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Lake Erie algal bloom discussions have historically focused on cyanobacteria, with foundational "blooms like it hot" and "high nutrient" paradigms considered as primary drivers behind cyanobacterial bloom success. Yet, recent surveys have rediscovered winter-spring diatom blooms, introducing another key player in the Lake Erie eutrophication and algal bloom story which has been historically overlooked. These blooms (summer vs. winter) have been treated as solitary events separated by spatial and temporal gradients. However, new evidence suggests they may not be so isolated, linked in a manner that manifests as an algal bloom cycle. Equally notable are the emerging reports of cyanobacterial blooms in cold and/or oligotrophic freshwaters, which have been interpreted by some as shifts in classical bloom paradigms. These emerging bloom reports have led many to ask "what is a bloom?". Furthermore, questioning classic paradigms has caused others to wonder if we are overlooking additional factors which constrain bloom success. In light of emerging data and ideas, we revisited foundational concepts within the context of Lake Erie algal blooms and derived five key take-aways: 1) Additional bloom-formers (diatoms) need to be included in Lake Erie algal discussions, 2) The term "bloom" must be reinforced with a clear definition and quantitative metrics for each event, 3) Algal blooms should not be studied solitarily, 4) Shifts in physiochemical conditions serve as an alternative interpretation to potential shifts in ecological paradigms, 5) Additional factors which constrain bloom success and succession (i.e., pH and light) require consideration.
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To elucidate the effects of environmental heterogeneity on diversity, composition, and degree of overlap between free-living (FL) and particle-attached (PA) bacteria, we sampled large, shallow, eutrophic Lake Taihu, China across gradients spanning riverine inflow, cyanobacterial blooms, and the open limnetic area. Using high-throughput sequencing of the 16S rRNA gene, we show that (i) bacterial communities near riverine inflow had high α-diversity and a high degree of overlap between FL and PA lifestyles, (ii) communities in cyanobacterial blooms have reduced α-diversity within the PA lifestyle, and (iii) communities from the limnetic area had the lowest bacterial α-diversity within the FL lifestyle and a medium degree of overlap between the FL and PA lifestyles. Redundancy analysis showed that the variation of the FL bacterial community was shaped by suspended solids and total phosphorous, while the variation of the PA bacterial community was shaped by suspended solids, dissolved oxygen, and the percentage of organic matter in suspended solids. This study highlights the importance of environmental heterogeneity, riverine input, cyanobacterial blooms, and nutrient status on the spatial distribution patterns of FL and PA bacterial communities in freshwater lakes.
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Cianobactérias , Lagos , Lagos/microbiologia , RNA Ribossômico 16S/genética , Biodiversidade , Cianobactérias/genética , China , EutrofizaçãoRESUMO
Cylindrospermopsis (Raphidiopsis) raciborskii is an invasive, filamentous, nitrogen-fixing cyanobacterium that forms frequent blooms in freshwater habitats. While viruses play key roles in regulating the abundance, production and diversity of their hosts in aquatic ecosystems, the role(s) of viruses in the ecology of C. raciborskii is almost unexplored. Progress in this field has been hindered by the absence of a characterized virus-host system in C. raciborskii. To bridge this gap, we sequenced the genome of CrV-01T, a previously isolated cyanosiphovirus, and its host, C. raciborskii strain Cr2010. Analyses suggest that CrV-01T represents a distinct clade of siphoviruses infecting, and perhaps lysogenizing, filamentous cyanobacteria. Its genome contains unique features that include an intact CRISPR array and a 12 kb inverted duplication. Evidence suggests CrV-01T recently gained the ability to infect Cr2010 and recently lost the ability to form lysogens. The cyanobacterial host contains a CRISPR-Cas system with CRISPR spacers matching protospacers within the inverted duplication of the CrV-01T genome. Examination of metagenomes demonstrates that viruses with high genetic identity to CrV-01T, but lacking the inverted duplication, are present in C. raciborskii blooms in Australia. The unique genomic features of the CrV/Cr2010 system offers opportunities to investigate in more detail virus-host interactions in an ecologically important bloom-forming cyanobacterium.
