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ABSTRACT The cyanobacterial genusMicrocystisis globally distributed and known for its ability to produce microcystins, a structurally diverse group of cyanotoxins. However, the biosynthetic capacity ofMicrocystisis vast; its diverse genomes contain a variety of biosynthetic gene clusters (BGCs) encoding the synthesis of metabolites that may be toxic, have important ecological function, or have applications for biotechnology or drug discovery. Recent studies illustrate that these BGCs vary significantly acrossMicrocystisstrains, can be highly expressed in environmental conditions, and may play key roles in cellular physiology, grazer deterrence, and microbial interactions. However, many of these BGCs and metabolites remain poorly characterized or completely uncharacterized, having been identified only through genome sequencing or mass spectrometry, respectively, leaving no knowledge of their structure, bioactivity, or physiological or ecological functions. Here, we synthesize the current body of knowledge regarding the secondary metabolism ofMicrocystisin terms of genetic and chemical diversity, potential drivers of synthesis, and physiological and ecological functions. This review highlights the need for further research to characterize the largely unexplored genetic and chemical diversity ofMicrocystisin communities in the environment and discusses the challenges and opportunities of integrating high-throughput multiomic approaches to link uncharacterized gene clusters with their corresponding metabolites.Microcystiswill continue to be a rich source for secondary metabolite research as its genetic and chemical potential likely plays a critical role in the persistence and observed dynamics of harmful algal blooms and may harbor uncharacterized toxins and metabolites. 

ABSTRACT Microcystisspp. are renowned for producing the hepatotoxin microcystin in freshwater cyanobacterial harmful algal blooms around the world, threatening drinking water supplies and public and environmental health. However,Microcystisgenomes also harbor numerous biosynthetic gene clusters (BGCs) encoding the biosynthesis of other secondary metabolites, including many with toxic properties. Most of these BGCs are uncharacterized and currently lack links to biosynthesis products. However, recent field studies show that many of these BGCs are abundant and transcriptionally active in natural communities, suggesting potentially important yet unknown roles in bloom ecology and water quality. Here, we analyzed 21 xenicMicrocystiscultures isolated from western Lake Erie to investigate the diversity of the biosynthetic potential of this genus. Through metabologenomic andin silicoapproaches, we show that theseMicrocystisstrains contain variable BGCs, previously observed in natural populations, and encode distinct metabolomes across cultures. Additionally, we find that the majority of metabolites and gene clusters are uncharacterized, highlighting our limited understanding of the chemical repertoire ofMicrocystisspp. Due to the complex metabolomes observed in culture, which contain a wealth of diverse congeners as well as unknown metabolites, these results underscore the need to deeply explore and identify secondary metabolites produced byMicrocystisbeyond microcystins to assess their impacts on human and environmental health.IMPORTANCEThe genusMicrocystisforms dense cyanobacterial harmful algal blooms (cyanoHABs) and can produce the toxin microcystin, which has been responsible for drinking water crises around the world. While microcystins are of great concern,Microcystisalso produces an abundance of other secondary metabolites that may be of interest due to their potential for toxicity, ecological importance, or pharmaceutical applications. In this study, we combine genomic and metabolomic approaches to study the genes responsible for the biosynthesis of secondary metabolites as well as the chemical diversity of produced metabolites inMicrocystisstrains from the Western Lake Erie Culture Collection. This unique collection comprisesMicrocystisstrains that were directly isolated from western Lake Erie, which experiences substantial cyanoHAB events annually and has had negative impacts on drinking water, tourism, and industry. 

ABSTRACT Cyanobacterial harmful algal blooms (cyanoHABs) threaten human, animal, and ecosystem health and safety through production of toxic secondary metabolites.Microcystis,a cosmopolitan bloom‐forming cyanobacterial genus, is well‐known for producing hepatotoxic microcystins (MCs), but it can produce many other bioactive cyanopeptides, such as anabaenopeptins (APs), that occur at high levels in blooms. The toxicological and ecological impacts of such co‐occurring cyanopeptides in the natural environment remain understudied. Here we evaluated the effects of pure MCs and APs individually and in combination, as well as extracts ofMicrocystiscultures producing diverse suites of cyanopeptides, including strains with and without MCs and APs, on human lung (A549), kidney (HK2), and liver (Hep‐3B) cell viability. Individual MC and AP congeners exhibited a gradient of toxic effects across cell lines; MC‐LA caused the most toxic effects, MC‐LR had comparable effects to AP‐A and AP‐B, and MC‐RR caused the least toxicity. Combined exposure to MC‐LA and AP‐B produced dose‐dependent synergistic effects across all three cell lines.Microcystisculture extracts significantly reduced cell viability in dose‐ andMicrocystisstrain‐dependent patterns that could not be explained by microcystin or anabaenopeptin content alone, suggesting a role of other metabolites and their interactions within the mixtures. These findings demonstrate that mixtures of environmentally relevant cyanopeptides can have greater toxic threats than individual compounds and underscore the importance of considering metabolites beyond MCs and their potential interactions in public health, future risk assessments, and management strategies for cyanoHAB‐impacted waters. 

ABSTRACT Here, we report on the raw and coassembled metatranscriptomes of 39 Lake Erie surface (1.0 m) water samples collected over a 2-day diel period encompassing episodic weather and bloom events. Preliminary taxonomic annotations and read mappings revealed thatMicrocystisspp. accounted for up to ~47% of the transcriptionally active community. 

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. 

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.