Hydrothermal vents as observatories for future ocean acidification (OA) scenarios: an in-situ study to unravel the involvement of ATP binding cassette (ABC) transporters in the adaptation of marine polychaetes Platynereis spp. to OA

Silvia Simonetti^1,2*Kevin Nzumbi Mutemi³Patrizia Romano⁴Till Luckenbach⁵Valerio Zupo²Maria Cristina Gambi⁶Ilaria Corsi¹

• ¹Department of Physical, Earth and the Environmental Sciences, University of Siena, Siena, Tuscany, Italy
• ²Department of Marine Biotechnology, Anton Dohrn Zoological Station, Naples, Campania, Italy
• ³European Molecular Biology Laboratory Heidelberg, Heidelberg, Baden-Württemberg, Germany
• ⁴National Institute of Marine Biology, Ecology and Biotechnology, Anton Dohrn Zoological Station Naples, Ischia, Naples, Italy
• ⁵Department Ecotoxicology, Helmholtz Centre for Environmental Research (UFZ), Leipzig, Germany, Leipzig, Lower Saxony, Germany
• ⁶National Institute of Oceanography and Applied Geophysics (Italy), Trieste, Friuli-Venezia Giulia, Italy

The marine annelid Platynereis dumerilii is a key model in genetics, evolution, neurobiology, ecology, and ecotoxicology. Along with its sibling species, P. cfr massiliensis, it thrives in both normal and naturally acidified environments, making these species ideal candidates for studying mechanisms of tolerance to acidified conditions that resemble future ocean acidification (OA) scenarios. ATP-binding cassette (ABC) transporter porteins help mitigating the adverse impacts of drugs, xenobiotics, and physical stressors. Recent studies in bacteria and tumor cells suggest their involvement to mediate tolerance towards acid-stress. Such a function may aid marine species in coping with OA and should be considered when predicting future OA scenarios for marine fauna. Here we addressed the question if ABC transporters of Platynereis spp. are involved in compensating adverse effects of low pH by studying ABC transporter transcript levels in marine animals exposed to various pH levels. We first screened the P. dumerilii genome (version EMBL_pdum_1.0; GenBank assembly: GCA_026936325.1) through homology searches and identified 81 ABC transporter genes across subfamilies A–G. Using a single-cell atlas of P. dumerilii gene expression data, we then determined that a subset of ABCB, ABCC, and ABCG genes are expressed in different organ/tissues including the midgut, nervous system, epidermis, and muscle. To assess how seawater pH affects ABC transporter expression, we conducted an in situ reciprocal transplant experiment involving individuals of P. dumerilii/P. cfr massiliensis. Adult specimens were collected inside and outside the CO2 vents off Castello Aragonese (Ischia Island, Italy). Individuals collected from normal pH areas (8.18 ± 0.005) were transplanted to acidified conditions (7.33 ± 0.312), and vice versa, while others were placed in their original areas. After 30 days, qPCR analyses revealed differential expression of three out of the seven selected genes from the subfamilies ABCB, ABCC, and ABCG (up-regulation of abcb_1 and down-regulation of abcg abcb_3). Based on the homology with human ABCB1 and ABCG2, which are crucial in tumor cell adaptation to acidified environments, it seems reasonable to hypothesize that abcb_1, abcb_3 and abcg play a similar role in Platynereis spp. helping in maintaining cellular homeostasis and surviving acid stress.