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      UV radiation and temperature increase alter the PSII function and defense mechanisms in a bloom-forming cyanobacterium Microcystis aeruginosa

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          Abstract

          The aim was to determine the response of a bloom-forming Microcystis aeruginosa to climatic changes. Cultures of M. aeruginosa FACHB 905 were grown at two temperatures (25°C, 30°C) and exposed to high photosynthetically active radiation (PAR: 400–700 nm) alone or combined with UVR (PAR + UVR: 295–700 nm) for specified times. It was found that increased temperature enhanced M. aeruginosa sensitivity to both PAR and PAR + UVR as shown by reduced PSII quantum yields ( F v/F m ) in comparison with that at growth temperature (25°C), the presence of UVR significantly exacerbated the photoinhibition. M. aeruginosa cells grown at high temperature exhibited lower PSII repair rate ( K rec ) and sustained nonphotochemical quenching (NPQs) induction during the radiation exposure, particularly for PAR + UVR. Although high temperature alone or worked with UVR induced higher SOD and CAT activity and promoted the removal rate of PsbA, it seemed not enough to prevent the damage effect from them showing by the increased value of photoinactivation rate constant ( K pi ). In addition, the energetic cost of microcystin synthesis at high temperature probably led to reduced materials and energy available for PsbA turnover, thus may partly account for the lower K rec and the declination of photosynthetic activity in cells following PAR and PAR + UVR exposure. Our findings suggest that increased temperature modulates the sensitivity of M. aeruginosa to UVR by affecting the PSII repair and defense capacity, thus influencing competitiveness and abundance in the future water environment.

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          Most cited references54

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          How do plants feel the heat?

          In plants, the heat stress response (HSR) is highly conserved and involves multiple pathways, regulatory networks and cellular compartments. At least four putative sensors have recently been proposed to trigger the HSR. They include a plasma membrane channel that initiates an inward calcium flux, a histone sensor in the nucleus, and two unfolded protein sensors in the endoplasmic reticulum and the cytosol. Each of these putative sensors is thought to activate a similar set of HSR genes leading to enhanced thermotolerance, but the relationship between the different pathways and their hierarchical order is unclear. In this review, we explore the possible involvement of different thermosensors in the plant response to warming and heat stress. Copyright © 2011 Elsevier Ltd. All rights reserved.
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            The Cyanobacterial Hepatotoxin Microcystin Binds to Proteins and Increases the Fitness of Microcystis under Oxidative Stress Conditions

            Microcystins are cyanobacterial toxins that represent a serious threat to drinking water and recreational lakes worldwide. Here, we show that microcystin fulfils an important function within cells of its natural producer Microcystis. The microcystin deficient mutant ΔmcyB showed significant changes in the accumulation of proteins, including several enzymes of the Calvin cycle, phycobiliproteins and two NADPH-dependent reductases. We have discovered that microcystin binds to a number of these proteins in vivo and that the binding is strongly enhanced under high light and oxidative stress conditions. The nature of this binding was studied using extracts of a microcystin-deficient mutant in vitro. The data obtained provided clear evidence for a covalent interaction of the toxin with cysteine residues of proteins. A detailed investigation of one of the binding partners, the large subunit of RubisCO showed a lower susceptibility to proteases in the presence of microcystin in the wild type. Finally, the mutant defective in microcystin production exhibited a clearly increased sensitivity under high light conditions and after hydrogen peroxide treatment. Taken together, our data suggest a protein-modulating role for microcystin within the producing cell, which represents a new addition to the catalogue of functions that have been discussed for microbial secondary metabolites.
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              How rising CO2 and global warming may stimulate harmful cyanobacterial blooms.

              Climate change is likely to stimulate the development of harmful cyanobacterial blooms in eutrophic waters, with negative consequences for water quality of many lakes, reservoirs and brackish ecosystems across the globe. In addition to effects of temperature and eutrophication, recent research has shed new light on the possible implications of rising atmospheric CO2 concentrations. Depletion of dissolved CO2 by dense cyanobacterial blooms creates a concentration gradient across the air-water interface. A steeper gradient at elevated atmospheric CO2 concentrations will lead to a greater influx of CO2, which can be intercepted by surface-dwelling blooms, thus intensifying cyanobacterial blooms in eutrophic waters. Bloom-forming cyanobacteria display an unexpected diversity in CO2 responses, because different strains combine their uptake systems for CO2 and bicarbonate in different ways. The genetic composition of cyanobacterial blooms may therefore shift. In particular, strains with high-flux carbon uptake systems may benefit from the anticipated rise in inorganic carbon availability. Increasing temperatures also stimulate cyanobacterial growth. Many bloom-forming cyanobacteria and also green algae have temperature optima above 25°C, often exceeding the temperature optima of diatoms and dinoflagellates. Analysis of published data suggests that the temperature dependence of the growth rate of cyanobacteria exceeds that of green algae. Indirect effects of elevated temperature, like an earlier onset and longer duration of thermal stratification, may also shift the competitive balance in favor of buoyant cyanobacteria while eukaryotic algae are impaired by higher sedimentation losses. Furthermore, cyanobacteria differ from eukaryotic algae in that they can fix dinitrogen, and new insights show that the nitrogen-fixation activity of heterocystous cyanobacteria can be strongly stimulated at elevated temperatures. Models and lake studies indicate that the response of cyanobacterial growth to rising CO2 concentrations and elevated temperatures can be suppressed by nutrient limitation. The greatest response of cyanobacterial blooms to climate change is therefore expected to occur in eutrophic and hypertrophic lakes.
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                Author and article information

                Contributors
                URI : https://loop.frontiersin.org/people/440866/overviewRole: Role:
                URI : https://loop.frontiersin.org/people/2554189/overviewRole: Role: Role:
                URI : https://loop.frontiersin.org/people/1524220/overviewRole: Role: Role:
                URI : https://loop.frontiersin.org/people/497354/overviewRole: Role: Role: Role:
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                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                16 January 2024
                2024
                : 15
                : 1351796
                Affiliations
                [1] 1School of Life Science, Ludong University , Yantai, China
                [2] 2Key Laboratory of Marine Biotechnology in Universities of Shandong, Ludong University , Yantai, China
                Author notes

                Edited by: Feixue Fu, University of Southern California, United States

                Reviewed by: Gang Li, Chinese Academy of Sciences (CAS), China; Yaping Wu, Jiangsu Ocean Universiity, China; Peng Jin, University of Guangzhou, China

                *Correspondence: Hongyan Wu, sdwuhongyan@ 123456126.com

                These authors have contributed equally to this work

                Article
                10.3389/fmicb.2024.1351796
                10825000
                38292251
                a30f552c-a669-4b5d-95c6-10fe1018925c
                Copyright © 2024 Yan, Li, Zang, Xu, Bao and Wu.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 07 December 2023
                : 04 January 2024
                Page count
                Figures: 6, Tables: 1, Equations: 1, References: 54, Pages: 8, Words: 6336
                Funding
                The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work was supported by the National Natural Science Foundation of China (42376107, 42276119), the Provincial Natural Science Foundation of Shandong, China (ZR2023QD091).
                Categories
                Microbiology
                Original Research
                Custom metadata
                Aquatic Microbiology

                Microbiology & Virology
                microcystis aeruginosa,uv radiation,temperature,photosynthesis,cyanobacteria

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