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Cianobactérias/virologia , Especificidade de Hospedeiro , Vírus/isolamento & purificação , Austrália , Repetições Palindrômicas Curtas Agrupadas e Regularmente Espaçadas , Cianobactérias/fisiologia , Ecossistema , Água Doce/microbiologia , Água Doce/virologia , Genoma Viral , Genômica , Nitrogênio , Fenômenos Fisiológicos Virais , Vírus/genéticaRESUMO
Freshwater cyanobacterial blooms are regularly formed by Microcystis spp., which are well-known producers of the hepatotoxin microcystin. The environmental factors that regulate microcystin synthesis remain unclear. We used reverse transcription-quantitative PCR (RT-qPCR), metabolomics, and toxin profiling (both by LC-MS) to measure the response of Microcystis aeruginosa NIES-843 to nitrogen (N) concentration, N chemistry (nitrate versus urea), and a range of seasonally relevant temperatures. Growth rates at lower temperatures were slower but resulted in increased cellular microcystin content (quota), and at these lower temperatures, N concentration had no effect on toxin production. In contrast, at warmer temperatures, reduction in N concentration increased toxin production, especially when urea was supplied as the nitrogen source. Our culture results demonstrate how temperature may lead to physiological responses ranging from slow growing yet very toxic cells at cool temperatures, to faster growing but less-toxic cells at warmer temperatures. This response represents a key interaction in bloom dynamics. Capturing this phenomenon as a temperature-driven toxin phenotype incorporated into models might improve the ability to predict microcystin biosynthesis during cyanobacterial blooms.
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Cianobactérias , Microcystis , Microcistinas , Nitrogênio , TemperaturaRESUMO
The rediscovery of diatom blooms embedded within and beneath the Lake Erie ice cover (2007-2012) ignited interest in psychrophilic adaptations and winter limnology. Subsequent studies determined the vital role ice plays in winter diatom ecophysiology as diatoms partition to the underside of ice, thereby fixing their location within the photic zone. Yet, climate change has led to widespread ice decline across the Great Lakes, with Lake Erie presenting a nearly "ice-free" state in several recent winters. It has been hypothesized that the resultant turbid, isothermal water column induces light limitation amongst winter diatoms and thus serves as a competitive disadvantage. To investigate this hypothesis, we conducted a physiochemical and metatranscriptomic survey that spanned spatial, temporal, and climatic gradients of the winter Lake Erie water column (2019-2020). Our results suggest that ice-free conditions decreased planktonic diatom bloom magnitude and altered diatom community composition. Diatoms increased their expression of various photosynthetic genes and iron transporters, which suggests that the diatoms are attempting to increase their quantity of photosystems and light-harvesting components (a well-defined indicator of light limitation). We identified two gene families which serve to increase diatom fitness in the turbid ice-free water column: proton-pumping rhodopsins (a potential second means of light-driven energy acquisition) and fasciclins (a means to "raft" together to increase buoyancy and co-locate to the surface to optimize light acquisition). With large-scale climatic changes already underway, our observations provide insight into how diatoms respond to the dynamic ice conditions of today and shed light on how they will fare in a climatically altered tomorrow.
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Diatomáceas , Diatomáceas/genética , Ecossistema , Camada de Gelo , Lagos , ÁguaRESUMO
For Microcystis aeruginosa PCC 7806, temperature decreases from 26° C to 19° C double the microcystin quota per cell during growth in continuous culture. Here we tested whether this increase in microcystin provided M. aeruginosa PCC 7806 with a fitness advantage during colder-temperature growth by comparing cell concentration, cellular physiology, and the transcriptomics-inferred metabolism to a non-toxigenic mutant strain M. aeruginosa PCC 7806 ΔmcyB. Photo-physiological data combined with transcriptomic data revealed metabolic changes in the mutant strain during growth at 19° C, which included increased electron sinks and non-photochemical quenching. Increased gene expression was observed for a glutathione-dependent peroxiredoxin during cold treatment, suggesting compensatory mechanisms to defend against reactive oxygen species are employed in the absence of microcystin in the mutant. Our observations highlight the potential selective advantages of a longer-term defensive strategy in management of oxidative stress (i.e., making microcystin) vs the shorter-term proactive strategy of producing cellular components to actively dissipate or degrade oxidative stress agents.
