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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.more » « less
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Summary Global warming and eutrophication contribute to the worldwide increase in cyanobacterial blooms, and the level of cyanobacterial biomass is strongly associated with rises in methane emissions from surface lake waters. Hence, methane‐metabolizing microorganisms may be important for modulating carbon flow in cyanobacterial blooms. Here, we surveyed methanogenic and methanotrophic communities associated with floatingMicrocystisaggregates in 10 lakes spanning four continents, through sequencing of 16S rRNA and functional marker genes. Methanogenic archaea (mainlyMethanoregulaandMethanosaeta) were detectable in 5 of the 10 lakes and constituted the majority (~50%–90%) of the archaeal community in these lakes. Three of the 10 lakes contained relatively more abundant methanotrophs than the other seven lakes, with the methanotrophic generaMethyloparacoccus,Crenothrix, and an uncultured species related toMethylobacterdominating and nearly exclusively found in each of those three lakes. These three are among the five lakes in which methanogens were observed. Operational taxonomic unit (OTU) richness and abundance of methanotrophs were strongly positively correlated with those of methanogens, suggesting that their activities may be coupled. TheseMicrocystis‐aggregate‐associated methanotrophs may be responsible for a hitherto overlooked sink for methane in surface freshwaters, and their co‐occurrence with methanogens sheds light on the methane cycle in cyanobacterial aggregates.more » « less
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Abstract Bacteria play key roles in the function and diversity of aquatic systems, but aside from study of specific bloom systems, little is known about the diversity or biogeography of bacteria associated with harmful cyanobacterial blooms (cyanoHABs). CyanoHAB species are known to shape bacterial community composition and to rely on functions provided by the associated bacteria, leading to the hypothesized cyanoHAB interactome, a coevolved community of synergistic and interacting bacteria species, each necessary for the success of the others. Here, we surveyed the microbiome associated withMicrocystis aeruginosaduring blooms in 12 lakes spanning four continents as an initial test of the hypothesizedMicrocystisinteractome. We predicted that microbiome composition and functional potential would be similar across blooms globally. Our results, as revealed by 16S rRNA sequence similarity, indicate thatM. aeruginosais cosmopolitan in lakes across a 280° longitudinal and 90° latitudinal gradient. The microbiome communities were represented by a wide range of operational taxonomic units and relative abundances. Highly abundant taxa were more related and shared across most sites and did not vary with geographic distance, thus, likeMicrocystis, revealing no evidence for dispersal limitation. High phylogenetic relatedness, both within and across lakes, indicates that microbiome bacteria with similar functional potential were associated with all blooms. WhileMicrocystisand the microbiome bacteria shared many genes, whole‐community metagenomic analysis revealed a suite of biochemical pathways that could be considered complementary. Our results demonstrate a high degree of similarity across globalMicrocystisblooms, thereby providing initial support for the hypothesizedMicrocystisinteractome.more » « less
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