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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 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. 

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2. 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)

   Summary 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. 

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3. Dual phosphorus and nitrogen nutrient reduction will be more effective than a phosphorus‐only reduction in mitigating diatom and cyanobacterial blooms in Lake Erie, USA –Canada

   https://doi.org/10.1002/lno.12719  

   Paerl, Hans W; Chaffin, Justin D; Cheshire, Jack H; Plaas, Haley E; Barnard, Malcolm A; Goerlitz, Lillian B; Braddy, Jeremy S; Sabo, Alexandrea; Nelson, Leah M; Yue, Lindsay (November 2024, Limnology and Oceanography)

   Abstract Lake Erie, USA–Canada, plays an important ecological and socioeconomic role but has suffered from chronic eutrophication. In particular, western Lake Erie (WLE) is the site of harmful algal blooms (HABs) which are suspected of being driven by excessive nutrient (phosphorus (P) and nitrogen (N)) inputs. During 2022 and 2023, in situ nutrient dilution and addition bioassays were conducted at a WLE bloom‐impacted location to investigate whether a nutrient reduction regime would be effective in limiting phytoplankton growth during the June diatom‐dominated spring blooms and August cyanobacteria‐dominated summer blooms. The primary objectives of this experiment were to (1) Determine if a proposed 40% P‐alone reduction would effectively reduce phytoplankton growth and mitigate blooms and (2) assess whether reductions in both P and N are more effective in controlling phytoplankton biomass than exclusive reductions in either N or P. Samples were analyzed for nutrient concentrations and growth rate responses for specific algal groups, utilizing diagnostic (for major algal groups) photopigments. Results indicated that although both 20% and 40% dilutions led to lower phytoplankton biomass and growth rates, 40% reductions were more effective. Our results support the USA–Canada Great Lakes Water Quality Agreement recommendation of a 40% P reduction, but also indicate that a parallel reduction of N input by 40% would be most effective in controlling bloom magnitudes. Overall, our findings underscore the recommendation that a year‐round dual N and P 40% reduction is needed for long‐term control of eutrophication and algal blooms, including cyanobacteria and diatoms, in Lake Erie. 

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4. 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. 

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5. Elevated pH Conditions Associated With Microcystis spp. Blooms Decrease Viability of the Cultured Diatom Fragilaria crotonensis and Natural Diatoms in Lake Erie

   https://doi.org/10.3389/fmicb.2021.598736  

   Zepernick, Brittany N.; Gann, Eric R.; Martin, Robbie M.; Pound, Helena L.; Krausfeldt, Lauren E.; Chaffin, Justin D.; Wilhelm, Steven W. (February 2021, Frontiers in Microbiology)

   null (Ed.)

   Cyanobacterial Harmful Algal Blooms (CyanoHABs) commonly increase water column pH to alkaline levels ≥9.2, and to as high as 11. This elevated pH has been suggested to confer a competitive advantage to cyanobacteria such as Microcystis aeruginosa . Yet, there is limited information regarding the restrictive effects bloom-induced pH levels may impose on this cyanobacterium’s competitors. Due to the pH-dependency of biosilicification processes, diatoms (which seasonally both precede and proceed Microcystis blooms in many fresh waters) may be unable to synthesize frustules at these pH levels. We assessed the effects of pH on the ecologically relevant diatom Fragilaria crotonensis in vitro , and on a Lake Erie diatom community in situ . In vitro assays revealed F. crotonensis monocultures exhibited lower growth rates and abundances when cultivated at a starting pH of 9.2 in comparison to pH 7.7. The suppressed growth trends in F. crotonensis were exacerbated when co-cultured with M. aeruginosa at pH conditions and cell densities that simulated a cyanobacteria bloom. Estimates demonstrated a significant decrease in silica (Si) deposition at alkaline pH in both in vitro F. crotonensis cultures and in situ Lake Erie diatom assemblages, after as little as 48 h of alkaline pH-exposure. These observations indicate elevated pH negatively affected growth rate and diatom silica deposition; in total providing a competitive disadvantage for diatoms. Our observations demonstrate pH likely plays a significant role in bloom succession, creating a potential to prolong summer Microcystis blooms and constrain diatom fall resurgence. 

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