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For Microcystis aeruginosa PCC 7806, temperature decreases from 26 °C to 19 °C double the microcystin quota per cell during growth in continuous culture. Here we tested whether this increase in microcystin provided M. aeruginosa PCC 7806 with a fitness advantage during colder-temperature growth by comparing cell concentration, cellular physiology, reactive oxygen species damage, and the transcriptomics-inferred metabolism to a non-toxigenic mutant strain M. aeruginosa PCC 7806 ΔmcyB. Photo-physiological data combined with transcriptomic data revealed metabolic changes in the mutant strain during growth at 19 °C, which included increased electron sinks and non-photochemical quenching. Increased gene expression was observed for a glutathione-dependent peroxiredoxin during cold treatment, suggesting compensatory mechanisms to defend against reactive oxygen species are employed in the absence of microcystin in the mutant. Our observations highlight the potential selective advantages of a longer-term defensive strategy in management of oxidative stress (i.e., making microcystin) vs the shorter-term proactive strategy of producing cellular components to actively dissipate or degrade oxidative stress agents.
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Microcistinas , Microcystis , Microcistinas/metabolismo , Temperatura Baixa , Espécies Reativas de Oxigênio/metabolismo , AclimataçãoRESUMO
Pseudanabaena spp. are filamentous cyanobacteria widely distributed in temperate lakes. Though infrequent, they can form harmful algal blooms. Here, we present a high-quality metagenome-assembled genome of a Pseudanabaena sp. from a toxic, crimson cyanobacterial bloom in Lake Salubria, NY.
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Huisman et al. claim that our model is poorly supported or contradicted by other studies and the predictions are "seriously flawed." We show their criticism is based on an incomplete selection of evidence, misinterpretation of data, or does not actually refute the model. Like all ecosystem models, our model has simplifications and uncertainties, but it is better than existing approaches hat ignore biology and do not predict toxin concentration.
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Toxinas Bacterianas , Lagos , Microcystis , Fósforo , Ecossistema , Lagos/química , Lagos/microbiologia , Fósforo/deficiência , Toxinas Bacterianas/metabolismo , Toxinas Bacterianas/toxicidade , Microcystis/metabolismoRESUMO
Harmful cyanobacteria are a global environmental problem, yet we lack actionable understanding of toxigenic versus nontoxigenic strain ecology and toxin production. We performed a large-scale meta-analysis including 103 papers and used it to develop a mechanistic, agent-based model of Microcystis growth and microcystin production. Simulations for Lake Erie suggest that the observed toxigenic-to-nontoxigenic strain succession during the 2014 Toledo drinking water crisis was controlled by different cellular oxidative stress mitigation strategies (protection by microcystin versus degradation by enzymes) and the different susceptibility of those mechanisms to nitrogen limitation. This model, as well as a simpler empirical one, predicts that the planned phosphorus load reduction will lower biomass but make nitrogen and light more available, which will increase toxin production, favor toxigenic cells, and increase toxin concentrations.
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Lagos , Microcistinas , Microcystis , Fósforo , Canadá , Água Potável , Lagos/química , Lagos/microbiologia , Microcistinas/análise , Microcistinas/metabolismo , Microcistinas/toxicidade , Microcystis/genética , Microcystis/crescimento & desenvolvimento , Microcystis/metabolismo , Nitrogênio/metabolismo , Fósforo/análise , Fósforo/metabolismo , Estados Unidos , Abastecimento de ÁguaRESUMO
Harmful algal blooms (HABs) caused by the toxin-producing cyanobacteria Microcystis spp., can increase water column pH. While the effect(s) of these basified conditions on the bloom formers are a high research priority, how these pH shifts affect other biota remains understudied. Recently, it was shown these high pH levels decrease growth and Si deposition rates in the freshwater diatom Fragilaria crotonensis and natural Lake Erie (Canada-US) diatom populations. However, the physiological mechanisms and transcriptional responses of diatoms associated with these observations remain to be documented. Here, we examined F. crotonensis with a set of morphological, physiological, and transcriptomic tools to identify cellular responses to high pH. We suggest 2 potential mechanisms that may contribute to morphological and physiological pH effects observed in F. crotonensis. Moreover, we identified a significant upregulation of mobile genetic elements in the F. crotonensis genome which appear to be an extreme transcriptional response to this abiotic stress to enhance cellular evolution rates-a process we have termed "genomic roulette." We discuss the ecological and biogeochemical effects high pH conditions impose on fresh waters and suggest a means by which freshwater diatoms such as F. crotonensis may evade high pH stress to survive in a "basified" future.
