Table 7_Evolutionary conservation of dopamine-mediated cellular plasticity in Arctic sponges (Porifera).docx

Dopamine is an evolutionarily ancient signaling molecule implicated in stress responses across the tree of life. The role of dopamine is well-documented in the nervous system of animals, yet in the early-branching animal lineage of sponges its utility is poorly understood. Arctic marine sponges inhabiting the tidal zone of the White Sea, with fluctuating seasonal ice cover and solute concentrations, exhibit remarkable physiological plasticity, making them ideal models for studying conserved stress-response mechanisms. We investigated the dopamine signaling in two sponge species, Sycon ciliatum (class Calcarea) and Halisarca dujardini (class Demospongiae), using metagenomics, transcriptomics, high performance liquid chromatography, mass spectrometry, molecular docking, and immunofluorescence. S. ciliatum expresses an aromatic amino acid decarboxylase-like enzyme and efficiently converts L-DOPA to dopamine, whereas H. dujardini lacks this canonical biosynthetic enzyme, but accumulates dopamine, likely via its symbionts. During morphogenetic transitions in H. dujardini, genes involved in dopamine turnover, including tyrosinase, dopamine β-hydroxylase, and G protein–coupled receptors (GPCRs), showed dynamic expression. Molecular docking revealed that GPCR affinity for dopamine is modulated by cellular redox status. Notably, we report the first evidence of post-translational dopaminylation of cytoskeleton proteins in a non-bilaterian animal. Fluctuations in cellular dopamine levels and actin dopaminylation correlated with structural remodeling of the aquiferous system throughout the sponge life cycle. These findings demonstrate that dopamine regulates cellular plasticity through both transcriptional and post-translational mechanisms. The discovery of dopaminylation in sponges expands the evolutionary scope of catecholamine signaling and underscores the ancient role of dopamine in the regulatory interactions of animal cells.

多巴胺（Dopamine）是一种进化上古老的信号分子，参与整个生命树的应激反应。多巴胺在动物神经系统中的作用已有充分研究，但在早期分化的动物谱系——海绵动物中，其功能仍鲜为人知。栖息于白海潮间带、面临季节性海冰覆盖与溶质浓度波动的北极海洋海绵，表现出显著的生理可塑性，使其成为研究保守应激反应机制的理想模型。本研究采用宏基因组学、转录组学、高效液相色谱、质谱、分子对接及免疫荧光技术，对两种海绵——毛壶（Sycon ciliatum，钙质海绵纲）和杜氏软海绵（Halisarca dujardini，寻常海绵纲）的多巴胺信号通路进行了探究。毛壶表达一种类芳香族氨基酸脱羧酶，可高效将L-多巴（L-DOPA）转化为多巴胺；而杜氏软海绵缺乏该经典生物合成酶，却能通过共生体积累多巴胺。在杜氏软海绵的形态发生转变过程中，参与多巴胺代谢周转的基因——包括酪氨酸酶、多巴胺β-羟化酶及G蛋白偶联受体（G protein–coupled receptors, GPCRs）——呈现动态表达模式。分子对接结果显示，GPCR对多巴胺的亲和力受细胞氧化还原状态调控。值得注意的是，本研究首次在非两侧对称动物中发现了细胞骨架蛋白的翻译后多巴胺化修饰证据。在海绵的整个生命周期中，细胞多巴胺水平与肌动蛋白多巴胺化修饰的波动，均与水沟系统的结构重塑密切相关。本研究结果表明，多巴胺可通过转录及翻译后修饰两种机制调控细胞可塑性。海绵中多巴胺化修饰的发现，拓展了儿茶酚胺信号通路的进化范围，并凸显了多巴胺在动物细胞调控互作中的古老功能。