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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. 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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3. Response of Green Lake, Wisconsin, to Changes in Phosphorus Loading, With Special Emphasis on Near-Surface Total Phosphorus Concentrations and Metalimnetic Dissolved Oxygen Minima

   https://doi.org/10.3133/sir20225003  

   Robertson, D.M. ( January 2022 , Scientific investigations report)

   Green Lake is the deepest natural inland lake in Wisconsin, with a maximum depth of about 72 meters. In the early 1900s, the lake was believed to have very good water quality (low nutrient concentrations and good water clarity) with low dissolved oxygen (DO) concentrations occurring in only the deepest part of the lake. Because of increased phosphorus (P) inputs from anthropogenic activities in its watershed, total phosphorus (TP) concentrations in the lake have increased; these changes have led to increased algal production and low DO concentrations not only in the deepest areas but also in the middle of the water column (metalimnion). The U.S. Geological Survey has routinely monitored the lake since 2004 and its tributaries since 1988. Results from this monitoring led the Wisconsin Department of Natural Resources (WDNR) to list the lake as impaired because of low DO concentrations in the metalimnion, and they identified elevated TP concentrations as the cause of impairment. As part of this study by the U.S. Geological Survey, in cooperation with the Green Lake Sanitary District, the lake and its tributaries were comprehensively sampled in 2017–18 to augment ongoing monitoring that would further describe the low DO concentrations in the lake (especially in the metalimnion). Empirical and process-driven water-quality models were then used to determine the causes of the low DO concentrations and the magnitudes of P-load reductions needed to improve the water quality of the lake enough to meet multiple water-quality goals, including the WDNR’s criteria for TP and DO. Data from previous studies showed that DO concentrations in the metalimnion decreased slightly as summer progressed in the early 1900s but, since the late 1970s, have typically dropped below 5 milligrams per liter (mg/L), which is the WDNR criterion for impairment. During 2014–18 (the baseline period for this study), the near-surface geometric mean TP concentration during June–September in the east side of the lake was 0.020 mg/L and in the west side was 0.016 mg/L (both were above the 0.015-mg/L WDNR criterion for the lake), and the metalimnetic DO minimum concentrations (MOMs) measured in August ranged from 1.0 to 4.7 mg/L. The degradation in water quality was assumed to have been caused by excessive P inputs to the lake; therefore, the TP inputs to the lake were estimated. The mean annual external P load during 2014–18 was estimated to be 8,980 kilograms per year (kg/yr), of which monitored and unmonitored tributary inputs contributed 84 percent, atmospheric inputs contributed 8 percent, waterfowl contributed 7 percent, and septic systems contributed 1 percent. During fall turnover, internal sediment recycling contributed an additional 7,040 kilograms that increased TP concentrations in shallow areas of the lake by about 0.020 mg/L. The elevated TP concentrations then persisted until the following spring. On an annual basis, however, there was a net deposition of P to the bottom sediments. Empirical models were used to describe how the near-surface water quality of Green Lake would be expected to respond to changes in external P loading. Predictions from the models showed a relatively linear response between P loading and TP and chlorophyll-a (Chl-a) concentrations in the lake, with the changes in TP and Chl-a concentrations being less on a percentage basis (50–60 percent for TP and 30–70 percent for Chl-a) than the changes in P loading. Mean summer water clarity, quantified by Secchi disk depths, had a greater response to decreases in P loading than to increases in P loading. Based on these relations, external P loading to the lake would need to be decreased from 8,980 kg/yr to about 5,460 kg/yr for the geometric mean June–September TP concentration in the east side of the lake, with higher TP concentrations than in the west side, to reach the WDNR criterion of 0.015 mg/L. This reduction of 3,520 kg/yr is equivalent to a 46-percent reduction in the potentially controllable external P sources (all external sources except for precipitation, atmospheric deposition, and waterfowl) from those measured during water years 2014–18. The total external P loading would need to decrease to 7,680 kg/yr (a 17-percent reduction in potentially controllable external P sources) for near-surface June–September TP concentrations in the west side of the lake to reach 0.015 mg/L. Total external P loading would need to decrease to 3,870–5,320 kg/yr for the lake to be classified as oligotrophic, with a near-surface June–September TP concentration of 0.012 mg/L. Results from the hydrodynamic water-quality model GLM–AED (General Lake Model coupled to the Aquatic Ecodynamics modeling library) indicated that MOMs are driven by external P loading and internal sediment recycling that lead to high TP concentrations during spring and early summer, which in turn lead to high phytoplankton production, high metabolism and respiration, and ultimately DO consumption in the upper, warmer areas of the metalimnion. GLM–AED results indicated that settling of organic material during summer might be slowed by the colder, denser, and more viscous water in the metalimnion and thus increase DO consumption. Based on empirical evidence from a comparison of MOMs with various meteorological, hydrologic, water quality, and in-lake physical factors, MOMs were lower during summers, when metalimnetic water temperatures were warmer, near-surface Chl-a and TP concentrations were higher, and Secchi depths were lower. GLM–AED results indicated that the external P load would need to be reduced to about 4,060 kg/yr, a 57-percent reduction from that measured in 2014–18, to eliminate the occurrence of MOMs less than 5 mg/L during more than 75 percent of the years (the target provided by the WDNR). Large reductions in external P loading are expected to have an immediate effect on the near-surface TP concentrations and metalimnetic DO concentrations in Green Lake; however, it may take several years for the full effects of the external-load reduction to be observed because internal sediment recycling is an important source of P for the following spring. 

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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)

   null (Ed.)

   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. 

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5. Physical drivers facilitating a toxigenic cyanobacterial bloom in a major Great Lakes tributary

   https://doi.org/10.1002/lno.11558  

   Matson, Paul G. ; Boyer, Gregory L. ; Bridgeman, Thomas B. ; Bullerjahn, George S. ; Kane, Douglas D. ; McKay, Robert M. ; McKindles, Katelyn M. ; Raymond, Heather A. ; Snyder, Brenda K. ; Stumpf, Richard P. ; et al ( January 2020 , Limnology and Oceanography)

   The Maumee River is the primary source for nutrients fueling seasonal Microcystis-dominated blooms in western Lake Erie’s open waters though such blooms in the river are infrequent. The river also serves as source water for multiple public water systems and a large food services facility in northwest Ohio. On 20 September 2017, an unprecedented bloom was reported in the Maumee River estuary within the Toledo metropolitan area, which triggered a recreational water advisory. Here we (1) explore physical drivers likely contributing to the bloom’s occurrence, and (2) describe the toxin concentration and bacterioplankton taxonomic composition. A historical analysis using 10-years of seasonal river discharge, water level, and local wind data identified two instances when high-retention conditions occurred over ≥ 10 d in the Maumee River estuary: in 2016 and during the 2017 bloom. Observation by remote sensing imagery supported the advection of cyanobacterial cells into the estuary from the lake during 2017 and the lack of an estuary bloom in 2016 due to a weak cyanobacterial bloom in the lake. A rapid-response survey during the 2017 bloom determined levels of the cyanotoxins, specifically microcystins, in excess of recreational contact limits at sites within the lower 20 km of the river while amplicon sequencing found these sites were dominated by Microcystis. These results highlight the need to broaden our understanding of physical drivers of cyanobacterial blooms within the interface between riverine and lacustrine systems, particularly as such blooms are expected to become more prominent in response to a changing climate. 

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