Biology subjects

Dick, G. J.

Publications and source records attributed to Dick, G. J..

6 recordsLinked to original sources

bioRxiv2023

THE DUAL ROLE OF THE MICROCYSTIS AERUGINOSA MICROBIOME ON CYANOTOXIN PRODUCTION: COMPETITION FOR AND REMINERALIZATION OF ORGANIC NITROGEN

Nutrient-induced blooms of the globally abundant freshwater toxic cyanobacterium Microcystis are the cause of worldwide public and ecosystem health concerns. The response of Microcystis growth and toxin production to new and recycled nitrogen (N) inputs, and the impact of heterotrophic bacteria in the Microcystis phycosphere on these processes are not well understood. Here, using microbiome transplant experiments, cyanotoxin analysis, and stable isotope tracing to measure N incorporation and exchange at single cell resolution, we monitored the growth, cyanotoxin production, and microbiome community structure of several Microcystis strains grown on amino acids and proteins as the sole N source. We demonstrate that 1) organic N availability shapes the microbiome community structure in the Microcystis phycosphere; 2) external organic N input leads to lower bacterial colonization of the phycosphere; 3) certain Microcystis strains can directly uptake amino acids, but with lower rates than heterotrophic bacteria; 4) biomass-specific microcystin production is not impacted by N source (i.e., nitrate, amino acids and protein) but rather by total N availability; and 5) some bacterial communities compete with Microcystis for organic N, but others remineralize organic N, in the process producing bio-available N for Microcystis. We conclude that organic N input can support Microcystis blooms and toxin production, and Microcystis-associated microbial communities play critical roles by influencing cyanobacterial succession through either decreasing (via competition) or increasing (via remineralization) N availability, especially under inorganic N scarcity.

microbiology↗

bioRxiv2023

Seasonal Shifts in Community Composition and Proteome Expression in a Sulfur-Cycling Cyanobacterial Mat

Seasonal changes in light and physicochemical conditions have strong impacts on cyanobacteria, but how they affect community structure, metabolism, and biogeochemistry of cyanobacterial mats remains unclear. Light may be particularly influential for cyanobacterial mats exposed to sulfide by altering the balance of oxygenic photosynthesis and sulfide-driven anoxygenic photosynthesis. We studied temporal shifts in irradiance, water chemistry, and community structure and function of microbial mats in Middle Island Sinkhole (MIS), where anoxic and sulfate-rich groundwater provides habitat for cyanobacteria that conduct both oxygenic and anoxygenic photosynthesis. Seasonal changes in light and groundwater chemistry were accompanied by shifts in bacterial community composition, with a succession of dominant cyanobacteria from Phormidium to Planktothrix, and an increase in diatoms, sulfur-oxidizing bacteria, and sulfate-reducing bacteria from summer to autumn. Differential abundance of cyanobacterial light harvesting proteins likely reflects a physiological response of cyanobacteria to light level. Beggiatoa sulfur oxidation proteins were more abundant in autumn. Correlated abundances of taxa through time suggest interactions between sulfur oxidizers and sulfate reducers, sulfate reducers and heterotrophs, and cyanobacteria and heterotrophs. These results support the conclusion that seasonal change, including light availability, has a strong influence on community composition and biogeochemical cycling of sulfur and O2 in cyanobacterial mats. Originality-Significance StatementCyanobacterial mats are found in terrestrial and aquatic environments on modern Earth and their fossil remains are present throughout the geologic record. They are biogeochemical oases that underpin diverse metabolic interactions, transform key nutrients and fix carbon, and can thrive in extreme environments. Mat-forming cyanobacteria can be metabolically versatile and conduct both oxygenic and anoxygenic photosynthesis using sulfide (OP and AP), thereby participating in both oxygen and sulfur cycling. The effect of seasonality on ecological factors constraining photosynthetic production and geochemical cycling in extreme cyanobacterial mats is not well known. In this study, we surveyed the mat community composition via bacterial 16S rRNA genes, microbial activity via metaproteomics, and water physico- and geochemistry over multiple seasons and years of the cyanobacterial mat in Middle Island Sinkhole, an O2-poor benthic sinkhole in Lake Huron, Michigan. We found that higher availability of sulfate-rich groundwater, together with higher light intensity, coincided with dominance of the metabolically flexible cyanobacterium Phormidium during the summer. Diverse sulfur cycling bacteria were more successful in other seasons when the mat experienced lower light and sulfate availability. These results provide insights into how seasonal environmental dynamics can shape the community structure and metabolisms of microbial mats, ultimately controlling biogeochemical cycling in these ecological hotspots.

