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The frequency and intensity of cyanobacterial blooms are increasing worldwide with major societal and economic costs. Interactions between toxic cyanobacteria and eukaryotic algal competitors can affect toxic bloom formation, but the exact mechanisms of interspecies interactions remain unknown. Using metabolomic and proteomic profiling of co-cultures of the toxic cyanobacterium Microcystis aeruginosa with a green alga as well as of microorganisms collected in a Microcystis spp. bloom in Lake Taihu (China), we disentangle novel interspecies allelopathic interactions. We describe an interspecies molecular network in which M. aeruginosa inhibits growth of Chlorella vulgaris , a model green algal competitor, via the release of linoleic acid. In addition, we demonstrate how M. aeruginosa takes advantage of the cell signaling compound nitric oxide produced by C. vulgaris , which stimulates a positive feedback mechanism of linoleic acid release by M. aeruginosa and its toxicity. Our high-throughput system-biology approach highlights the importance of previously unrecognized allelopathic interactions between a broadly distributed toxic cyanobacterial bloom former and one of its algal competitors.

SignificanceCyanobacterial blooms pose a major threat to the water quality of many eutrophic lakes and reservoirs. Cyanobacteria are thought to be very effective competitors when CO2 levels are depleted during dense blooms. Their response to elevated CO2 is less understood, however. We study competition among cyanobacteria, and find both laboratory and field evidence for natural selection of strains with different carbon uptake systems at different CO2 levels. Our results demonstrate that changes in inorganic carbon availability act as an important selective factor in cyanobacterial communities and suggest that future harmful cyanobacterial blooms will have a genotype composition that differs from contemporary blooms and will be tuned to the high-CO2 conditions. Rising atmospheric CO2 concentrations are likely to affect many ecosystems worldwide. However, to what extent elevated CO2 will induce evolutionary changes in photosynthetic organisms is still a major open question. Here, we show rapid microevolutionary adaptation of a harmful cyanobacterium to changes in inorganic carbon (Ci) availability. We studied the cyanobacterium Microcystis, a notorious genus that can develop toxic cyanobacterial blooms in many eutrophic lakes and reservoirs worldwide. Microcystis displays genetic variation in the Ci uptake systems BicA and SbtA, where BicA has a low affinity for bicarbonate but high flux rate, and SbtA has a high affinity but low flux rate. Our laboratory competition experiments show that bicA + sbtA genotypes were favored by natural selection at low CO2 levels, but were partially replaced by the bicA genotype at elevated CO2. Similarly, in a eutrophic lake, bicA + sbtA strains were dominant when Ci concentrations were depleted during a dense cyanobacterial bloom, but were replaced by strains with only the high-flux bicA gene when Ci concentrations increased later in the season. Hence, our results provide both laboratory and field evidence that increasing carbon concentrations induce rapid adaptive changes in the genotype composition of harmful cyanobacterial blooms.

Traditionally, it has often been hypothesized that cyanobacteria are superior competitors at low CO2 and high pH in comparison with eukaryotic algae, owing to their effective CO2-concentrating mechanism (CCM). However, recent work indicates that green algae can also have a sophisticated CCM tuned to low CO2 levels. Conversely, cyanobacteria with the high-flux bicarbonate uptake system BicA appear well adapted to high inorganic carbon concentrations. To investigate these ideas we studied competition between three species of green algae and a bicA strain of the harmful cyanobacterium Microcystis aeruginosa at low (100 ppm) and high (2000 ppm) CO2. Two of the green algae were competitively superior to the cyanobacterium at low CO2, whereas the cyanobacterium increased its competitive ability with respect to the green algae at high CO2. The experiments were supported by a resource competition model linking the population dynamics of the phytoplankton species with dynamic changes in carbon speciation, pH and light. Our results show (i) that competition between phytoplankton species at different CO2 levels can be predicted from species traits in monoculture, (ii) that green algae can be strong competitors under CO2-depleted conditions, and (iii) that bloom-forming cyanobacteria with high-flux bicarbonate uptake systems will benefit from elevated CO2 concentrations.

Blooms of the toxin-producing cyanobacterium Microcystis are increasing globally, leading to the loss of ecosystem services, threats to human health, as well as the deaths of pets and husbandry animals. While nutrient availability is a well-known driver of algal biomass, the factors controlling “who” is present in fresh waters are more complicated. Microcystis possesses multiple strategies to adapt to temperature, light, changes in nutrient chemistry, herbivory, and parasitism that provide a selective advantage over its competitors. Blooms of the toxin-producing cyanobacterium Microcystis are increasing globally, leading to the loss of ecosystem services, threats to human health, as well as the deaths of pets and husbandry animals. While nutrient availability is a well-known driver of algal biomass, the factors controlling “who” is present in fresh waters are more complicated. Microcystis possesses multiple strategies to adapt to temperature, light, changes in nutrient chemistry, herbivory, and parasitism that provide a selective advantage over its competitors. Moreover, its ability to alter ecosystem pH provides it a further advantage that helps exclude many of its planktonic competitors. While decades of nutrient monitoring have provided us with the tools to predict the accumulation of phytoplankton biomass, here, we point to factors on the horizon that may inform us why Microcystis is presently the dominant bloom former in freshwaters around the world.

