Decoding the gene expression response of Cerastoderma edule to chronic trematode infection: A comparison among host tissues

12 pages, 6 figures

Parasites can induce gene expression changes in their hosts, either benefiting the parasite or the host. In particular, trematodes are not only one of the most ubiquitous groups of aquatic parasites, they also have huge impacts on individual hosts with significant ecological and economic repercussions. The trematode Bucephalus minimus infects Cerastoderma edule (the edible cockle), a socioeconomically and ecologically important bivalve, as its first intermediate host. This parasite is one of the most harmful parasites infecting cockles, affecting their ability to reproduce, grow, and survive, thereby indirectly impacting ecosystem functioning. Despite the well-documented ecological effects of B. minimus, its impacts at a molecular level remain poorly understood. This study aimed to investigate the molecular mechanisms underlying B. minimus infection in cockles by analysing tissue-specific and systemic responses to long-term parasitic infection. It compared gene expression profiles in two critical tissues of naturally infected and non-infected cockles: the digestive gland, the primary target of infection, and the haemolymph, the backbone of the bivalve immune system. Results revealed extensive tissue-specific changes in gene expression. In the haemolymph, infected cockles showed significant downregulation of pathways related to cell division, cytoskeletal organization, and DNA repair, suggesting potentially parasite-induced reduction of immune responses and host cellular functions. Contrary to expectations, immune pathways did not show significantly increased expression, likely reflecting the chronic nature of infection and energy reallocation by the host. In the digestive gland, genes associated with gametogenesis, metabolism and immune function were downregulated, with no significant upregulation observed, except in some genes related to scavenger receptor activity and inflammation, suggesting localized immune responses. Shared responses among tissues included alterations in zinc ion transport and neurotransmitter biosynthesis, suggesting management of infection-induced stress. These findings highlight how B. minimus may manipulate host biology to suppress immunity and disrupt critical cellular processes, providing valuable insights into chronic trematode infections and host-parasite dynamics

This work was funded by “Pacto da Bioeconomia Azul” with reference C644915664-00000026 under the call 02/C05-i01/2022 of the Resilience and Recuperation Plan (PRR) and led by Inovmar Lda. Simão Correia benefited from PhD grant (https://doi.org/10.54499/2020.04688.BD) funded by National Funds through the Portuguese Science Foundation (Fundação para a Ciência e Tecnologia, FCT). Luísa Magalhães is funded by national funds (OE), through FCT (grant https://doi.org/10.54499/2021.01858.CEECIND/CP1659/CT0010). Thanks are also due to FCT for the financial support to CESAM under the project UID/50006 + LA/P/0094/2020 (https://doi.org/10.54499/LA/P/0094/2020). Sergio Fernández-Boo is funded through the CEEC Institutional program with ref. CEECINST/00027/2021/CP2789/CT0002. This research was also supported by the strategic funding UIDB/04423/2020 and UIDP/04423/2020, and LA/P/0101/2020 (https://doi.org/10.54499/LA/P/0101/2020) through national funds provided by FCT

Peer reviewed