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Impact of temperature on the temporal dynamics of microcystin in Microcystis aeruginosa PCC7806

Cyanobacterial blooms pose a serious threat to water quality and human health due to the production of the potent hepatotoxin microcystin. In microcystin-producing strains of the widespread genus Microcystis, the toxin is largely constitutively produced, but there are fluctuations between the cellul...

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Autores principales: Roy, Souvik, Guljamow, Arthur, Dittmann, Elke
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10500830/
https://www.ncbi.nlm.nih.gov/pubmed/37720143
http://dx.doi.org/10.3389/fmicb.2023.1200816
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author Roy, Souvik
Guljamow, Arthur
Dittmann, Elke
author_facet Roy, Souvik
Guljamow, Arthur
Dittmann, Elke
author_sort Roy, Souvik
collection PubMed
description Cyanobacterial blooms pose a serious threat to water quality and human health due to the production of the potent hepatotoxin microcystin. In microcystin-producing strains of the widespread genus Microcystis, the toxin is largely constitutively produced, but there are fluctuations between the cellular and extracellular pool and between free microcystin and protein-bound microcystin. Here we addressed the question of how different temperatures affect the growth and temporal dynamics of secondary metabolite production in the strain Microcystis aeruginosa PCC7806 and its microcystin-deficient ΔmcyB mutant. While the wild-type strain showed pronounced growth advantages at 20°C, 30°C, and 35°C, respectively, the ΔmcyB mutant was superior at 25°C. We further show that short-term incubations at 25°C–35°C result in lower amounts of freely soluble microcystin than incubations at 20°C and that microcystin congener ratios differ at the different temperatures. Subsequent assessment of the protein-bound microcystin pool by dot blot analysis and subcellular localization of microcystin using immunofluorescence microscopy showed re-localization of microcystin into the protein-bound pool combined with an enhanced condensation at the cytoplasmic membrane at temperatures above 25°C. This temperature threshold also applies to the condensate formation of the carbon-fixing enzyme RubisCO thereby likely contributing to reciprocal growth advantages of wild type and ΔmcyB mutant at 20°C and 25°C. We discuss these findings in the context of the environmental success of Microcystis at higher temperatures.
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spelling pubmed-105008302023-09-15 Impact of temperature on the temporal dynamics of microcystin in Microcystis aeruginosa PCC7806 Roy, Souvik Guljamow, Arthur Dittmann, Elke Front Microbiol Microbiology Cyanobacterial blooms pose a serious threat to water quality and human health due to the production of the potent hepatotoxin microcystin. In microcystin-producing strains of the widespread genus Microcystis, the toxin is largely constitutively produced, but there are fluctuations between the cellular and extracellular pool and between free microcystin and protein-bound microcystin. Here we addressed the question of how different temperatures affect the growth and temporal dynamics of secondary metabolite production in the strain Microcystis aeruginosa PCC7806 and its microcystin-deficient ΔmcyB mutant. While the wild-type strain showed pronounced growth advantages at 20°C, 30°C, and 35°C, respectively, the ΔmcyB mutant was superior at 25°C. We further show that short-term incubations at 25°C–35°C result in lower amounts of freely soluble microcystin than incubations at 20°C and that microcystin congener ratios differ at the different temperatures. Subsequent assessment of the protein-bound microcystin pool by dot blot analysis and subcellular localization of microcystin using immunofluorescence microscopy showed re-localization of microcystin into the protein-bound pool combined with an enhanced condensation at the cytoplasmic membrane at temperatures above 25°C. This temperature threshold also applies to the condensate formation of the carbon-fixing enzyme RubisCO thereby likely contributing to reciprocal growth advantages of wild type and ΔmcyB mutant at 20°C and 25°C. We discuss these findings in the context of the environmental success of Microcystis at higher temperatures. Frontiers Media S.A. 2023-08-31 /pmc/articles/PMC10500830/ /pubmed/37720143 http://dx.doi.org/10.3389/fmicb.2023.1200816 Text en Copyright © 2023 Roy, Guljamow and Dittmann. https://creativecommons.org/licenses/by/4.0/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.
spellingShingle Microbiology
Roy, Souvik
Guljamow, Arthur
Dittmann, Elke
Impact of temperature on the temporal dynamics of microcystin in Microcystis aeruginosa PCC7806
title Impact of temperature on the temporal dynamics of microcystin in Microcystis aeruginosa PCC7806
title_full Impact of temperature on the temporal dynamics of microcystin in Microcystis aeruginosa PCC7806
title_fullStr Impact of temperature on the temporal dynamics of microcystin in Microcystis aeruginosa PCC7806
title_full_unstemmed Impact of temperature on the temporal dynamics of microcystin in Microcystis aeruginosa PCC7806
title_short Impact of temperature on the temporal dynamics of microcystin in Microcystis aeruginosa PCC7806
title_sort impact of temperature on the temporal dynamics of microcystin in microcystis aeruginosa pcc7806
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10500830/
https://www.ncbi.nlm.nih.gov/pubmed/37720143
http://dx.doi.org/10.3389/fmicb.2023.1200816
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