Regionalized cell proliferation in the symbiont-bearing gill of the hydrothermal vent mussel Bathymodiolus azoricus
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Regionalized cell proliferation in the symbiont-bearing gill of the hydrothermal vent mussel Bathymodiolus azoricus Bérénice Piquet 1,2,3 & François H. Lallier 1 & Coralie André 1 & Bruce Shillito 2 & Ann C. Andersen 1 & Sébastien Duperron 3,4 Received: 4 June 2020 / Accepted: 14 September 2020 # Springer Nature B.V. 2020
Abstract Deep-sea mussels Bathymodiolus spp. harbor high densities of chemosynthetic bacterial symbionts located within their gill epithelial cells. Compared to non-symbiotic coastal mussel relatives of similar size, Bathymodiolus gills are considerably larger, a feature often considered an adaptation to symbiosis because it is related to the presence of intracellular bacteria in epithelial cells located in the lateral zone. In order to document the mechanisms underlying these sizes differences, this study compares gill cell proliferation patterns in Bathymodiolus azoricus and Mytilus edulis using microscopy-based approaches. We used incubation experiments with a synthetic nucleotide (5-ethynyl 2′-deoxyuridine, EdU), detectable throughout novel cell divisions, and phosphohistone H3 immunolabeling, a marker of mitosis. The results revealed proliferation areas in the ciliated zone and in the bacteria-loaded bacteriocytes located close to the frontal zone of gill filaments, swept by the incurrent sea-waterflow, and also in the dorsal region of gills in B. azoricus. Cell proliferation seems far less intensive in M. edulis. This study overall suggests high cell turnover and fast tissue dynamics in symbiont-bearing mussels. Keywords Bathymodiolus . EdU . Phosphohistone H3 . Hydrothermal vents . Cell division . Chemotrophic symbiosis
1 Introduction Tissues and organs that have evolved to host intracellular microorganisms are common in various animal taxa, including the endoderm of cnidarians, insect bacteriomes, and the trophosome of deep-sea tubeworms (Russel and Ruelas Castillo 2020). In a * Ann C. Andersen [email protected] * Sébastien Duperron [email protected]; https://orcid.org/0000-0002-6422-6821 1
Lab. Adaptation et Diversité en Milieu Marin, AD2M, Adaptation et Biologie des Invertébrés marins en Conditions Extrêmes (UMR 7144), ABICE, DYDIV, Station Biologique de Roscoff, Sorbonne Université CNRS, place Georges Teissier, Roscoff, France
2
Laboratoire de Biologie des Organismes et Ecosystèmes Aquatiques (BOREA), MNHN, CNRS-2030, IRD-207, Sorbonne Université, UCN, UA, Team: Adaptation aux Milieux Extrêmes (AMEX), 7 Quai Saint-Bernard, Paris, France
3
Muséum National d’Histoire Naturelle, CNRS, Lab. Mécanismes de Communication et Adaptation des Micro-organismes (UMR 7245), Team: Cyanobactéries, Cyanotoxines et Environnement, CCE, PTME 12 rue Buffon, Paris, France
4
Institut Universitaire de France, Paris, France
multicellular organism, the number of microbes within each host cell, as well as the size of symbiont-hosting tissues must be regulated in a way that does not compromise proper host development and maintenance. However, to understand the adaptations that underpin an o
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