Regulatory role of microcystin in the response of microcystin-producing cyanobacteria to elevated CO2: Insights from metabolic profiling

IF 4.6 2区 生物学 Q1 BIOTECHNOLOGY & APPLIED MICROBIOLOGY Algal Research-Biomass Biofuels and Bioproducts Pub Date : 2024-10-20 DOI:10.1016/j.algal.2024.103760
Jingjie Ma , Peifang Wang , Xun Wang , Bin Hu , Jin Qian
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Abstract

The regulatory role of microcystin in the response of microcystin-producing cyanobacteria to elevated CO2 remains poorly understood. To address this gap, this study compared the responses of wild-type toxic Microcystis PCC 7806 and its mcyB-knockout mutant to elevated CO2 using metabolomic profiling under nitrogen (N)-rich and N-poor conditions. Under N-poor conditions, elevated CO2 promoted carbohydrate synthesis and tricarboxylic acid cycle in both strains, without affecting their growth. Under N-rich conditions, both strains exhibited increased biomass with rising CO2 levels, attributed to enhanced carbohydrate synthesis, tricarboxylic acid cycle, glutamate-glutamine cycle, purine synthesis, and arginine synthesis. However, compared to the mutant, the proliferation of wild-type toxic Microcystis was less stimulated by elevated CO2. The difference was associated with its reduced activity in the pentose phosphate pathway, likely linked to microcystin synthesis. Besides, the difference was related to higher utilization of glutamate, arginine, and aspartate due to increased microcystin production, indicating the regulatory role of microcystin in the response of microcystin-producing cyanobacteria to elevated CO2. Importantly, elevated CO2 could enhance microcystin synthesis by promoting the production of carbon backbones (malonyl CoA), amino acids (including arginine, glutamate and aspartate) and methyl donors (S-adenosylmethionine) of the wild-type toxic Microcystis PCC 7806. Notably, sufficient nitrogen sources were required for increased amino acid and methyl donors synthesis at high CO2 concentration. The discovery revealed underlying mechanisms behind the potential for elevated CO2 levels to increase toxicity risk associated with Microcystis blooms.

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微囊藻毒素在产微囊藻蓝藻对高浓度 CO2 的反应中的调控作用:代谢剖析的启示
人们对微囊藻毒素在产微囊藻蓝藻对高浓度 CO2 的反应中的调控作用仍然知之甚少。为了填补这一空白,本研究比较了野生型毒性微囊藻 PCC 7806 及其 mcyB 基因敲除突变体在富氮和贫氮条件下对高浓度 CO2 的响应。在贫氮条件下,高浓度 CO2 促进了两株菌株的碳水化合物合成和三羧酸循环,但不影响其生长。在富氮条件下,随着二氧化碳水平的升高,两株菌株的生物量都有所增加,这归因于碳水化合物合成、三羧酸循环、谷氨酸-谷氨酰胺循环、嘌呤合成和精氨酸合成的增强。然而,与突变体相比,野生型毒性微囊藻的增殖受二氧化碳升高的刺激较小。这种差异与其磷酸戊糖途径活性降低有关,而磷酸戊糖途径可能与微囊藻毒素的合成有关。此外,这种差异还与微囊藻毒素产量增加导致谷氨酸、精氨酸和天冬氨酸的利用率提高有关,表明微囊藻毒素在产微囊藻蓝藻对高浓度 CO2 的反应中起着调节作用。重要的是,高浓度 CO2 可促进野生型毒性微囊藻 PCC 7806 的碳骨架(丙二酰 CoA)、氨基酸(包括精氨酸、谷氨酸和天门冬氨酸)和甲基供体(S-腺苷蛋氨酸)的产生,从而增强微囊藻毒素的合成。值得注意的是,在高浓度二氧化碳条件下,氨基酸和甲基供体的合成需要充足的氮源。这一发现揭示了二氧化碳浓度升高可能增加与微囊藻藻华相关的毒性风险的潜在机制。
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来源期刊
Algal Research-Biomass Biofuels and Bioproducts
Algal Research-Biomass Biofuels and Bioproducts BIOTECHNOLOGY & APPLIED MICROBIOLOGY-
CiteScore
9.40
自引率
7.80%
发文量
332
期刊介绍: Algal Research is an international phycology journal covering all areas of emerging technologies in algae biology, biomass production, cultivation, harvesting, extraction, bioproducts, biorefinery, engineering, and econometrics. Algae is defined to include cyanobacteria, microalgae, and protists and symbionts of interest in biotechnology. The journal publishes original research and reviews for the following scope: algal biology, including but not exclusive to: phylogeny, biodiversity, molecular traits, metabolic regulation, and genetic engineering, algal cultivation, e.g. phototrophic systems, heterotrophic systems, and mixotrophic systems, algal harvesting and extraction systems, biotechnology to convert algal biomass and components into biofuels and bioproducts, e.g., nutraceuticals, pharmaceuticals, animal feed, plastics, etc. algal products and their economic assessment
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