More Like this

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 ,more »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.« less
2. Genomic signatures of Lake Erie bacteria suggest interaction in the Microcystis phycosphere

   https://doi.org/10.1371/journal.pone.0257017  

   Hoke, Alexa K. ; Reynoso, Guadalupe ; Smith, Morgan R. ; Gardner, Malia I. ; Lockwood, Dominique J. ; Gilbert, Naomi E. ; Wilhelm, Steven W. ; Becker, Isabella R. ; Brennan, Grant J. ; Crider, Katherine E. ; et al ( September 2021 , PLOS ONE)

   Humbert, Jean-François (Ed.)

   Microbial interactions in harmful algal bloom (HAB) communities have been examined in marine systems, but are poorly studied in fresh waters. To investigate HAB-microbe interactions, we isolated bacteria with close associations to bloom-forming cyanobacteria, Microcystis spp., during a 2017 bloom in the western basin of Lake Erie. The genomes of five isolates ( Exiguobacterium sp. JMULE1, Enterobacter sp. JMULE2, Deinococcus sp. JMULE3, Paenibacillus sp. JMULE4, and Acidovorax sp. JMULE5.) were sequenced on a PacBio Sequel system. These genomes ranged in size from 3.1 Mbp ( Exiguobacterium sp. JMULE1) to 5.7 Mbp ( Enterobacter sp. JMULE2). The genomes were analyzed for genes relating to critical metabolic functions, including nitrogen reduction and carbon utilization. All five of the sequenced genomes contained genes that could be used in potential signaling and nutrient exchange between the bacteria and cyanobacteria such as Microcystis . Gene expression signatures of algal-derived carbon utilization for two isolates were identified in Microcystis blooms in Lake Erie and Lake Tai ( Taihu ) at low levels, suggesting these organisms are active and may have a functional role during Microcystis blooms in aggregates, but were largely missing from whole water samples. These findings build on the growing evidence that the bacterialmore »microbiome associated with bloom-forming algae have the functional potential to contribute to nutrient exchange within bloom communities and interact with important bloom formers like Microcystis .« less
3. Feedback Regulation between Aquatic Microorganisms and the Bloom-Forming Cyanobacterium Microcystis aeruginosa

   https://doi.org/10.1128/AEM.01362-19  

   Zhang, Meng ; Lu, Tao ; Paerl, Hans W. ; Chen, Yiling ; Zhang, Zhenyan ; Zhou, Zhigao ; Qian, Haifeng ; Drake, Harold L. ( November 2019 , Applied and Environmental Microbiology)

   ABSTRACT The frequency and intensity of cyanobacterial blooms are increasing worldwide. Interactions between toxic cyanobacteria and aquatic microorganisms need to be critically evaluated to understand microbial drivers and modulators of the blooms. In this study, we applied 16S/18S rRNA gene sequencing and metabolomics analyses to measure the microbial community composition and metabolic responses of the cyanobacterium Microcystis aeruginosa in a coculture system receiving dissolved inorganic nitrogen and phosphorus (DIP) close to representative concentrations in Lake Taihu, China. M. aeruginosa secreted alkaline phosphatase using a DIP source produced by moribund and decaying microorganisms when the P source was insufficient. During this process, M. aeruginosa accumulated several intermediates in energy metabolism pathways to provide energy for sustained high growth rates and increased intracellular sugars to enhance its competitive capacity and ability to defend itself against microbial attack. It also produced a variety of toxic substances, including microcystins, to inhibit metabolite formation via energy metabolism pathways of aquatic microorganisms, leading to a negative effect on bacterial and eukaryotic microbial richness and diversity. Overall, compared with the monoculture system, the growth of M. aeruginosa was accelerated in coculture, while the growth of some cooccurring microorganisms was inhibited, with the diversity and richness of eukaryoticmore »microorganisms being more negatively impacted than those of prokaryotic microorganisms. These findings provide valuable information for clarifying how M. aeruginosa can potentially modulate its associations with other microorganisms, with ramifications for its dominance in aquatic ecosystems. IMPORTANCE We measured the microbial community composition and metabolic responses of Microcystis aeruginosa in a microcosm coculture system receiving dissolved inorganic nitrogen and phosphorus (DIP) close to the average concentrations in Lake Taihu. In the coculture system, DIP is depleted and the growth and production of aquatic microorganisms can be stressed by a lack of DIP availability. M. aeruginosa could accelerate its growth via interactions with specific cooccurring microorganisms and the accumulation of several intermediates in energy metabolism-related pathways. Furthermore, M. aeruginosa can decrease the carbohydrate metabolism of cooccurring aquatic microorganisms and thus disrupt microbial activities in the coculture. This also had a negative effect on bacterial and eukaryotic microbial richness and diversity. Microcystin was capable of decreasing the biomass of total phytoplankton in aquatic microcosms. Overall, compared to the monoculture, the growth of total aquatic microorganisms is inhibited, with the diversity and richness of eukaryotic microorganisms being more negatively impacted than those of prokaryotic microorganisms. The only exception is M. aeruginosa in the coculture system, whose growth was accelerated.« less
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.
5. 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 inmore »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.« less