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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.

 

China has made a concerted effort to successfully improve water quality of rivers, but lake water quality has not improved. Lakes require controls on both catchment external nutrient loads and in-lake internal loads, where nature-based solutions are coupled with engineered systems to achieve the United Nations Sustainable Development Goals (SDGs).

 

ABSTRACT The frequency and intensity of cyanobacterial blooms are increasing worldwide. Interactions between toxic cyanobacteria and aquatic microorganisms need to be critically evaluated to understand microbial drivers and modulators of the blooms. In this study, we applied 16S/18S rRNA gene sequencing and metabolomics analyses to measure the microbial community composition and metabolic responses of the cyanobacterium Microcystis aeruginosa in a coculture system receiving dissolved inorganic nitrogen and phosphorus (DIP) close to representative concentrations in Lake Taihu, China. M. aeruginosa secreted alkaline phosphatase using a DIP source produced by moribund and decaying microorganisms when the P source was insufficient. During this process, M. aeruginosa accumulated several intermediates in energy metabolism pathways to provide energy for sustained high growth rates and increased intracellular sugars to enhance its competitive capacity and ability to defend itself against microbial attack. It also produced a variety of toxic substances, including microcystins, to inhibit metabolite formation via energy metabolism pathways of aquatic microorganisms, leading to a negative effect on bacterial and eukaryotic microbial richness and diversity. Overall, compared with the monoculture system, the growth of M. aeruginosa was accelerated in coculture, while the growth of some cooccurring microorganisms was inhibited, with the diversity and richness of eukaryotic microorganisms being more negatively impacted than those of prokaryotic microorganisms. These findings provide valuable information for clarifying how M. aeruginosa can potentially modulate its associations with other microorganisms, with ramifications for its dominance in aquatic ecosystems. IMPORTANCE We measured the microbial community composition and metabolic responses of Microcystis aeruginosa in a microcosm coculture system receiving dissolved inorganic nitrogen and phosphorus (DIP) close to the average concentrations in Lake Taihu. In the coculture system, DIP is depleted and the growth and production of aquatic microorganisms can be stressed by a lack of DIP availability. M. aeruginosa could accelerate its growth via interactions with specific cooccurring microorganisms and the accumulation of several intermediates in energy metabolism-related pathways. Furthermore, M. aeruginosa can decrease the carbohydrate metabolism of cooccurring aquatic microorganisms and thus disrupt microbial activities in the coculture. This also had a negative effect on bacterial and eukaryotic microbial richness and diversity. Microcystin was capable of decreasing the biomass of total phytoplankton in aquatic microcosms. Overall, compared to the monoculture, the growth of total aquatic microorganisms is inhibited, with the diversity and richness of eukaryotic microorganisms being more negatively impacted than those of prokaryotic microorganisms. The only exception is M. aeruginosa in the coculture system, whose growth was accelerated.