{"title":"Grazer‐induced toxin production is energetically costly and significantly reduces growth of cylindrospermopsin‐producing cyanobacteria","authors":"Lamei Lei, Wei Liu, Zihan Chen, Liang Peng, Li‐Juan Xiao, Bo‐Ping Han, Brett A. Neilan","doi":"10.1002/lno.12721","DOIUrl":null,"url":null,"abstract":"Toxins have been proposed as a defense mechanism for phytoplankton against zooplankton grazing. However, the associated costs are not understood. Here, we aim to reveal the costs in terms of both physiological and molecular responses in the cylindrospermopsin (CYN)‐producing cyanobacterium <jats:italic>Raphidiopsis raciborskii</jats:italic>. Exposure of <jats:italic>R. raciborskii</jats:italic> to <jats:italic>Daphnia magna</jats:italic> resulted in a significant increase in its CYN cell quota which was grazer cell density‐dependent, indicating an inducible effect on CYN production. A negative and significant relationship between cellular growth rate and CYN production suggested a growth‐defense trade‐off, highlighting the costly nature of toxin production. Despite strong transcriptional responses (121 differentially expressed genes) in <jats:italic>R. raciborskii</jats:italic> under grazing pressure, the CYN gene cluster remained largely unaffected, implying post‐transcriptional regulation of CYN biosynthesis. Significant variation was observed in transcripts for phosphorus metabolism and photosynthesis‐related genes, and evidenced that energy (ATP) metabolic processes were stimulated. This study is the first to demonstrate the high energy requirements for CYN production and provide insight into the molecular basis underlying the costs of toxin production.","PeriodicalId":18143,"journal":{"name":"Limnology and Oceanography","volume":null,"pages":null},"PeriodicalIF":3.8000,"publicationDate":"2024-10-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Limnology and Oceanography","FirstCategoryId":"89","ListUrlMain":"https://doi.org/10.1002/lno.12721","RegionNum":1,"RegionCategory":"地球科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"LIMNOLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
Toxins have been proposed as a defense mechanism for phytoplankton against zooplankton grazing. However, the associated costs are not understood. Here, we aim to reveal the costs in terms of both physiological and molecular responses in the cylindrospermopsin (CYN)‐producing cyanobacterium Raphidiopsis raciborskii. Exposure of R. raciborskii to Daphnia magna resulted in a significant increase in its CYN cell quota which was grazer cell density‐dependent, indicating an inducible effect on CYN production. A negative and significant relationship between cellular growth rate and CYN production suggested a growth‐defense trade‐off, highlighting the costly nature of toxin production. Despite strong transcriptional responses (121 differentially expressed genes) in R. raciborskii under grazing pressure, the CYN gene cluster remained largely unaffected, implying post‐transcriptional regulation of CYN biosynthesis. Significant variation was observed in transcripts for phosphorus metabolism and photosynthesis‐related genes, and evidenced that energy (ATP) metabolic processes were stimulated. This study is the first to demonstrate the high energy requirements for CYN production and provide insight into the molecular basis underlying the costs of toxin production.
毒素被认为是浮游植物抵御浮游动物掠食的一种防御机制。然而,相关的代价却不为人所知。在这里,我们旨在从生理和分子反应两方面揭示产生圆柱状红藻毒素(CYN)的蓝藻 Raphidiopsis raciborskii 的代价。将 R. raciborskii 暴露于大型蚤后,其 CYN 细胞配额显著增加,而这与捕食者细胞密度有关,表明 CYN 的产生具有诱导效应。细胞生长率与 CYN 产量之间的显著负相关关系表明了生长与防御之间的权衡,突出了毒素生产的高成本性质。尽管在放牧压力下 R. raciborskii 的转录反应强烈(121 个差异表达基因),但 CYN 基因簇基本不受影响,这意味着 CYN 生物合成受转录后调控。在磷代谢和光合作用相关基因的转录本中观察到了显著的变化,证明能量(ATP)代谢过程受到了刺激。这项研究首次证明了 CYN 生产对能量的高要求,并深入探讨了毒素生产成本的分子基础。
期刊介绍:
Limnology and Oceanography (L&O; print ISSN 0024-3590, online ISSN 1939-5590) publishes original articles, including scholarly reviews, about all aspects of limnology and oceanography. The journal''s unifying theme is the understanding of aquatic systems. Submissions are judged on the originality of their data, interpretations, and ideas, and on the degree to which they can be generalized beyond the particular aquatic system examined. Laboratory and modeling studies must demonstrate relevance to field environments; typically this means that they are bolstered by substantial "real-world" data. Few purely theoretical or purely empirical papers are accepted for review.