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1. Uptake of Phytoplankton-Derived Carbon and Cobalamins by Novel Acidobacteria Genera in Microcystis Blooms Inferred from Metagenomic and Metatranscriptomic Evidence

   https://doi.org/10.1128/aem.01803-21  

   Smith, Derek J. ; Kharbush, Jenan J. ; Kersten, Roland D. ; Dick, Gregory J. ( July 2022 , Applied and Environmental Microbiology)

   Glass, Jennifer B. (Ed.)

   ABSTRACT Interactions between bacteria and phytoplankton can influence primary production, community composition, and algal bloom development. However, these interactions are poorly described for many consortia, particularly for freshwater bloom-forming cyanobacteria. Here, we assessed the gene content and expression of two uncultivated Acidobacteria from Lake Erie Microcystis blooms. These organisms were targeted because they were previously identified as important catalase producers in Microcystis blooms, suggesting that they protect Microcystis from H 2 O 2 . Metatranscriptomics revealed that both Acidobacteria transcribed genes for uptake of organic compounds that are known cyanobacterial products and exudates, including lactate, glycolate, amino acids, peptides, and cobalamins. Expressed genes for amino acid metabolism and peptide transport and degradation suggest that use of amino acids and peptides by Acidobacteria may regenerate nitrogen for cyanobacteria and other organisms. The Acidobacteria genomes lacked genes for biosynthesis of cobalamins but expressed genes for its transport and remodeling. This indicates that the Acidobacteria obtained cobalamins externally, potentially from Microcystis , which has a complete gene repertoire for pseudocobalamin biosynthesis; expressed them in field samples; and produced pseudocobalamin in axenic culture. Both Acidobacteria were detected in Microcystis blooms worldwide. Together, the data support the hypotheses that uncultured and previously unidentified Acidobacteria taxamore »exchange metabolites with phytoplankton during harmful cyanobacterial blooms and influence nitrogen available to phytoplankton. Thus, novel Acidobacteria may play a role in cyanobacterial physiology and bloom development. IMPORTANCE Interactions between heterotrophic bacteria and phytoplankton influence competition and successions between phytoplankton taxa, thereby influencing ecosystem-wide processes such as carbon cycling and algal bloom development. The cyanobacterium Microcystis forms harmful blooms in freshwaters worldwide and grows in buoyant colonies that harbor other bacteria in their phycospheres. Bacteria in the phycosphere and in the surrounding community likely influence Microcystis physiology and ecology and thus the development of freshwater harmful cyanobacterial blooms. However, the impacts and mechanisms of interaction between bacteria and Microcystis are not fully understood. This study explores the mechanisms of interaction between Microcystis and uncultured members of its phycosphere in situ with population genome resolution to investigate the cooccurrence of Microcystis and freshwater Acidobacteria in blooms worldwide.« less
2. 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
3. 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.
4. 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)

   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.
5. Individual Microcystis colonies harbour distinct bacterial communities that differ by Microcystis oligotype and with time

   https://doi.org/10.1111/1462-2920.15514  

   Smith, Derek J. ; Tan, James Y. ; Powers, McKenzie A. ; Lin, Xiaoxia N. ; Davis, Timothy W. ; Dick, Gregory J. ( April 2021 , Environmental Microbiology)

   Interactions between bacteria and phytoplankton in the phycosphere have impacts at the scale of whole ecosystems, including the development of harmful algal blooms. The cyanobacteriumMicrocystiscauses toxic blooms that threaten freshwater ecosystems and human health globally.Microcystisgrows in colonies that harbour dense assemblages of other bacteria, yet the taxonomic composition of these phycosphere communities and the nature of their interactions withMicrocystisare not well characterized. To identify the taxa and compositional variance withinMicrocystisphycosphere communities, we performed 16S rRNA V4 region amplicon sequencing on individualMicrocystiscolonies collected biweekly via high‐throughput droplet encapsulation during a western Lake Erie cyanobacterial bloom. TheMicrocystisphycosphere communities were distinct from microbial communities in whole water and bulk phytoplankton seston in western Lake Erie but lacked ‘core’ taxa found across all colonies. However, dissimilarity in phycosphere community composition correlated with sampling date and theMicrocystis16S rRNA oligotype. Several taxa in the phycosphere were specific to and conserved withMicrocystisof a single oligotype or sampling date. Together, this suggests that physiological differences betweenMicrocystisstrains, temporal changes in strain phenotypes, and the composition of seeding communities may impact community composition of theMicrocystisphycosphere.