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1. Impacts of microbial assemblage and environmental conditions on the distribution of anatoxin-a producing cyanobacteria within a river network

   Bouma-Gregson, Keith; Olm, Matthew R.; Probst, Alexander J.; Anantharaman, Karthik; Power, Mary E.; Banfield, Jillian F. (January 2019, ISME)

   Blooms of planktonic cyanobacteria have long been of concern in lakes, but more recently, harmful impacts of riverine benthic cyanobacterial mats been recognized. As yet, we know little about how various benthic cyanobacteria are distributed in river networks, or how environmental conditions or other associated microbes in their consortia affect their biosynthetic capacities. We performed metagenomic sequencing for 22 Oscillatoriales-dominated (Cyanobacteria) microbial mats collected across the Eel River network in Northern California and investigated factors associated with anatoxin-a producing cyanobacteria. All microbial communities were dominated by one or two cyanobacterial species, so the key mat metabolisms involve oxygenic photosynthesis and carbon oxidation. Only a few metabolisms fueled the growth of the mat communities, with little evidence for anaerobic metabolic pathways. We genomically defined four cyanobacterial species, all which shared <96% average nucleotide identity with reference Oscillatoriales genomes and are potentially novel species in the genus Microcoleus. One of the Microcoleus species contained the anatoxin-a biosynthesis genes, and we describe the first anatoxin-a gene cluster from the Microcoleus clade within Oscillatoriales. Occurrence of these four Microcoleus species in the watershed was correlated with total dissolved nitrogen and phosphorus concentrations, and the species that contains the anatoxin-a gene cluster was found in sites with higher nitrogen concentrations. Microbial assemblages in mat samples with the anatoxin-a gene cluster consistently had a lower abundance of Burkholderiales (Betaproteobacteria) species than did mats without the anatoxin-producing genes. The associations of water nutrient concentrations and certain co-occurring microbes with anatoxin-a producing Microcoleus motivate further exploration for their roles as potential controls on the distributions of toxigenic benthic cyanobacteria in river networks. 

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2. Microcoleus (Cyanobacteria) form watershed‐wide populations without strong gradients in population structure

   https://doi.org/10.1111/mec.16208  

   Bouma‐Gregson, Keith; Crits‐Christoph, Alexander; Olm, Mathew R.; Power, Mary E.; Banfield, Jillian F. (October 2021, Molecular Ecology)

   Abstract The relative importance of separation by distance and by environment to population genetic diversity can be conveniently tested in river networks, where these two drivers are often independently distributed over space. To evaluate the importance of dispersal and environmental conditions in shaping microbial population structures, we performed genome‐resolved metagenomic analyses of benthicMicrocoleus‐dominated cyanobacterial mats collected in the Eel and Russian River networks (California, USA). The 64 Microcoleusgenomes were clustered into three species that shared >96.5% average nucleotide identity (ANI). Most mats were dominated by one strain, but minor alleles within mats were often shared, even over large spatial distances (>300 km). Within the most commonMicrocoleusspecies, the ANI between the dominant strains within mats decreased with increasing spatial separation. However, over shorter spatial distances (tens of kilometres), mats from different subwatersheds had lower ANI than mats from the same subwatershed, suggesting that at shorter spatial distances environmental differences between subwatersheds in factors like canopy cover, conductivity, and mean annual temperature decreases ANI. Since mats in smaller creeks had similar levels of nucleotide diversity (π) as mats in larger downstream subwatersheds, within‐mat genetic diversity does not appear to depend on the downstream accumulation of upstream‐derived strains. The four‐gamete test and sequence length bias suggest recombination occurs between almost all strains within each species, even between populations separated by large distances or living in different habitats. Overall, our results show that, despite some isolation by distance and environmental conditions, sufficient gene‐flow occurs among cyanobacterial strains to prevent either driver from producing distinctive population structures across the watershed. 

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3. Anatoxin concentrations, algal assemblages, and water quality data for the South Fork Eel, Salmon, and Russian Rivers in northern California, 2022-2023

   https://doi.org/10.6073/pasta/7fa428fd275d9b90720204b9f491c18f  

   Zabrecky, Jordan M; Elliott, Taryn A; Hickey, Meaghan; Lei, Helen; Christova, Rosalina S; Boyer, Gregory; Genzoli, Laurel; Johnson, Grant; Blaszczak, Joanna R (April 2025, Environmental Data Initiative)

   We collected this data to better understand the timing of peak benthic cyanobacterial mat occurrence (specifically taxa associated with anatoxin production, Microcoleus and Anabaena) and mat anatoxin concentrations in rivers. We sampled in northern California on the South Fork Eel, Salmon, and Russian Rivers biweekly in 2022, and the Salmon River biweekly and South Fork Eel weekly in 2023. During each sampling event, we conducted benthic cover surveys, measured in-situ water quality parameters (temperature, pH, dissolved oxygen, conductivity), and collected surface water samples and targeted cyanobacteria samples. In 2022 on all rivers and in 2023 at the Salmon River, we also collected distributed non-targeted periphyton samples to characterize full-reach community compositions. All sampling was completed in 150-m reaches upstream of sensors recording continuous dissolved oxygen, conductivity, and temperature data. We analyzed surface water samples for nitrate, ammonium, soluble reactive phosphate, total dissolved carbon, and dissolved organic carbon. We also analyzed surface water samples from 2022 for major anions (Cl, SO4, Br) and cations (Na, K, Mg, Ca). Targeted-cyanobacteria and non-target periphyton samples were analyzed for anatoxins, relative abundance of algal taxa (via microscopy), ash-free dry mass, and chlorophyll-a. To estimate mean river depth within the dissolved oxygen footprint upstream of sensors, we kayaked portions of the river and collected river depth measurements. We also measured discharge at each river excluding the Salmon River (due to high discharge) and completed pebble counts at the South Fork Eel River to obtain sediment grain size distributions. 

