The Importance of Allelopathic Picocyanobacterium Synechococcus sp. on the Abundance, Biomass Formation, and Structure of Phytoplankton Assemblages in Three Freshwater Lakes

Bubak, Iwona; Śliwińska‐Wilczewska, Sylwia; Głowacka, Paulina; Szczerba, Agnieszka; Możdżeń, Katarzyna

doi:10.3390/toxins12040259

Cited by 15 publications

(11 citation statements)

References 65 publications

(92 reference statements)

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“…Not all cyanobacteria are affected by 7dSh treatment: while several species are only affected in high concentrations ( Figure 3 ), others are completely growth inhibited or even lysed at low μM concentrations of 7dSh ( A. variabilis , Oscillatoria accuminata , Figure 3 ; Brilisauer et al, 2019 ). In complex communities involving different species, it is common that some species remain sensitive towards allelopathic inhibitors, whereas others develop strategies to tolerate the compounds ( Bubak et al, 2020 ). The isolation of spontaneous 7dSh-resistant mutants demonstrates that cyanobacteria can easily adapt to the inhibitor.…”

Section: Discussionmentioning

confidence: 99%

In vivo Inhibition of the 3-Dehydroquinate Synthase by 7-Deoxysedoheptulose Depends on Promiscuous Uptake by Sugar Transporters in Cyanobacteria

et al. 2021

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7-Deoxysedoheptulose (7dSh) is a bioactive deoxy-sugar actively excreted by the unicellular cyanobacterium Synechococcus elongatus PCC 7942 (S. elongatus) but also Streptomyces setonensis. In our previous publications we have shown that in S. elongatus, 7dSh is exclusively synthesized by promiscuous enzyme activity from an inhibitory by-product of radical SAM enzymes, without a specific gene cluster being involved. Additionally, we showed that 7dSh inhibits the growth of cyanobacteria, but also the growth of plants and fungi, presumably by inhibiting the 3-dehydroquinate synthase (DHQS), the second enzyme of the shikimate pathway, as the substrate of this enzyme strongly accumulates in cells treated with 7dSh. In this study, by using purified DHQS of Anabaena variabilis ATCC 29413 (A. variabilis) we biochemically confirmed that 7dSh is a competitive inhibitor of this enzyme. By analyzing the effect of 7dSh on a subset of cyanobacteria from all the five subsections, we identified different species whose growth was inhibited by 7dSh. We also found that in some of the susceptible cyanobacteria import of 7dSh is mediated by structurally different and promiscuous transporters: 7dSh can be taken up by the fructose ABC-transporter in A. variabilis and via the glucose permease in Synechocystis sp. PCC 6803 (Synechocystis sp.). In both cases, an effective uptake and thereby intracellular enrichment of 7dSh was essential for the inhibitory activity. Importantly, spontaneous mutations in the sugar transporters of A. variabilis and Synechocystis sp. not only disabled growth of the two strains on fructose and glucose, respectively, but also almost abolished their sensitivity to 7dSh. Although we have clearly shown in these examples that the effective uptake plays an essential role in the inhibitory effect of 7dSh, questions remain about how 7dSh resistance works in other (cyano)bacteria. Also, the involvement of a putative ribokinase in 7dSh resistance in the producer strain S. elongatus remained to be further investigated. Overall, these data establish 7dSh as the first allelochemical targeting the shikimate pathway in other cyanobacteria and plants and suggest a role of 7dSh in niche competition.

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Section: Discussionmentioning

confidence: 99%

In vivo Inhibition of the 3-Dehydroquinate Synthase by 7-Deoxysedoheptulose Depends on Promiscuous Uptake by Sugar Transporters in Cyanobacteria

et al. 2021

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“…Allelopathic activity of Synechococcus sp. was found in fresh waters [53][54][55], but few evidences were found in marine strains, which might also be an importance influence of the Synechococcus population dynamics when competing with other phytoplankton. The relative importance of abiotic and biotic factors in controlling ecotypes of these picocyanobacteria has to be further investigated.…”

Section: Discussionmentioning

confidence: 96%

Dynamics and Distribution of Marine Synechococcus Abundance and Genotypes during Seasonal Hypoxia in a Coastal Marine Ranch

