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1. Tracing the active genetic diversity of Microcystis and Microcystis phage through a temporal survey of Taihu

   https://doi.org/10.1371/journal.pone.0244482  

   Pound, Helena L.; Wilhelm, Steven W. (December 2020, PLOS ONE)

   Humbert, Jean-François (Ed.)

   Harmful algal blooms are commonly thought to be dominated by a single genus, but they are not homogenous communities. Current approaches, both molecular and culture-based, often overlook fine-scale variations in community composition that can influence bloom dynamics. We combined homology-based searches (BLASTX) and phylogenetics to distinguish and quantify Microcystis host and phage members across a summer season during a 2014 Microcystis- dominated bloom that occurred in Lake Tai ( Taihu ), China. We found 47 different genotypes of the Microcystis- specific DNA-dependent RNA polymerase ( rpo B), which included several morphospecies. Microcystis flos-aquae and Microcystis wesenbergii accounted for ~86% of total Microcystis transcripts, while the more commonly studied Microcystis aeruginosa only accounted for ~7%. Microcystis genotypes were classified into three temporal groups according to their expression patterns across the course of the bloom: early, constant and late. All Microcystis morphospecies were present in each group, indicating that expression patterns were likely dictated by competition driven by environmental factors, not phylogeny. We identified three primary Microcystis -infecting phages based on the viral terminase, including a novel Siphoviridae phage that may be capable of lysogeny. Within our dataset, Myoviridae phages consistent with those infecting Microcystis in a lytic manner were positively correlated to the early host genotypes, while the Siphoviridae phages were positively correlated to the late host genotypes, when the Myoviridae phages express putative genetic markers for lysogeny. The expression of genes in the microcystin-encoding mcy cassette was estimated using mcyA , which revealed 24 Microcystis- specific genotypes that were negatively correlated to the early host genotypes. Of all environmental factors measured, pH best described the temporal shift in the Microcystis community genotypic composition, promoting hypotheses regarding carbon concentration mechanisms and oxidative stress. Our work expounds on the complexity of HAB events, using a well-studied dataset to highlight the need for increased resolution of community dynamics. 

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2. Aerobic anoxygenic phototrophs play important roles in nutrient cycling within cyanobacterial Microcystis bloom microbiomes

   https://doi.org/10.1186/s40168-024-01801-4  

   Cai, Haiyuan; McLimans, Christopher_J; Jiang, Helong; Chen, Feng; Krumholz, Lee_R; Hambright, K_David (May 2024, Microbiome)

   Abstract BackgroundDuring the bloom season, the colonial cyanobacteriumMicrocystisforms complex aggregates which include a diverse microbiome within an exopolymer matrix. Early research postulated a simple mutualism existing with bacteria benefitting from the rich source of fixed carbon andMicrocystisreceiving recycled nutrients. Researchers have since hypothesized thatMicrocystisaggregates represent a community of synergistic and interacting species, an interactome, each with unique metabolic capabilities that are critical to the growth, maintenance, and demise ofMicrocystisblooms. Research has also shown that aggregate-associated bacteria are taxonomically different from free-living bacteria in the surrounding water. Moreover, research has identified little overlap in functional potential betweenMicrocystisand members of its microbiome, further supporting the interactome concept. However, we still lack verification of general interaction and know little about the taxa and metabolic pathways supporting nutrient and metabolite cycling withinMicrocystisaggregates. ResultsDuring a 7-month study of bacterial communities comparing free-living and aggregate-associated bacteria in Lake Taihu, China, we found that aerobic anoxygenic phototrophic (AAP) bacteria were significantly more abundant withinMicrocystisaggregates than in free-living samples, suggesting a possible functional role for AAP bacteria in overall aggregate community function. We then analyzed gene composition in 102 high-quality metagenome-assembled genomes (MAGs) of bloom-microbiome bacteria from 10 lakes spanning four continents, compared with 12 completeMicrocystisgenomes which revealed that microbiome bacteria andMicrocystispossessed complementary biochemical pathways that could serve in C, N, S, and P cycling. Mapping published transcripts fromMicrocystisblooms onto a comprehensive AAP and non-AAP bacteria MAG database (226 MAGs) indicated that observed high levels of expression of genes involved in nutrient cycling pathways were in AAP bacteria. ConclusionsOur results provide strong corroboration of the hypothesizedMicrocystisinteractome and the first evidence that AAP bacteria may play an important role in nutrient cycling withinMicrocystisaggregate microbiomes. 

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3. Genomic signatures of Lake Erie bacteria suggest interaction in the Microcystis phycosphere

   https://doi.org/10.1371/journal.pone.0257017  

   Hoke, Alexa K.; Reynoso, Guadalupe; Smith, Morgan R.; Gardner, Malia I.; Lockwood, Dominique J.; Gilbert, Naomi E.; Wilhelm, Steven W.; Becker, Isabella R.; Brennan, Grant J.; Crider, Katherine E.; et al (September 2021, PLOS ONE)

   Humbert, Jean-François (Ed.)