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4. Omics-Inferred Partitioning and Expression of Diverse Biogeochemical Functions in a Low-O ₂ Cyanobacterial Mat Community

   https://doi.org/10.1128/mSystems.01042-21  

   Grim, Sharon L.; Voorhies, Alexander A.; Biddanda, Bopaiah A.; Jain, Sunit; Nold, Stephen C.; Green, Russ; Dick, Gregory J. (December 2021, mSystems)

   Bernstein, Hans C. (Ed.)

   ABSTRACT Cyanobacterial mats profoundly influenced Earth’s biological and geochemical evolution and still play important ecological roles in the modern world. However, the biogeochemical functioning of cyanobacterial mats under persistent low-O 2 conditions, which dominated their evolutionary history, is not well understood. To investigate how different metabolic and biogeochemical functions are partitioned among community members, we conducted metagenomics and metatranscriptomics on cyanobacterial mats in the low-O 2 , sulfidic Middle Island sinkhole (MIS) in Lake Huron. Metagenomic assembly and binning yielded 144 draft metagenome assembled genomes, including 61 of medium quality or better, and the dominant cyanobacteria and numerous Proteobacteria involved in sulfur cycling. Strains of a Phormidium autumnale -like cyanobacterium dominated the metagenome and metatranscriptome. Transcripts for the photosynthetic reaction core genes psaA and psbA were abundant in both day and night. Multiple types of psbA genes were expressed from each cyanobacterium, and the dominant psbA transcripts were from an atypical microaerobic type of D1 protein from Phormidium . Further, cyanobacterial transcripts for photosystem I genes were more abundant than those for photosystem II, and two types of Phormidium sulfide quinone reductase were recovered, consistent with anoxygenic photosynthesis via photosystem I in the presence of sulfide. Transcripts indicate active sulfur oxidation and reduction within the cyanobacterial mat, predominately by Gammaproteobacteria and Deltaproteobacteria , respectively. Overall, these genomic and transcriptomic results link specific microbial groups to metabolic processes that underpin primary production and biogeochemical cycling in a low-O 2 cyanobacterial mat and suggest mechanisms for tightly coupled cycling of oxygen and sulfur compounds in the mat ecosystem. IMPORTANCE Cyanobacterial mats are dense communities of microorganisms that contain photosynthetic cyanobacteria along with a host of other bacterial species that play important yet still poorly understood roles in this ecosystem. Although such cyanobacterial mats were critical agents of Earth’s biological and chemical evolution through geological time, little is known about how they function under the low-oxygen conditions that characterized most of their natural history. Here, we performed sequencing of the DNA and RNA of modern cyanobacterial mat communities under low-oxygen and sulfur-rich conditions from the Middle Island sinkhole in Lake Huron. The results reveal the organisms and metabolic pathways that are responsible for both oxygen-producing and non-oxygen-producing photosynthesis as well as interconversions of sulfur that likely shape how much O 2 is produced in such ecosystems. These findings indicate tight metabolic reactions between community members that help to explain the limited the amount of O 2 produced in cyanobacterial mat ecosystems. 

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5. Environmental Factors Impacting the Development of Toxic Cyanobacterial Proliferations in a Central Texas Reservoir

   https://doi.org/10.3390/toxins16020091  

   Perri, Katherine A.; Bellinger, Brent J.; Ashworth, Matt P.; Manning, Schonna R. (February 2024, Toxins)

   Cyanobacterial harmful algal proliferations (cyanoHAPs) are increasingly associated with dog and livestock deaths when benthic mats break free of their substrate and float to the surface. Fatalities have been linked to neurotoxicosis from anatoxins, potent alkaloids produced by certain genera of filamentous cyanobacteria. After numerous reports of dog illnesses and deaths at a popular recreation site on Lady Bird Lake, Austin, Texas in late summer 2019, water and floating mat samples were collected from several sites along the reservoir. Water quality parameters were measured and mat samples were maintained for algal isolation and DNA identification. Samples were also analyzed for cyanobacterial toxins using LC-MS. Dihydroanatoxin-a was detected in mat materials from two of the four sites (0.6–133 ng/g wet weight) while water samples remained toxin-free over the course of the sampling period; no other cyanobacterial toxins were detected. DNA sequencing analysis of cyanobacterial isolates yielded a total of 11 genera, including Geitlerinema, Tyconema, Pseudanabaena, and Phormidium/Microcoleus, taxa known to produce anatoxins, including dihydroanatoxin, among other cyanotoxins. Analyses indicate that low daily upriver dam discharge, higher TP and NO3 concentrations, and day of the year were the main parameters associated with the presence of toxic floating cyanobacterial mats. 

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