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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 â¼35% of Microcystis-specific functional genes and â¼45% 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.
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In shallow lakes, wind wave turbulence alters underwater spectral composition, but the influence of this phenomenon on phytoplankton community structure is poorly understood. We used 100L mesocosms to investigate the influence of light quality on a natural phytoplankton community collected from Taihu Lake in China. The communities in mesocosms were exposed to sunlight filtered for white, blue, green, and red light, while wave-making pumps simulated wind wave turbulence similar to Taihu Lake. Over the course of experiment, each filtered light reduced the total phytoplankton abundance compared to white light. The mean abundance of phytoplankton in controls was 1.72, 1.78, and 7.89 times of that in the red, blue, and green light treatments. Red, blue, and green light significantly promoted the growth of cyanobacteria, green algae, and diatoms, respectively, and induced successional change of the phytoplankton species under the tested conditions. The proportion of Microcystis to total phytoplankton abundance in controls and red light shifted from 87.09% at the beginning to 37.95% and 56.30% at the end of the experiment, respectively, and maintained its dominance, whereas Microcystis lost its dominance and was replaced by Scenedesmus (53.78%) and Synedra (53.18%) in the blue and green light, respectively. Given the process of how these phytoplankton compete in designated spectrum, exploring these influences could help provide new insights into the dominance formation of toxic cyanobacteria.
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Cianobactérias , Microcystis , Scenedesmus , China , Eutrofização , Lagos , FitoplânctonRESUMO
Raphidiopsis raciborskii and Planktothrix agardhii are filamentous, potentially toxin-producing cyanobacteria that form nuisance blooms in fresh waters. Here, we report high-quality metagenome-assembled genome sequences of R. raciborskii and P. agardhii collected from a bloom in Kissena Lake, New York.
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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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Microcystins produced during harmful cyanobacterial blooms are a public health concern. Although patterns are emerging, the environmental cues that stimulate production of microcystin remain confusing, hindering our ability to predict fluctuations in bloom toxicity. In earlier work, growth at cool temperatures relative to optimum (18°C vs. 26°C) was confirmed to increase microcystin quota in batch cultures of Microcystis aeruginosa NIES-843. Here, we tested this response in M. aeruginosa PCC 7806 using continuous cultures to examine temporal dynamics and using RNA-sequencing to investigate the physiological nature of the response. A temperature reduction from 26 to 19°C increased microcystin quota â¼2-fold, from an average of â¼464 ag µm-3 cell volume to â¼891 ag µm-3 over a 7-9 d period. Reverting the temperature to 26°C returned the cellular microcystin quota to â¼489 ag µm-3. Long periods (31-42 d) at 19°C did not increase or decrease microcystin quota beyond that observed at 7-9 d. Nitrogen concentration had little effect on the overall response. RNA sequencing indicated that the decrease in temperature to 19°C induced a classic cold-stress response in M. aeruginosa PCC 7806, but this operated on a different timescale than the increased microcystin production. Microcystin quota showed a strong 48- to 72-h time-lag correlation to mcy gene expression, but no correlation to concurrent mcy expression. This work confirms an effect of temperature on microcystin quota and extends our understanding of the physiological nature of the response.