   Microbial interactions in harmful algal bloom (HAB) communities have been examined in marine systems, but are poorly studied in fresh waters. To investigate HAB-microbe interactions, we isolated bacteria with close associations to bloom-forming cyanobacteria, Microcystis spp., during a 2017 bloom in the western basin of Lake Erie. The genomes of five isolates ( Exiguobacterium sp. JMULE1, Enterobacter sp. JMULE2, Deinococcus sp. JMULE3, Paenibacillus sp. JMULE4, and Acidovorax sp. JMULE5.) were sequenced on a PacBio Sequel system. These genomes ranged in size from 3.1 Mbp ( Exiguobacterium sp. JMULE1) to 5.7 Mbp ( Enterobacter sp. JMULE2). The genomes were analyzed for genes relating to critical metabolic functions, including nitrogen reduction and carbon utilization. All five of the sequenced genomes contained genes that could be used in potential signaling and nutrient exchange between the bacteria and cyanobacteria such as Microcystis . Gene expression signatures of algal-derived carbon utilization for two isolates were identified in Microcystis blooms in Lake Erie and Lake Tai ( Taihu ) at low levels, suggesting these organisms are active and may have a functional role during Microcystis blooms in aggregates, but were largely missing from whole water samples. These findings build on the growing evidence that the bacterial microbiome associated with bloom-forming algae have the functional potential to contribute to nutrient exchange within bloom communities and interact with important bloom formers like Microcystis . 

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4. Contrasting drivers of abundant phage and prokaryotic communities revealed in diverse coastal ecosystems

   https://doi.org/10.1038/s43705-023-00333-6  

   Weinheimer, Alaina R; Aylward, Frank O; Leray, Matthieu; Scott, Jarrod J (December 2023, ISME Communications)

   Abstract Phages (viruses of bacteria and archaea) are a ubiquitous top-down control on microbial communities by selectively infecting and killing cells. As obligate parasites, phages are inherently linked to processes that impact their hosts’ distribution and physiology, but phages can also be impacted by external, environmental factors, such as UV radiation degrading their virions. To better understand these complex links of phages to their hosts and the environment, we leverage the unique ecological context of the Isthmus of Panama, which narrowly disconnects the productive Tropical Eastern Pacific (EP) and nutrient-poor Tropical Western Atlantic (WA) provinces. We could thus compare patterns of phage and prokaryotic communities at both global scales (between oceans) and local-scales (between habitats within an ocean). Although both phage and prokaryotic communities differed sharply between the oceans, phage community composition did not significantly differ between mangroves and reefs of the WA, while prokaryotic communities were distinct. These results suggest phages are more shaped by dispersal processes than local conditions regardless of spatial scale, while prokaryotes tend to be shaped by local conditions at smaller spatial scales. Collectively, we provide a framework for addressing the co-variability between phages and prokaryotes in marine systems and identifying factors that drive consistent versus disparate trends in community shifts, essential to informing models of biogeochemical cycles that include these interactions. 

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5. 16S rRNA/rRNA Gene Ratios and Cell Activity Staining Reveal Consistent Patterns of Microbial Activity in Plant-Associated Soil

   https://doi.org/10.1128/mSystems.00003-19  

   Bowsher, Alan W.; Kearns, Patrick J.; Shade, Ashley; Deveau, Aurélie (April 2019, mSystems)

   ABSTRACT At any given time, only a subset of microbial community members are active in their environment. The others are in a state of dormancy, with strongly reduced metabolic rates. It is of interest to distinguish active and inactive microbial cells and taxa to understand their functional contributions to ecosystem processes and to understand shifts in microbial activity in response to change. Of the methods used to assess microbial activity-dormancy dynamics, 16S rRNA/rRNA gene amplicons (16S ratios) and active cell staining with 5-cyano-2,3-ditolyl tetrazolium chloride (CTC) are two of the most common, yet each method has limitations. Given that in situ activity-dormancy dynamics are proxied only by laboratory methods, further study is needed to assess the level of agreement and potential complementarity of these methods. We conducted two experiments investigating microbial activity in plant-associated soils. First, we treated corn field soil with phytohormones to simulate plant soil stress signaling, and second, we used rhizosphere soil from common bean plants exposed to drought or nutrient enrichment. Overall, the 16S ratio and CTC methods exhibited similar patterns of relative activity across treatments when treatment effects were large, and the instances in which they differed could be attributed to changes in community size (e.g., cell death or growth). Therefore, regardless of the method used to assess activity, we recommend quantifying community size to inform ecological interpretation. Our results suggest that the 16S ratio and CTC methods report comparable patterns of activity that can be applied to observe ecological dynamics over time, space, or experimental treatment. IMPORTANCE Although the majority of microorganisms in natural ecosystems are dormant, relatively little is known about the dynamics of the active and dormant microbial pools through both space and time. The limited knowledge of microbial activity-dormancy dynamics is in part due to uncertainty in the methods currently used to quantify active taxa. Here, we directly compared two of the most common methods (16S ratios and active cell staining) for estimating microbial activity in plant-associated soil and found that they were largely in agreement in the overarching patterns. Our results suggest that 16S ratios and active cell staining provide complementary information for measuring and interpreting microbial activity-dormancy dynamics in soils. They also support the idea that 16S rRNA/rRNA gene ratios have comparative value and offer a high-throughput, sequencing-based option for understanding relative changes in microbiome activity, as long as this method is coupled with quantification of community size. 

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