Song

Zheng

et al. 2021

JMSE

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Marine Synechococcus are an ecologically important picocyanobacterial group widely distributed in various oceanic environments. Little is known about the dynamics and distribution of Synechococcus abundance and genotypes during seasonal hypoxia in coastal zones. In this study, an investigation was conducted in a coastal marine ranch along two transects in Muping, Yantai, where hypoxic events (defined here as the dissolved oxygen concentration <3 mg L−1) occurred in the summer of 2015. The hypoxia occurred in the bottom waters from late July and persisted until late August. It was confined at nearshore stations of the two transects, one running across a coastal ranch and the other one outside. During this survey, cell abundance of Synechococcus was determined with flow cytometry, showing great variations ranging from 1 × 104 to 3.0 × 105 cells mL−1, and a bloom of Synechococcus occurred when stratification disappeared and hypoxia faded out outside the ranch. Regression analysis indicated that dissolved oxygen, pH, and inorganic nutrients were the most important abiotic factors in explaining the variation in Synechococcus cell abundance. Diverse genotypes (mostly belonged to the sub-clusters 5.1 and 5.2) were detected using clone library sequencing and terminal restriction fragment length polymorphism analysis of the 16S–23S rRNA internal transcribed spacer region. The richness of genotypes was significantly related to salinity, temperature, silicate, and pH, but not dissolved oxygen. Two environmental factors, temperature and salinity, collectively explained 17% of the variation in Synechococcus genotype assemblage. With the changes in population composition in diverse genotypes, the Synechococcus assemblages survived in the coastal hypoxia event and thrived when hypoxia faded out.

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“…can have an adverse effect on co-occurring species. Indeed, such effects have been observed for freshwater Synechococcus spp., which were able to impact the growth of other freshwater cyanobacteria or green algae [ 66 , 67 ]. Adverse effects caused by allelopathic compounds from marine Synechococcus spp.…”

Section: Discussionmentioning

confidence: 99%

“…This suggests that, if Synechococcus outcompetes Planktothrix in its ecological niche, allelopathic compounds (such as toxins), amongst other factors, may be used to compete against the respective other species. Indeed, allelopathic activity is one of the major competitive strategies of freshwater Synechococcus against coexisting phytoplankton species [ 66 ], further supporting the potential role of picocyanobacterial exudates in competition with other cyanobacteria, such as Planktothrix . Counterintuitively, some freshwater Synechococcus spp.…”

Section: Discussionmentioning

confidence: 99%

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Is Toxin-Producing Planktothrix sp. an Emerging Species in Lake Constance?

Fournier

Riehle

Dietrich

et al. 2021

Toxins

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Recurring blooms of filamentous, red-pigmented and toxin-producing cyanobacteria Planktothrix rubescens have been reported in numerous deep and stratified prealpine lakes, with the exception of Lake Constance. In a 2019 and 2020 Lake Constance field campaign, we collected samples from a distinct red-pigmented biomass maximum below the chlorophyll-a maximum, which was determined using fluorescence probe measurements at depths between 18 and 20 m. Here, we report the characterization of these deep water red pigment maxima (DRM) as cyanobacterial blooms. Using 16S rRNA gene-amplicon sequencing, we found evidence that the blooms were, indeed, contributed by Planktothrix spp., although phycoerythrin-rich Synechococcus taxa constituted most of the biomass (>96% relative read abundance) of the cyanobacterial DRM community. Through UPLC–MS/MS, we also detected toxic microcystins (MCs) in the DRM in the individual sampling days at concentrations of ≤1.5 ng/L. Subsequently, we reevaluated the fluorescence probe measurements collected over the past decade and found that, in the summer, DRM have been present in Lake Constance, at least since 2009. Our study highlights the need for a continuous monitoring program also targeting the cyanobacterial DRM in Lake Constance, and for future studies on the competition of the different cyanobacterial taxa. Future studies will address the potential community composition changes in response to the climate change driven physiochemical and biological parameters of the lake.

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The Importance of Allelopathic Picocyanobacterium Synechococcus sp. on the Abundance, Biomass Formation, and Structure of Phytoplankton Assemblages in Three Freshwater Lakes

Cited by 15 publications

References 65 publications

In vivo Inhibition of the 3-Dehydroquinate Synthase by 7-Deoxysedoheptulose Depends on Promiscuous Uptake by Sugar Transporters in Cyanobacteria

In vivo Inhibition of the 3-Dehydroquinate Synthase by 7-Deoxysedoheptulose Depends on Promiscuous Uptake by Sugar Transporters in Cyanobacteria

Dynamics and Distribution of Marine Synechococcus Abundance and Genotypes during Seasonal Hypoxia in a Coastal Marine Ranch

Is Toxin-Producing Planktothrix sp. an Emerging Species in Lake Constance?

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