The local ecosystems, fishery and human health are all threatened by water blooms, so effectively controlling water blooms has become an urgent and challenging issue. Biological control of water blooms is given priority due to its low cost, high efficiency and environmental friendliness. In this study, Pseudomonas ZY-1 and Bacillus FY-1, two highly-effective algicidal bacteria strains which are able to indirectly lyse algae by separating and screening from the vigorous water body in the paddy alga of Northeast China were obtained. The two bacterial strains have stronger ability to lyse alga in the bacterial liquid concentration of 10 6 CFU/ml, and the alga-lysing rate on 7 d reached 84.03% and 83.11% respectively. The active substance secreted by ZY-1 is not sensitive to the changes of temperature and pH value, while as FY-1 cell-free filtrate is not stable in high temperature above 50 ℃ and pH of 5, it requires the sun light to have the algaecidal effect. The cell-free filtrates of strains ZY-1 and FY-1 had the best lysis effect on Microcystis aeruginosa cells , and the chlorophyll a content of algae decreased to 0.13 ± 0.02 mg/L and 0.14 ± 0.03 mg/L respectively and the Fv/Fm of Microcystis aeruginosa decreased by 97.22% after 7 days. The algaecidal process of ZY-1 and FY-1 may be that the cell-free filtrate inhibits the photosynthesis of Microcystis aeruginosa , and meanwhile it avoids the regeneration and repair of photosynthesis of algal cells by affecting the gene expression and damaging the repair system of algal cells, so the membrane lipid peroxidation is exacerbated and then the membrane of algal cells is broken, the algal cells can’t do normal life activities, and finally the algal cell would be killed. The rice seedlings in the algal liquid treatment group are short and show root dysplasia, few roots and brown roots. After treated with cell-free filtrate of ZY-1 and FY-1, the oxidative damage of the rice is obviously reduced, and the harm from Microcystis aeruginosa is reduced, which has the repair effect to the roots of rice seedlings and its aboveground growth. The cell-free filtrate of FY-1 works better than ZY-1. The bacteria strains of ZY-1 and FY-1 have the indirect algaecide trait, which makes them the potential environmentally-friendly algaecidal bacteria and they show broad application in the agricultural production and the control of water blooms.

The main goal of the present work is to test the hypothesis that small-scale turbulence affected physiological activities and the morphology of cyanobacteria in high turbulence environments. Using quantified turbulence in a stirring device, we conducted one set of experiments on cultures of two strains of cyanobacteria with different phenotypes; i.e., unicellular Microcystis flos-aquae and colonial Anabaena flos-aquae. The effect of small-scale turbulence examined varied from 0 to 8.01×10-2 m2s-3, covering the range of turbulence intensities experienced by cyanobacteria in the field. The results of photosynthesis activity and the cellular chlorophyll a in both strains did not change significantly among the turbulence levels, indicating that the potential indirect effects of a light regime under the gradient of turbulent mixing could be ignored. However, the experiments demonstrated that small-scale turbulence significantly modulated algal nutrient uptake and growth in comparison to the stagnant control. Cellular N and C of the two stains showed approximately the same responses, resulting in a similar pattern of C/N ratios. Moreover, the change in the phosphate uptake rate was similar to that of growth in two strains, which implied that growth characteristic responses to turbulence may be dependent on the P strategy, which was correlated with accumulation of polyphosphate. Additionally, our results also showed the filament length of A. flos-aquae decreased in response to high turbulence, which could favor enhancement of the nutrient uptake. These findings suggested that both M. flos-aquae and A. flos-aquae adjust their growth rates in response to turbulence levels in the ways of asynchronous cellular stoichiometry of C, N, and P, especially the phosphorus strategy, to improve the nutrient application efficiency. The fact that adaptation strategies of cyanobacteria diversely to turbulence depending on their physiological conditions presents a good example to understand the direct cause-effect relationship between hydrodynamic forces and algae.

Cyanobacteria are photosynthetic microorganisms that compose phytoplankton and therefore have a trophic relationship with zooplankton, which represent an important link for energy flux in aquatic food webs. Several species can form blooms and produce bioactive metabolites known as cyanotoxins. However, the ecological and adaptative role of these toxins are still under debate. Many studies have addressed the cyanotoxins’ function in defense against herbivory when grazing pressure by zooplankton plays a role in phytoplankton top-down control. Thus, the present study evaluated the ecophysiological responses of the cyanobacterial strain Microcystis aeruginosa NPLJ-4 underlying the chemical induced defense against the cladoceran Daphnia gessneri. Exposure to predator infochemicals consisted of cultures established in ASM-1 medium prepared in a filtrate from a culture of adults of D. gessneri at an environmentally relevant density. Daphnia infochemicals promoted a significant increase in toxin production by M. aeruginosa. However, no differences in growth were observed, despite a significant increase in both maximum photosynthetic efficiency and electron transport rate in response to zooplankton. Additionally, there was no significant variation in the production of exopolysaccharides. Overall, although a grazer-induced defense response was demonstrated, there were no effects on M. aeruginosa fitness, which maintained its growth in the presence of Daphnia alarm cues.

