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1. 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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2. Harmful algal blooms and cyanotoxins in Lake Amatitlán, Guatemala, coincided with ancient Maya occupation in the watershed

   https://doi.org/10.1073/pnas.2109919118  

   Waters, Matthew Neal; Brenner, Mark; Curtis, Jason Hilleary; Romero-Oliva, Claudia Suseth; Dix, Margaret; Cano, Manuel (November 2021, Proceedings of the National Academy of Sciences)

   Human-induced deforestation and soil erosion were environmental stressors for the ancient Maya of Mesoamerica. Furthermore, intense, periodic droughts during the Terminal Classic Period, ca. Common Era 830 to 950, have been documented from lake sediment cores and speleothems. Today, lakes worldwide that are surrounded by dense human settlement and intense riparian land use often develop algae/cyanobacteria blooms that can compromise water quality by depleting oxygen and producing toxins. Such environmental impacts have rarely been explored in the context of ancient Maya settlement. We measured nutrients, biomarkers for cyanobacteria, and the cyanotoxin microcystin in a sediment core from Lake Amatitlán, highland Guatemala, which spans the last ∼2,100 y. The lake is currently hypereutrophic and characterized by high cyanotoxin concentrations from persistent blooms of the cyanobacterium Microcystis aeruginosa . Our paleolimnological data show that harmful cyanobacteria blooms and cyanotoxin production occurred during periods of ancient Maya occupation. Highest prehistoric concentrations of cyanotoxins in the sediment coincided with alterations of the water system in the Maya city of Kaminaljuyú, and changes in nutrient stoichiometry and maximum cyanobacteria abundance were coeval with times of greatest ancient human populations in the watershed. These prehistoric episodes of cyanobacteria proliferation and cyanotoxin production rivaled modern conditions in the lake, with respect to both bloom magnitude and toxicity. This suggests that pre-Columbian Maya occupation of the Lake Amatitlán watershed negatively impacted water potability. Prehistoric cultural eutrophication indicates that human-driven nutrient enrichment of water bodies is not an exclusively modern phenomenon and may well have been a stressor for the ancient Maya. 

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3. Bacterial community and cyanotoxin gene distribution of the Winam Gulf, Lake Victoria, Kenya

   https://doi.org/10.1111/1758-2229.13297  

   Brown, Katelyn M; Barker, Katelyn B; Wagner, Ryan S; Ward, Christopher S; Sitoki, Lewis; Njiru, James; Omondi, Reuben; Achiya, James; Getabu, Albert; McKay, R Michael; et al (June 2024, Environmental Microbiology Reports)

   Abstract The Winam Gulf (Kenya) is frequently impaired by cyanobacterial harmful algal blooms (cHABs) due to inadequate wastewater treatment and excess agricultural nutrient input. While phytoplankton in Lake Victoria have been characterized using morphological criteria, our aim is to identify potential toxin‐producing cyanobacteria using molecular approaches. The Gulf was sampled over two successive summer seasons, and 16S and 18S ribosomal RNA gene sequencing was performed. Additionally, key genes involved in production of cyanotoxins were examined by quantitative PCR. Bacterial communities were spatially variable, forming distinct clusters in line with regions of the Gulf. Taxa associated with diazotrophy were dominant near Homa Bay. On the eastern side, samples exhibited elevatedcyrAabundances, indicating genetic capability of cylindrospermopsin synthesis. Indeed, near the Nyando River mouth in 2022,cyrAexceeded 10 million copies L⁻¹where there were more than 6000Cylindrospermopsisspp. cells mL⁻¹. In contrast, the southwestern region had elevatedmcyEgene (microcystin synthesis) detections near Homa Bay whereMicrocystisandDolichospermumspp. were observed. These findings show that within a relatively small embayment, composition and toxin synthesis potential of cHABs can vary dramatically. This underscores the need for multifaceted management approaches and frequent cyanotoxin monitoring to reduce human health impacts. 

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4. Production of Cyanotoxins by Microcystis aeruginosa Mediates Interactions with the Mixotrophic Flagellate Cryptomonas

   https://doi.org/10.3390/toxins11040223  

   Princiotta, Sarah DeVaul; Hendricks, Susan P.; White, David S. (April 2019, Toxins)

   Eutrophication of inland waters is expected to increase the frequency and severity of harmful algal blooms (HABs). Toxin-production associated with HABs has negative effects on human health and aquatic ecosystem functioning. Despite evidence that flagellates can ingest toxin-producing cyanobacteria, interactions between members of the microbial loop are underestimated in our understanding of the food web and algal bloom dynamics. Physical and allelopathic interactions between a mixotrophic flagellate (Cryptomonas sp.) and two strains of a cyanobacteria (Microcystis aeruginosa) were investigated in a full-factorial experiment in culture. The maximum population growth rate of the mixotroph (0.25 day−1) occurred during incubation with filtrate from toxic M. aeruginosa. Cryptomonas was able to ingest toxic and non-toxic M. aeruginosa at maximal rates of 0.5 and 0.3 cells day−1, respectively. The results establish that although Cryptomonas does not derive benefits from co-incubation with M. aeruginosa, it may obtain nutritional supplement from filtrate. We also provide evidence of a reduction in cyanotoxin concentration (microcystin-LR) when toxic M. aeruginosa is incubated with the mixotroph. Our work has implications for “trophic upgrading” within the microbial food web, where cyanobacterivory by nanoflagellates may improve food quality for higher trophic levels and detoxify secondary compounds. 

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5. Thermal acclimation influences the growth and toxin production of freshwater cyanobacteria

   https://doi.org/10.1002/lol2.10197  

   Layden, Tamara J.; Kremer, Colin T.; Brubaker, Delaney L.; Kolk, Maeve A.; Trout‐Haney, Jessica V.; Vasseur, David A.; Fey, Samuel B. (May 2021, Limnology and Oceanography Letters)

   Abstract Understanding how altered temperature regimes affect harmful cyanobacterial bloom formation is essential for managing aquatic ecosystems amidst ongoing climate warming. This is difficult because algal performance can depend on both current and past environments, as plastic physiological changes (acclimation) may lag behind environmental change. Here, we investigate how temperature variation on sub‐weekly timescales affects population growth and toxin production given acclimation. We studied four ecologically important freshwater cyanobacterial strains under low‐ and high‐nutrient conditions, measuring population growth rate after acclimation and new exposure to a range of temperatures. Cold‐acclimated populations (15.7°C) outperformed fully acclimated populations (held in constant conditions) across 65% of thermal environments, while hot‐acclimated populations (35.7–42.6°C) underperformed across 75% of thermal environments. Over a 5‐day period, cold‐acclimatedMicrocystis aeruginosaproduced ~2.5‐fold more microcystin than hot‐acclimated populations experiencing the same temperature perturbation. Our results suggest that thermal variation and physiology interact in underappreciated ways to influence cyanobacterial growth, toxin production, and likely bloom formation. 

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