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Butterfield Lake is a mesotrophic lake in New York State where residents and pets have experienced unexplained health issues. Microseira wollei (basionym Lyngbya wollei) was found at two of 15 sites in Butterfield Lake and analyzed for microcystins, anatoxins, cylindrospermopsins, and paralytic shellfish poisoning toxins (PSTs). Only PSTs and trace levels of anatoxin-a were detected in these samples. This is the first published report of PSTs within a New York State lake. To evaluate the environmental and temporal drivers leading to the observed toxicity, PST content at the two sites was examined in detail. There were distinct differences in the total PST content, filament nutrient, filament chlorophyll, and relationship to environmental drivers between the sites, as well as distinct differences in the total PST content measured using different analytical techniques. A multivariate model containing site, temperature, and filament chlorophyll explained 85% of the variation in PSTs observed over the growing season. This work emphasizes the importance of proper site selection and choice of analytical technique in the development of monitoring programs to protect lake users from the occurrence of benthic cyanobacteria toxins.
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Toxinas Bacterianas/análise , Cianobactérias/isolamento & purificação , Lagos/análise , Microcistinas/análise , Saxitoxina/análise , Tropanos/análise , Uracila/análogos & derivados , Poluentes da Água/análise , Alcaloides , Cianobactérias/genética , Toxinas de Cianobactérias , Monitoramento Ambiental , New York , RNA Ribossômico 16S , Intoxicação por Frutos do Mar , Uracila/análiseRESUMO
Toxoplasma gondii counts among the most consequential food-borne parasites, and although the parasite occurs in a wide range of wild and domesticated animals, farms may constitute a specific and important locus of transmission. If so, parasites in animals that inhabit agricultural habitats might be suspected of harbouring genetically distinct parasite types. To better understand habitat effects pertinent to this parasite's transmission, we compiled and analysed existing genotypic data of 623 samples from animals across a proximity gradient from areas of human settlement to the wilderness in North America. To facilitate such analysis, T. gondii isolates were divided into three groups: (i) from farm-bound animals (with the most limited home ranges on farms); (ii) from free-roaming animals (with wider home ranges on or near farms); and (iii) from wildlife. In addition, parasite genotype distribution in different animal species was analysed. We observed no absolute limitation of any of five major genotypes to any one habitat; however, the frequency of four genotypes decreased across the gradient from the farm-bound group, to the free-roaming group, then the wildlife, whereas a fifth genotype increased along that gradient. Genetic diversity was greater in free-roaming than in farm-bound animals. The genotypic composition of parasites in wildlife differed from those in farm-bound and free-roaming animals. Furthermore, parasite genotypes differed among host species. We conclude that T. gondii genotype distributions are influenced by the spatial habitat and host species composition, and parasite diversity decreases towards areas of human settlement, elucidating facts which may influence transmission dynamics and zoonotic potential in this ubiquitous but regionally variable parasite.
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Animais Domésticos/parasitologia , Animais Selvagens/parasitologia , Genótipo , Toxoplasma/genética , Toxoplasmose Animal/parasitologia , Animais , Demografia , Variação Genética , Especificidade de Hospedeiro , Humanos , América do Norte/epidemiologia , Toxoplasmose Animal/epidemiologiaRESUMO
Microcystins are secondary metabolites produced by several freshwater, bloom-forming cyanobacterial species. Microcystin-producing cyanobacteria co-occur with a complex community of heterotrophic bacteria. Though conflicting, studies suggest that microcystins affect the physiology of heterotrophic bacteria by inducing oxidative stress and increasing cell envelope permeability. Based on these observations, we hypothesized that exposure to microcystin should induce differential expression in genes responding to oxidative and envelope stress and trigger shifts in metabolite pools. We tested this hypothesis by exposing Escherichia coli MG1655 to 1 and 10 mg/L microcystin-LR and monitored global changes to gene expression, cellular metabolite pools, and lipid composition using RNA-sequencing and UPLC-MS. Contrary to reported studies, we observed no evidence that microcystin-LR induced oxidative or cell envelope stress in E. coli under the tested conditions. Our results suggest a potential difference in mechanism by which microcystin-LR interacts with heterotrophic bacteria vs. cyanobacteria.