microbiology↗

bioRxiv2022

The Western Lake Erie Culture Collection: A promising resource for evaluating the physiological and genetic diversity of Microcystis and its associated microbiome

Cyanobacteria harmful algal blooms (cyanoHABs) dominated by Microcystis spp. have significant public health and economic implications in freshwater bodies around the world. These blooms are capable of producing a variety of cyanotoxins, including microcystins, that affect fishing and tourism industries, human and environmental health, and access to drinking water. In this study, we isolated and sequenced the genomes of 21 unialgal Microcystis cultures collected from western Lake Erie between 2017-2019. While some cultures isolated in different years have a high degree of genetic similarity (Average Nucleotide Identity >99%), genomic data shows that these cultures also represent much of the breadth of known Microcystis diversity in natural populations. Only 5 isolates contained all the genes required for microcystin synthesis while 2 isolates contained a previously described partial mcy operon. Microcystin production within cultures was also assessed using Enzyme-Linked Immunosorbent Assay (ELISA) and supported genomic results with high concentrations (up to 900 g L-1) in cultures with complete mcy operons and no or low toxin detected otherwise. These xenic cultures also contained a substantial diversity of bacteria associated with Microcystis, which has become increasingly recognized as an essential component of cyanoHAB community dynamics. These results highlight the genomic diversity among Microcystis strains and associated bacteria in Lake Erie, and their potential impacts on bloom development, toxin production, and toxin degradation. This collection significantly increases the availability of environmentally relevant Microcystis strains from temperate North America, which is changing rapidly due to climate change. HighlightsO_LITwenty one xenic Microcystis cultures were isolated from western Lake Erie and capture the diversity of Microcystis strains observed in natural populations as well as their associated bacteria C_LIO_LIMicrocystis strains show variability in core and accessory gene content, and genetically similar strains produce varying concentrations and congeners of microcystins C_LIO_LIThis collection is a valuable resource for studying strain diversity and interactions between Microcystis and associated bacteria C_LIO_LIOur collection increases the availability of environmentally relevant strains from temperate North America, which is historically underrepresented in culture collections. C_LI

microbiology↗

bioRxiv2022

Expression of Microcystis biosynthetic gene clusters in natural populations suggests temporally dynamic synthesis of novel and known secondary metabolites in western Lake Erie

SummaryMicrocystis spp. produces diverse secondary metabolites within freshwater cyanoHABs around the world. In addition to the biosynthetic gene clusters (BGCs) encoding known compounds, Microcystis genomes harbor numerous BGCs of unknown function, indicating its poorly understood chemical repertoire. While recent studies show that Microcystis produces several metabolites in the lab and field, little work has focused on analyzing the abundance and expression of its broader suite of BGCs during cyanoHAB events. Here, we use metagenomic and metatranscriptomic approaches to track the relative abundance of Microcystis BGCs and their transcripts throughout the 2014 western Lake Erie cyanoHAB. Results indicate the presence of several transcriptionally active BGCs that are predicted to synthesize both known and novel secondary metabolites. The abundance and expression of these BGCs shifted throughout the bloom, with transcript abundance levels correlating with temperature, nitrate and phosphorus concentrations, and the abundance of co-occurring predatory and competitive eukaryotic microorganisms, suggesting the importance of both abiotic and biotic controls in regulating expression. This work highlights the need for understanding the chemical ecology and potential risks to human and environmental health posed by secondary metabolites that are produced but unmonitored, as well as the potential discovery of pharmaceutical compounds from cyanoHAB-derived BGCs. Originality-Statement of SignificanceMicrocystis spp. dominate cyanobacterial harmful algal blooms (cyanoHABs) worldwide and pose significant threats to water quality through the production of numerous secondary metabolites, many of which are toxic. While the toxicity and biochemistry of microcystins and several other compounds have been well studied, the broader suite of secondary metabolites produced by Microcystis remains poorly understood, leaving gaps in our understanding of their impacts on ecology, human and ecosystem health, or potential pharmaceutical application. In this study, we use metagenomic and transcriptomic datasets to examine the diversity of genes encoding synthesis of secondary metabolites in natural Microcystis populations and assess their patterns of transcription in the context of biotic and abiotic conditions in western Lake Erie cyanoHABs. Our results reveal the presence of a large diversity of both known gene clusters that encode toxic secondary metabolites as well as novel ones that encode cryptic compounds. This research highlights the need for targeted studies of the secondary metabolite diversity in western Lake Erie, a vital freshwater source to the United States and Canada.

