Evolutionary Conservation of Dopamine-Mediated Cellular Plasticity in Arctic Sponges (Porifera)

Oksana I Kravchuk¹Alexander D Finoshin¹Yulia O Nikishina¹Victoria I Melnikova¹Ilya V Kublanov²Dmitry A Sutormin³Anastasiia N Rusanova¹Maxim T Ri³Artem B Isaev³Kirill V Mikhailov⁴Rustam Ziganshin⁵Kim I Adameyko¹Anastasia A. Anashkina⁶Vasilina M Ignatyuk¹Nikolai G Gornostaev¹Elena E. Voronezhskaya¹Agniya M Sokolova¹Victor Mikhailov¹Yulia V Lyupina^7*

• ¹FGBUN Institut biologii razvitia imeni N K Kol'cova Rossijskoj akademii nauk, Moscow, Russia
• ²Institut mikrobiologii imeni S N Vinogradskogo Rossijskoj akademii nauk, Moscow, Russia
• ³Skolkovskij institut nauki i tehnologij, Moscow, Russia
• ⁴Moskovskij gosudarstvennyj universitet imeni M V Lomonosova Naucno-issledovatel'skij institut fiziko-himiceskoj biologii imeni A N Belozerskogo, Moscow, Russia
• ⁵FBGUN Institut bioorganiceskoj himii im akademikov M M Semakina i U A Ovcinnikova Rossijskoj akademii nauk, Moscow, Russia
• ⁶FGBUN Institut molekularnoj biologii imeni V A Engel'gardta Rossijskoj akademii nauk, Moscow, Russia
• ⁷Koltzov Institute of Developmental Biology, Russian Academy of Sciences, Moscow, Russia

Dopamine is an evolutionarily ancient signaling molecule involved in responses to environmental stress throughout the tree of life. In sponges, one of the earliest lineages of metazoans, its role in cellular plasticity remains poorly understood. Arctic sponges are highly sensitive to environmental changes and represent a unique model for identifying conserved stress response mechanisms and structural adaptations. This study investigated the dopamine signaling in arctic sponges. While Sycon ciliatum (class Calcarea) expresses aromatic amino acid decarboxylase and efficiently converts L-DOPA to dopamine, Halisarca dujardini (class Demospongiae) lacks this enzyme but also accumulates dopamine in the cells presumably from a symbiont-mediated biosynthetic pathway. During morphogenetic transitions in H. dujardini, genes involved in dopamine turnover, including tyrosinase, dopamine β-hydroxylase, and G protein-coupled receptors, showed dynamic expression patterns. The affinity of G protein-coupled receptors for dopamine is modulated by cellular redox status. Moreover, we detected for the first time post-translational dopaminylation of cytoskeleton proteins in sponge cells. Fluctuations in cell dopamine levels and actin dopaminylation during the life cycle of H. dujardini correlated with structural remodeling of the sponge aquifer system. The discovery of dopaminylation in a non-bilateral model expands the known scope of catecholamine signaling, suggesting an ancient role for dopamine in modulating cellular plasticity through both transcriptional and post-translational regulatory mechanisms.