Epigenetic Regulation Links Bacterial Signaling to Growth and Reproductive Development in the Green Macroalga Ulva compressa (Chlorophyta)

IF 2.8 3区 生物学 Q3 BIOTECHNOLOGY & APPLIED MICROBIOLOGY
Janine F. M. Otto, Hermann Holbl, Nico Ueberschaar, Georg Pohnert, Thomas Wichard
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Abstract

DNA (deoxyribonucleic acid) methylation is a key epigenetic mechanism that regulates gene expression and developmental transitions in eukaryotes. Interestingly, algal growth- and morphogenesis-promoting bacteria can reduce global DNA methylation levels in the green seaweed Ulva (Chlorophyta), highlighting DNA methylation as a dynamic and environmentally responsive epigenetic mechanism in marine macroalgae. We hypothesized that DNA methylation serves as a rapid and essential epigenetic regulatory mechanism during gametogenesis in the model organism Ulva compressa (cultivar U. mutabilis slender). We further propose that this process is controlled by sporulation inhibitors - extracellular compounds long known to regulate reproduction in Ulva, yet whose molecular mode of action has remained elusive. Using ultra-high-performance liquid chromatography-mass spectrometry (HPLC–HRMS), we quantified global levels of 5-methylcytosine (5mC) and N6-methyladenine (6mA) across defined life-cycle stages of Ulva, including gametogenesis induction and gamete release. We observed a rapid and pronounced increase in 5mC immediately following removal of sporulation inhibitors, consistent with active epigenetic reprogramming. In contrast, 6mA was detected only in mature thallus (vegetative tissue of macroalgae) and gametes, and not throughout gametogenesis, indicating a distinct yet minor role for this DNA modification in Ulva development. Re-addition of sporulation inhibitors prevented both gametogenesis and the characteristic methylation dynamics, indicating that these not-yet-characterized inhibitors act as epigenetic modulators. Together, our findings identify DNA methylation as a key regulatory layer linking bacterial cues, sporulation control, and reproductive development in Ulva, with direct implications for the epigenetic management of growth and reproduction in marine algal biotechnology.

Graphical Abstract

表观遗传调控将细菌信号传导与绿藻的生长和生殖发育联系起来。
DNA(脱氧核糖核酸)甲基化是调控真核生物基因表达和发育转变的关键表观遗传机制。有趣的是,促进藻类生长和形态发生的细菌可以降低绿海藻Ulva(绿藻)的整体DNA甲基化水平,突出了DNA甲基化是海洋大型藻类动态和环境响应的表观遗传机制。我们假设DNA甲基化在模式生物Ulva compressa(品种U. mutabilis slender)配子体发生过程中是一种快速而必要的表观遗传调控机制。我们进一步提出,这一过程是由孢子抑制物控制的,这是一种细胞外化合物,众所周知,它可以调节Ulva的繁殖,但其分子作用方式仍然难以捉摸。利用超高效液相色谱-质谱(HPLC-HRMS),我们定量了Ulva在不同生命周期阶段(包括配子发生诱导和配子释放)中5-甲基胞嘧啶(5mC)和n6 -甲基腺嘌呤(6mA)的全球水平。我们观察到,在去除孢子抑制因子后,5mC立即迅速而显著地增加,这与活跃的表观遗传重编程一致。相比之下,6mA仅在成熟的菌体(大型藻类的营养组织)和配子中检测到,而不是在整个配子发生过程中检测到,这表明这种DNA修饰在Ulva发育中起着明显但次要的作用。再次添加孢子抑制因子阻止配子体发生和特征甲基化动力学,表明这些尚未表征的抑制剂起表观遗传调节剂的作用。总之,我们的研究结果确定了DNA甲基化是连接细菌线索、孢子控制和Ulva生殖发育的关键调控层,对海洋藻类生物技术生长和繁殖的表观遗传管理具有直接意义。图形抽象
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来源期刊
Marine Biotechnology
Marine Biotechnology 工程技术-海洋与淡水生物学
CiteScore
4.80
自引率
3.30%
发文量
95
审稿时长
2 months
期刊介绍: Marine Biotechnology welcomes high-quality research papers presenting novel data on the biotechnology of aquatic organisms. The journal publishes high quality papers in the areas of molecular biology, genomics, proteomics, cell biology, and biochemistry, and particularly encourages submissions of papers related to genome biology such as linkage mapping, large-scale gene discoveries, QTL analysis, physical mapping, and comparative and functional genome analysis. Papers on technological development and marine natural products should demonstrate innovation and novel applications.
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