Research Article: High rates of apoptosis visualized in the symbiont-bearing gills of deep-sea Bathymodiolus mussels

Date Published: February 4, 2019

Publisher: Public Library of Science

Author(s): Bérénice Piquet, Bruce Shillito, François H. Lallier, Sébastien Duperron, Ann C. Andersen, Clara F. Rodrigues.


Symbiosis between Bathymodiolus and Gammaproteobacteria allows these deep-sea mussels to live in toxic environments such as hydrothermal vents and cold seeps. The quantity of endosymbionts within the gill-bacteriocytes appears to vary according to the hosts environment; however, the mechanisms of endosymbiont population size regulation remain obscure. We investigated the possibility of a control of endosymbiont density by apoptosis, a programmed cell death, in three mussel species. Fluorometric TUNEL and active Caspase-3-targeting antibodies were used to visualize and quantify apoptotic cells in mussel gills. To control for potential artefacts due to depressurization upon specimen recovery from the deep-sea, the apoptotic rates between mussels recovered unpressurised, versus mussels recovered in a pressure-maintaining device, were compared in two species from hydrothermal vents on the Mid-Atlantic Ridge: Bathymodiolus azoricus and B. puteoserpentis. Results show that pressurized recovery had no significant effect on the apoptotic rate in the gill filaments. Apoptotic levels were highest in the ciliated zone and in the circulating hemocytes, compared to the bacteriocyte zone. Apoptotic gill-cells in B. aff. boomerang from cold seeps off the Gulf of Guinea show similar distribution patterns. Deep-sea symbiotic mussels have much higher rates of apoptosis in their gills than the coastal mussel Mytilus edulis, which lacks chemolithoautotrophic symbionts. We discuss how apoptosis might be one of the mechanisms that contribute to the adaptation of deep-sea mussels to toxic environments and/or to symbiosis.

Partial Text

Symbiosis is of major significance to life on Earth. Because symbiosis between two (or several) partners may straddle the line between cooperation and conflict, each partner theoretically initiates and carries on a continued dialogue with the other partners, to keep some degree of control over the interaction. Many symbioses involve partners from different domains of life, such as a eukaryotic host and a bacterial symbiont. The question then arises: how can reciprocal control occur between such distantly related organisms, and are some of the mechanisms involved universal? One of the mechanisms by which an animal host can control symbiont populations is apoptosis. Apoptosis is a programmed cell death involving three main steps: (1) nuclear condensation and fragmentation, (2) cell-wall budding into apoptotic bodies, and (3) their release and possible phagocytosis by neighboring cells [1,2]. Apoptosis plays multiple roles in normal cell turnover, during development, and in the immune system [3].

All analyses were performed on transversal sections of the gill lamellae (S2 Fig). From the FISH results, it is noteworthy that bacteriocytes close to the frontal ciliated zone contained large quantities of endosymbionts, and that both the height of the bacteriocytes and their symbiont density decreased towards the abfrontal zone in B. puteoserpentis, and B. azoricus (Fig 1). This frontal/abfrontal decrease in symbiont density also appears with the DAPI staining, as this labels not only the host nuclei, but also the DNA of the bacterial symbionts.




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