; Bullerjahn, George S. ; Bridgeman, Thomas B. ; et al ( January 2021 , Toxins)

   null (Ed.)

   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 Microcystis spp. bloom in Maumee Bay that extends throughout the western basin, and a Planktothrix 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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2. Eutrophication mediates rapid clonal evolution in Daphnia pulicaria

   https://doi.org/10.1111/fwb.13303  

   Chislock, Michael F. ; Kaul, RajReni B. ; Durham, Kristin A. ; Sarnelle, Orlando ; Wilson, Alan E. ( April 2019 , Freshwater Biology)

   Laboratory studies have revealed thatDaphniaspecies can evolve to tolerate toxic cyanobacteria in the diet. Specifically,Daphniafrom eutrophic lakes where cyanobacteria are common tend to have higher growth rates and survival when fed toxic cyanobacteria than populations from oligotrophic environments with low abundance of cyanobacteria.

   We conducted an in‐lake mesocosm (i.e. limnocorral) experiment during the autumn of 2009 to assess the effects of nutrient enrichment on clonal evolution inDaphnia pulicaria. As nutrient enrichment often favours grazing‐resistant cyanobacteria, we hypothesised that fertilisation would influence the genotypic composition ofD. pulicariathat vary in tolerance to cyanobacteria. Mesocosms were fertilised to manipulate phytoplankton and cyanobacterial abundance and concentrations of a cyanobacterial toxin (microcystin). Thus, half of the mesocosms were high‐nutrient and half were low‐nutrient. We then stocked half of the mesocosms with a mixture of six genetically‐distinctD. pulicariagenotypes (three genotypes from oligotrophic lakes and three from eutrophic lakes) leaving half of the mesocosmsDaphnia‐free to assess grazing effects, using a fully factorial design.

   When compared to the low nutrient treatment, high nutrient mesocosms had nearly five‐fold higher chlorophyllaconcentrations, eight‐fold higher cyanobacterial dry biomass, and three‐fold higher microcystin levels at the start of the experiment. In contrast, low nutrient mesocosms had phytoplankton concentrations typical of mesotrophic lakes.

   Fertilisation strongly affectedDaphniagenetic diversity in the mesocosms. FinalDaphniagenotype diversity in the mesocosms with low‐cyanobacteria (richness = 5.83, Shannon–Weiner index = 1.55, evenness = 0.88) was similar to the initial stocked diversity (richness = 5.50, Shannon–Weiner index = 1.48, evenness = 0.87). In contrast, final diversity in fertilised mesocosms with high cyanobacteria was greatly reduced (richness = 2, Shannon–Weiner index = 0.17), with oneDaphniagenotype that originated from the most‐eutrophic lake being highly dominant (evenness = 0.25). Thus, eutrophication mediated strong clonal selection of a cyanobacteria‐tolerantDaphniagenotype over just 10 weeks.

   By the end of the experiment,Daphniasignificantly reduced phytoplankton biomass in the high‐nutrient, but not in the low‐nutrient treatment. This difference in effect size was largely driven by the five‐fold higher initial phytoplankton biomass in the high‐nutrient treatment. Thus, the ability ofDaphniato reduce phytoplankton biomass in eutrophic lakes may be driven more so by the abundance of planktivorous fishes, as opposed to the prevalence of cyanobacteria and their associated toxins.

    

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3. Nitrogen flux into metabolites and microcystins changes in response to different nitrogen sources in Microcystis aeruginosaNIES ‐843

   https://doi.org/10.1111/1462-2920.15032  

   Krausfeldt, Lauren E. ; Farmer, Abigail T. ; Castro, Hector F. ; Boyer, Gregory L. ; Campagna, Shawn R. ; Wilhelm, Steven W. ( May 2020 , Environmental Microbiology)

   The over‐enrichment of nitrogen (N) in the environment has contributed to severe and recurring harmful cyanobacterial blooms, especially by the non‐N₂‐fixingMicrocystisspp. 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 inMicrocystis aeruginosaNIES‐843. Global metabolic changes were driven by both N speciation and diel cycling. Tracing¹⁵N‐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,¹⁵N 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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4. Metagenomic and Metatranscriptomic Insights into Population Diversity of Microcystis Blooms: Spatial and Temporal Dynamics of mcy Genotypes, Including a Partial Operon That Can Be Abundant and Expressed

   https://doi.org/10.1128/aem.02464-21  

   Yancey, Colleen E. ; Smith, Derek J. ; Den Uyl, Paul A. ; Mohamed, Osama G. ; Yu, Fengan ; Ruberg, Steven A. ; Chaffin, Justin D. ; Goodwin, Kelly D. ; Tripathi, Ashootosh ; Sherman, David H. ; et al ( May 2022 , Applied and Environmental Microbiology)

   Rudi, Knut (Ed.)

