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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. Genome evolution and host‐microbiome shifts correspond with intraspecific niche divergence within harmful algal bloom‐forming Microcystis aeruginosa

   https://doi.org/10.1111/mec.15198  

   Jackrel, Sara L. ; White, Jeffrey D. ; Evans, Jacob T. ; Buffin, Kyle ; Hayden, Kristen ; Sarnelle, Orlando ; Denef, Vincent J. ( August 2019 , Molecular Ecology)

   Intraspecific niche divergence is an important driver of species range, population abundance and impacts on ecosystem functions. Genetic changes are the primary focus when studying intraspecific divergence; however, the role of ecological interactions, particularly host‐microbiome symbioses, is receiving increased attention. The relative importance of these evolutionary and ecological mechanisms has seen only limited evaluation. To address this question, we usedMicrocystis aeruginosa, the globally distributed cyanobacterium that dominates freshwater harmful algal blooms. These blooms have been increasing in occurrence and intensity worldwide, causing major economic and ecological damages. We evaluated 46 isolates ofM. aeruginosaand their microbiomes,collected from 14 lakes in Michigan, USA, that vary over 20‐fold in phosphorus levels, the primary limiting nutrient in freshwater systems. Genomes ofM. aeruginosadiverged along this phosphorus gradient in genomic architecture and protein functions. Fitness in low‐phosphorus lakes corresponded with additional shifts withinM. aeruginosaincluding genome‐wide reductions in nitrogen use, an expansion of phosphorus assimilation genes and an alternative life history strategy of nonclonal colony formation. In addition to host shifts, despite culturing in common‐garden conditions, host‐microbiomes diverged along the gradient in taxonomy, but converged in function with evidence of metabolic interdependence between the host and its microbiome. Divergence corresponded with a physiological trade‐off between fitness in low‐phosphorus environments and growth rate in phosphorus‐rich conditions. Co‐occurrence of genotypes adapted to different nutrient environments in phosphorus‐rich lakes may have critical implications for understanding howM. aeruginosablooms persist after initial nutrient depletion. Ultimately, we demonstrate that the intertwined effects of genome evolution, host life history strategy and ecological interactions between a host and its microbiome correspond with an intraspecific niche shift with important implications for whole ecosystem function.

    

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3. The microbiome of the pelagic tunicate Dolioletta gegenbauri : A potential link between the grazing and microbial food web

   https://doi.org/10.1111/mec.16668  

   Pereira, Tiago J. ; Walters, Tina L. ; El‐Shaffey, Hisham M. ; Bik, Holly M. ; Frischer, Marc E. ( September 2022 , Molecular Ecology)

   Bloom‐forming gelatinous zooplankton occur circumglobally and significantly influence the structure of pelagic marine food webs and biogeochemical cycling through interactions with microbial communities. During bloom conditions especially, gelatinous zooplankton are keystone taxa that help determine the fate of primary production, nutrient remineralization, and carbon export. Using the pelagic tunicateDolioletta gegenbaurias a model system for gelatinous zooplankton, we carried out a laboratory‐based feeding experiment to investigate the potential ecosystem impacts of doliolid gut microbiomes and microbial communities associated with doliolid faecal pellets and the surrounding seawater. Metabarcoding targeting Bacteria and Archaea 16S rRNA genes/Archaea) and qPCR approaches were used to characterize microbiome assemblages. Comparison between sample types revealed distinct patterns in microbial diversity and biomass that were replicable across experiments. These observations support the hypothesis that through their presence and trophic activity, doliolids influence the structure of pelagic food webs and biogeochemical cycling in subtropical continental shelf systems where tunicate blooms are common. Bacteria associated with starved doliolids (representative of the resident gut microbiome) possessed distinct low‐biomass and low‐diversity microbial assemblages, suggesting that the doliolid microbiome is optimized to support a detrital trophic mode. Bacterial generaPseudoalteromomasandShimiawere the most abundant potential core microbiome taxa, similar to patterns observed in other marine invertebrates. Exploratory bioinformatic analyses of predicted functional genes suggest that doliolids, via their interactions with bacterial communities, may affect important biogeochemical processes including nitrogen, sulphur, and organic matter cycling.

    

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4. Sulfolipid substitution ratios of Microcystis aeruginosa and planktonic communities as an indicator of phosphorus limitation in Lake Erie

   https://doi.org/10.1002/lno.12333  

   Martin, Robbie M. ; Denney, Maddie K. ; Pound, Helena L. ; Chaffin, Justin D. ; Bullerjahn, George S. ; McKay, R. Michael L. ; Zastepa, Arthur ; Jones, Katarina A. ; Castro, Hector F. ; Campagna, Shawn R. ; et al ( March 2023 , Limnology and Oceanography)

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

    

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5. Global co‐occurrence of methanogenic archaea and methanotrophic bacteria in Microcystis aggregates

   https://doi.org/10.1111/1462-2920.15691  

   Li, Chuang ; Hambright, K. David ; Bowen, Hannah G. ; Trammell, Majoi A. ; Grossart, Hans‐Peter ; Burford, Michele A. ; Hamilton, David P. ; Jiang, Helong ; Latour, Delphine ; Meyer, Elisabeth I. ; et al ( August 2021 , Environmental Microbiology)

   Global warming and eutrophication contribute to the worldwide increase in cyanobacterial blooms, and the level of cyanobacterial biomass is strongly associated with rises in methane emissions from surface lake waters. Hence, methane‐metabolizing microorganisms may be important for modulating carbon flow in cyanobacterial blooms. Here, we surveyed methanogenic and methanotrophic communities associated with floatingMicrocystisaggregates in 10 lakes spanning four continents, through sequencing of 16S rRNA and functional marker genes. Methanogenic archaea (mainlyMethanoregulaandMethanosaeta) were detectable in 5 of the 10 lakes and constituted the majority (~50%–90%) of the archaeal community in these lakes. Three of the 10 lakes contained relatively more abundant methanotrophs than the other seven lakes, with the methanotrophic generaMethyloparacoccus,Crenothrix, and an uncultured species related toMethylobacterdominating and nearly exclusively found in each of those three lakes. These three are among the five lakes in which methanogens were observed. Operational taxonomic unit (OTU) richness and abundance of methanotrophs were strongly positively correlated with those of methanogens, suggesting that their activities may be coupled. TheseMicrocystis‐aggregate‐associated methanotrophs may be responsible for a hitherto overlooked sink for methane in surface freshwaters, and their co‐occurrence with methanogens sheds light on the methane cycle in cyanobacterial aggregates.

    

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