Flavonoids are natural polyphenolic compounds produced by many aquatic plants and released in their environments. In this study, the effects of several aquatic flavonoids on cyanobacterial Microcystis aeruginosa, especially in relation to the cell growth, photosynthetic activity, cell morphology, and cell membrane integrity, were investigated. Significant growth inhibition was observed when the cyanobacteria were exposed to three flavonoids, namely, 5,4'-dihydroxyflavone (DHF), apigenin, and luteolin. Luteolin reduced the effective quantum yield, photosynthetic efficiency, and maximal electron transport rate by 70%, 59% and 44%, respectively, whereas 5,4'-DHF and apigenin slightly affected these parameters, which implies that luteolin disrupts the photosynthetic system. Moreover, 5,4'-DHF and apigenin compromised the membrane integrity, and induced membrane depolarization in 52% and 38%, and permeabilization in 30% and 44% of the cells, respectively. The 5,4'-DHF and apigenin showed more pronounced effects on M. aeruginosa morphology and membrane integrity, compared to the luteolin. These results suggest that flavonoids could have significant effects on growth and physiological functions in cyanobacterial species.

  Prediction of the complex cyanobacteria-environment interactions is vital for understanding harmful bloom formation. Most previous studies on these interactions considered specific properties of cyanobacterial cells as representative for the entire population (e.g. growth rate, mortality, and photosynthetic capacity (Pmax)), and assumed that they remained spatiotemporally unchanged. Although, at the population level, the alteration of such traits can be driven by intraspecific competition, little is known about how traits and their plasticity change in response to environmental conditions and affect the bloom formation. Here we test the hypothesis that intraspecific variations in Pmax of cyanobacteria (Microcystis spp.) play an important role in its population dynamics. We coupled a one-dimensional hydrodynamic model with a trait-based phytoplankton model to simulate the effects of physical drivers (turbulence and turbidity) on the Pmax of Microcystis populations for a range of dynamic conditions typical for shallow eutrophic lakes. Our results revealed that turbulence acts as a directional selective driver for changes in Pmax. Depending on the intensity of daily-periodic turbulence, representing wind-driven mixing, a shift in population-averaged phenotypes occurred toward either low Pmax, allowing the population to capture additional light in the upper layers, or high Pmax, enhancing the efficiency of light utilization. Moreover, we observed that a high intraspecific diversity in Pmax accelerated the formation of surface scum by up to more than four times compared to a lower diversity. This study offers insights into mechanisms by which cyanobacteria populations respond to turbulence and underscores the significance of intraspecific variations in cyanobacterial bloom formation. Highlights 1) Numerical simulations of Microcystis population dynamics including intraspecific variations. 2) Moderate turbulence can induce a stable reduction in the photosynthetic capacity of the population. 3) High diversity in photosynthetic capacity accelerates scum formation.

This study assessed the distribution, abundance, and viability of pre- and post-overwintering Microcystis sediment seed stocks in Western Lake Erie and how these variables are potentially related to past and subsequent bloom formation. We conducted a two-year spatiotemporal survey of vegetative seed stocks in Western Lake Erie, the region where annual algal blooms generally develop. Sediment was collected from 16 sites covering an area of 375 km2 and water column depths ranging from 3-9 meters. Sample collection occurred in November 2014, April 2015, November 2015, and April 2016. The abundance of total and potentially-toxic Microcystis cell equivalents were determined using quantitative polymerase chain reaction. A series of laboratory experiments using lake sediment were conducted to assess the viability of Microcystis vegetative seed stocks. Across all sampling periods, the abundance of total Microcystis in the sediment ranged from 6.6 x 10(4) to 1.7 x 10(9) cell equivalents g-1, and potentially-toxic Microcystis ranged from 1.4 x 10(3) to 4.7 x 10(6) cell equivalents g-1. The percent potentially-toxic Microcystis in the sediment ranged from <1% to 68% across all samples. Total Microcystis abundance diminished significantly over winter with densities in spring nearly 10 times less than the previous fall. However, despite cell loss from fall to spring, lab experiments demonstrated that remaining non-toxic and potentially-toxic cells were viable after the overwintering period. Further, lab grow-out experiments indicate that potentially-toxic strains recruited at a slightly higher rate than non-toxic strains, and may in part, contribute to the pattern of higher relative toxicity during early stages of the blooms. The abundance and distribution of overwintering cells did not correlate strongly to areas in the lake where subsequent summer blooms were most persistent. However, numerical analysis suggests that recruitment of benthic overwintering populations could help explain a portion of the initial rapid increase in bloom biomass and the spatial extent of this bloom initiation, particularly when recruitment is paired with subsequent growth in appropriate water column conditions.