Genetic, metabolic and toxicological diversity within Prymnesium parvum (Haptophyte) from Polish waterbodies

IF 11.4 1区环境科学与生态学 Q1 ENGINEERING, ENVIRONMENTAL

Water Research Pub Date : 2025-04-29 DOI:10.1016/j.watres.2025.123744

Hanna Mazur-Marzec, Michał Grabski, Robert Konkel, Marta Cegłowska, Zuzanna Cyske, Lidia Gaffke, Łukasz Grabowski, Anastasia Hiskia, Marek Kajs, Triantafyllos Kaloudis, Agnieszka Napiórkowska-Krzebietke, Karolina Pierzynowska, Estera Rintz, Sofia Iliakopoulou, Semko Walat, Sevasti-Kiriaki Zervou, Monika Zielenkiewicz, Grzegorz Węgrzyn

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引用次数: 0

Abstract

Toxic blooms of Prymnesium parvum pose one of the most serious environmental threats. This alga occurs worldwide and has devastating effects on gill-breathing organisms inhabiting inland waters. In 2022, Polish society was faced with the problem for the first time. A high biomass of P. parvum in the Gliwice Canal, the Odra River and the oxbow lakes resulted in large-scale fish kills and significant economic losses. Since then, the toxic alga has become a permanent component of the Gliwice Canal phytoplankton community. Studies on P. parvum from other geographical regions have revealed existence of genotypic and phenotypic variation between and within the populations. Therefore, it was important to examine the specific characteristics of P. parvum from Polish water bodies. Here, we present the results of studies on the dynamics of B-type prymnesins (PRMs) production by P. parvum in the Gliwice Canal in 2023. For the purpose of the study, three B-type PRM variants were isolated and used as standards for toxins quantification and toxicity assessment. Differences in cytotoxicity of three isolated B-type prymnesins against fish (RTgill-W1) and human cells (fibroblasts – HDFa and lung cancer cells – A549) were documented for the first time. The lack of a clear correlation between the number of P. parvum cells and PRMs concentration indicates the heterogeneity of the population. Molecular characterisation of P. parvum CCNP2001 strain from Polish waters was also performed. The genome of the strain was sequenced, and the organisation of the PKZILLA genes involved in the biosynthesis of PRMs was described. These genes were present in all analysed bloom samples and in the isolated P. parvum strain. Analysis of the 5.8S rRNA gene sequence yielded unexpected results which indicated that CCNP2001 belongs to a type A prymnesin-producing strain. Additionally, high-resolution mass spectrometry analyses revealed the presence of A-type prymnesin in CCNP2001, supporting the findings of the genetic studies. This study also represents the first investigation into the impact of environmental conditions on the expression of the PKZILLA-1 and PKAZILLA-2 genes in P. parvum. The obtained results were compared to prymnesin production level. Our broad-scale studies provided new data on the dynamics, toxicity of PRMs, and molecular characteristics of P. parvum from Polish waterbodies. The results also highlighted existing gaps in knowledge regarding population diversity, the role of prymnesins, and potentially other metabolites, in harmful effects of P. parvum blooms.

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波兰水体小水蚤的遗传、代谢和毒理学多样性

小樱草（Prymnesium parvum）的毒华是最严重的环境威胁之一。这种藻类出现在世界各地，对居住在内陆水域的鳃呼吸生物具有破坏性影响。2022年，波兰社会第一次面临这个问题。Gliwice运河、Odra河和牛轭湖中细小疟原虫的高生物量导致了大规模的鱼类死亡和重大的经济损失。从那时起，这种有毒藻类就成为了格利维斯运河浮游植物群落的永久组成部分。对来自其他地理区域的小疟原虫的研究表明种群之间和种群内部存在基因型和表型变异。因此，研究波兰水体中细小疟原虫的具体特征非常重要。本文介绍了2023年Gliwice运河中P. parvum产生b型prymnesins （PRMs）的动态研究结果。本研究分离了3种b型PRM变体，并将其作为毒素定量和毒性评估的标准。首次报道了三种分离的b型prymnesins对鱼（RTgill-W1）和人细胞（成纤维细胞- HDFa和肺癌细胞- A549）的细胞毒性差异。细小疟原虫细胞数量与PRMs浓度之间缺乏明确的相关性，表明该种群存在异质性。对波兰水域的小疟原虫CCNP2001株进行了分子鉴定。对该菌株的基因组进行了测序，并描述了参与PRMs生物合成的PKZILLA基因的组织结构。这些基因存在于所有分析的水华样品和分离的细小疟原虫菌株中。对5.8S rRNA基因序列的分析结果表明，CCNP2001属于a型产朊酶菌株。此外，高分辨率质谱分析显示CCNP2001中存在a型prymnesin，支持遗传研究的发现。该研究也首次研究了环境条件对小孢子虫PKZILLA-1和PKAZILLA-2基因表达的影响。所得结果与原赖氨酸生产水平进行了比较。我们的大规模研究为波兰水体中PRMs的动力学、毒性和细小疟原虫的分子特征提供了新的数据。研究结果还强调了在种群多样性、prymnesins的作用以及潜在的其他代谢物等方面存在的知识空白。

本文章由计算机程序翻译，如有差异，请以英文原文为准。

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来源期刊

Water Research 环境科学-工程：环境

CiteScore

20.80

自引率

9.40%

发文量

1307

审稿时长

38 days

期刊介绍： Water Research, along with its open access companion journal Water Research X, serves as a platform for publishing original research papers covering various aspects of the science and technology related to the anthropogenic water cycle, water quality, and its management worldwide. The audience targeted by the journal comprises biologists, chemical engineers, chemists, civil engineers, environmental engineers, limnologists, and microbiologists. The scope of the journal include: •Treatment processes for water and wastewaters (municipal, agricultural, industrial, and on-site treatment), including resource recovery and residuals management; •Urban hydrology including sewer systems, stormwater management, and green infrastructure; •Drinking water treatment and distribution; •Potable and non-potable water reuse; •Sanitation, public health, and risk assessment; •Anaerobic digestion, solid and hazardous waste management, including source characterization and the effects and control of leachates and gaseous emissions; •Contaminants (chemical, microbial, anthropogenic particles such as nanoparticles or microplastics) and related water quality sensing, monitoring, fate, and assessment; •Anthropogenic impacts on inland, tidal, coastal and urban waters, focusing on surface and ground waters, and point and non-point sources of pollution; •Environmental restoration, linked to surface water, groundwater and groundwater remediation; •Analysis of the interfaces between sediments and water, and between water and atmosphere, focusing specifically on anthropogenic impacts; •Mathematical modelling, systems analysis, machine learning, and beneficial use of big data related to the anthropogenic water cycle; •Socio-economic, policy, and regulations studies.