   ABSTRACT Cyanobacterial harmful algal blooms (cyanoHABs) degrade freshwater ecosystems globally. Microcystis aeruginosa often dominates cyanoHABs and produces microcystin (MC), a class of hepatotoxins that poses threats to human and animal health. Microcystin toxicity is influenced by distinct structural elements across a diversity of related molecules encoded by variant mcy operons. However, the composition and distribution of mcy operon variants in natural blooms remain poorly understood. Here, we characterized the variant composition of mcy genes in western Lake Erie Microcystis blooms from 2014 and 2018. Sampling was conducted across several spatial and temporal scales, including different bloom phases within 2014, extensive spatial coverage on the same day (2018), and frequent, autonomous sampling over a 2-week period (2018). Mapping of metagenomic and metatranscriptomic sequences to reference sequences revealed three Microcystis mcy genotypes: complete (all genes present [ mcyA–J ]), partial (truncated mcyA , complete mcyBC , and missing mcyD–J ), and absent (no mcy genes). We also detected two different variants of mcyB that may influence the production of microcystin congeners. The relative abundance of these genotypes was correlated with pH and nitrate concentrations. Metatranscriptomic analysis revealed that partial operons were, at times, the most abundant genotype and expressed in situ , suggesting the potential biosynthesis of truncated products. Quantification of genetic divergence between genotypes suggests that the observed strains are the result of preexisting heterogeneity rather than de novo mutation during the sampling period. Overall, our results show that natural Microcystis populations contain several cooccurring mcy genotypes that dynamically shift in abundance spatiotemporally via strain succession and likely influence the observed diversity of the produced congeners. IMPORTANCE Cyanobacteria are responsible for producing microcystins (MCs), a class of potent and structurally diverse toxins, in freshwater systems around the world. While microcystins have been studied for over 50 years, the diversity of their chemical forms and how this variation is encoded at the genetic level remain poorly understood, especially within natural populations of cyanobacterial harmful algal blooms (cyanoHABs). Here, we leverage community DNA and RNA sequences to track shifts in mcy genes responsible for producing microcystin, uncovering the relative abundance, expression, and variation of these genes. We studied this phenomenon in western Lake Erie, which suffers annually from cyanoHAB events, with impacts on drinking water, recreation, tourism, and commercial fishing. 

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5. Heterotrophic Bacteria Dominate Catalase Expression during Microcystis Blooms

   https://doi.org/10.1128/aem.02544-21  

   Smith, Derek J. ; Berry, Michelle A. ; Cory, Rose M. ; Johengen, Thomas H. ; Kling, George W. ; Davis, Timothy W. ; Dick, Gregory J. ( July 2022 , Applied and Environmental Microbiology)

   Nojiri, Hideaki (Ed.)

   ABSTRACT In the oligotrophic oceans, key autotrophs depend on “helper” bacteria to reduce oxidative stress from hydrogen peroxide (H 2 O 2 ) in the extracellular environment. H 2 O 2 is also a ubiquitous stressor in freshwaters, but the effects of H 2 O 2 on autotrophs and their interactions with bacteria are less well understood in freshwaters. Naturally occurring H 2 O 2 in freshwater systems is proposed to impact the proportion of microcystin-producing (toxic) and non-microcystin-producing (nontoxic) Microcystis in blooms, which influences toxin concentrations and human health impacts. However, how different strains of Microcystis respond to naturally occurring H 2 O 2 concentrations and the microbes responsible for H 2 O 2 decomposition in freshwater cyanobacterial blooms are unknown. To address these knowledge gaps, we used metagenomics and metatranscriptomics to track the presence and expression of genes for H 2 O 2 decomposition by microbes during a cyanobacterial bloom in western Lake Erie in the summer of 2014. katG encodes the key enzyme for decomposing extracellular H 2 O 2 but was absent in most Microcystis cells. katG transcript relative abundance was dominated by heterotrophic bacteria. In axenic Microcystis cultures, an H 2 O 2 scavenger (pyruvate) significantly improved growth rates of one toxic strain while other toxic and nontoxic strains were unaffected. These results indicate that heterotrophic bacteria play a key role in H 2 O 2 decomposition in Microcystis blooms and suggest that their activity may affect the fitness of some Microcystis strains and thus the strain composition of Microcystis blooms but not along a toxic versus nontoxic dichotomy. IMPORTANCE Cyanobacterial harmful algal blooms (CHABs) threaten freshwater ecosystems globally through the production of toxins. Toxin production by cyanobacterial species and strains during CHABs varies widely over time and space, but the ecological drivers of the succession of toxin-producing species remain unclear. Hydrogen peroxide (H 2 O 2 ) is ubiquitous in natural waters, inhibits microbial growth, and may determine the relative proportions of Microcystis strains during blooms. However, the mechanisms and organismal interactions involved in H 2 O 2 decomposition are unexplored in CHABs. This study shows that some strains of bloom-forming freshwater cyanobacteria benefit from detoxification of H 2 O 2 by associated heterotrophic bacteria, which may impact bloom development. 

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