More Like this

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 taxa 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. 

   more » « less
2. 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. 

   more » « less
3. 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. 

   more » « less
4. Changes in Microbiome Activity and Sporadic Viral Infection Help Explain Observed Variability in Microcosm Studies

   https://doi.org/10.3389/fmicb.2022.809989  

   Pound, Helena L. ; Martin, Robbie M. ; Zepernick, Brittany N. ; Christopher, Courtney J. ; Howard, Sara M. ; Castro, Hector F. ; Campagna, Shawn R. ; Boyer, Gregory L. ; Bullerjahn, George S. ; Chaffin, Justin D. ; et al ( March 2022 , Frontiers in Microbiology)

   The environmental conditions experienced by microbial communities are rarely fully simulated in the laboratory. Researchers use experimental containers (“bottles”), where natural samples can be manipulated and evaluated. However, container-based methods are subject to “bottle effects”: changes that occur when enclosing the plankton community that are often times unexplained by standard measures like pigment and nutrient concentrations. We noted variability in a short-term, nutrient amendment experiment during a 2019 Lake Erie, Microcystis spp. bloom. We observed changes in heterotrophic bacteria activity (transcription) on a time-frame consistent with a response to experimental changes in nutrient availability, demonstrating how the often overlooked microbiome of cyanobacterial blooms can be altered. Samples processed at the time of collection (T0) contained abundant transcripts from Bacteroidetes, which reduced in abundance during incubation in all bottles, including controls. Significant biological variability in the expression of Microcystis -infecting phage was observed between replicates, with phosphate-amended treatments showing a 10-fold variation. The expression patterns of Microcystis -infecting phage were significantly correlated with ∼35% of Microcystis -specific functional genes and ∼45% of the cellular-metabolites measured across the entire microbial community, suggesting phage activity not only influenced Microcystis dynamics, but the biochemistry of the microbiome. Our observations demonstrate how natural heterogeneity among replicates can be harnessed to provide further insight on virus and host ecology. 

   more » « less
5. Isolation and Characterization of Rhizophydiales (Chytridiomycota), Obligate Parasites of Planktothrix agardhii in a Laurentian Great Lakes Embayment

   https://doi.org/10.1128/aem.02308-20  

   McKindles, Katelyn M. ; Jorge, Alejandro N. ; McKay, R. Michael ; Davis, Timothy W. ; Bullerjahn, George S. ( January 2021 , Applied and Environmental Microbiology)

   Stams, Alfons J. (Ed.)

   ABSTRACT Planktothrix agardhii dominates the cyanobacterial harmful algal bloom community in Sandusky Bay, Lake Erie (USA), from May through September. This filamentous cyanobacterium is host to a known obligate parasite, the chytrid Rhizophydium sp. During the 2018 bloom season, by utilizing dilution and single-filament isolation techniques, 7 chytrid and 12 P. agardhii strains were isolated from Sandusky Bay. These 7 chytrids and a selection of P. agardhii hosts were then characterized with respect to infection rates. Infections by the isolated chytrids were specific to Planktothrix planktonic species and were not found on other filamentous cyanobacterial taxa present in the bay ( Aphanizomenon sp. and Cuspidothrix sp.). Even among the potential P. agardhii host strains, individual chytrid isolates had different degrees of infectivity and showed preferences for different host isolates, suggesting possible ecological partitioning even within the same sample population. When mechanisms of chytrid pathogenesis were examined, the zoospores displayed a swarming pattern to attack and fracture the host filament and create new infection sites at the trichome termini. Infections by these parasitic chytrids also led to a release of intracellular microcystin toxins from the hosts. Additionally, infections were dependent on medium type, highlighting the importance of medium choice for experimental outcomes. Media in which chytrid swarming was observed closely matched the ionic strength of the natural environment. Understanding pathogenesis by fungal parasites will assist future efforts to determine environmental factors favoring loss mechanisms for Planktothrix agardhii -dominated blooms. IMPORTANCE Whereas many studies have focused on the factors contributing to the establishment and persistence of cyanobacterial harmful algal blooms (cHABs), few studies have examined bloom pathogenesis. Chytrid fungi infect cyanobacteria and stimulate food web interactions through manipulation of previously hard-to-digest filaments and the release of nutrients to support heterotrophic microbes. Specifically, chytrids infective for filamentous Planktothrix agardhii exhibit a species-specific infection that fragments trichomes into shorter units that can be consumed more easily by grazers. Chytrid zoospores also serve as a high-quality food source for the lower food web. Understanding host-pathogen relationships and mechanisms of pathogenesis on cyanobacteria will be necessary to effectively model the ecology of cHABs. 

   more » « less