microbiology↗

bioRxiv2022

Transcriptionally active nitrogen fixation and biosynthesis of diverse secondary metabolites by Dolichospermum and Aphanizominom-like Cyanobacteria in western Lake Erie Microcystis blooms

Cyanobacterial harmful algal blooms (cyanoHABs) in the western basin of Lake Erie are dominated by microcystin producing Microcystis spp., but other cyanobacterial taxa that coexist in these communities may play important roles in production of toxins and shaping bloom dynamics and community function. In this study, we used metagenomic and metatranscriptomic data from the 2014 western Lake Erie cyanoHAB to explore the genetic diversity and biosynthetic potential of cyanobacteria belonging to the Anabaena, Dolichospermum, Aphanizomenon (ADA) clade. We reconstructed two near-complete metagenome-assembled genomes from two distinct ADA clade species, each containing biosynthetic gene clusters that encode novel and known secondary metabolites that were transcriptionally active. These taxa also appear to have varying nutrient acquisition strategies, and their ability to fix N may be important for synthesizing N rich metabolites as well as supporting bloom persistence. Although not the dominant organism in this system, these results suggest that ADA may be important community members in western Lake Erie cyanoHABs that have the potential to produce unmonitored toxins. HighlightsO_LIThrough metagenomic approaches, we generated two near-complete metagenome assembled genomes from two distinct species that are dispersed across the ADA clade of cyanobacteria. C_LIO_LIThese ADA cyanobacteria have the potential to produce a variety of known and novel secondary metabolites, and use different nitrogen fixation strategies as observed through differential transcript abundance C_LIO_LIThis works highlights the diversity of cyanobacteria in western Lake Erie blooms despite their continued dominance by Microcystis, and that these less abundant cyanobacteria may produce unmonitored toxins and shape bloom dynamics through N-fixation. C_LI

microbiology↗

bioRxiv2022

The sulfur cycle connects microbiomes and biogeochemistry in deep-sea hydrothermal plumes

In globally distributed deep-sea hydrothermal vent plumes, microbiomes are shaped by the redox energy landscapes created by reduced hydrothermal vent fluids mixing with oxidized seawater. Plumes can disperse over thousands of kilometers and are complex. Their characteristics are determined by geochemical sources from hydrothermal vents, e.g., hydrothermal inputs, nutrients, and trace metals. However, the impacts of plume biogeochemistry on the oceans are poorly constrained due to a lack of integrated understanding of microbiomes, population genetics, and geochemistry. Here, we use microbial genomes to understand links between biogeography, evolution, and metabolic connectivity, and elucidate their impacts on biogeochemical cycling in the deep sea. Using data from 37 diverse plumes from 8 ocean basins, we show that sulfur metabolism defines the core microbiome of plumes and drives metabolic connectivity. Amongst all microbial metabolisms, sulfur transformations had the highest MW-score, a measure of metabolic connectivity in microbial communities. Our findings provide the ecological and evolutionary basis of change in sulfur-driven microbial communities and their population genetics in adaptation to changing geochemical gradients in the oceans.

microbiology↗