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

Type Article
Date 2019-02
Language English
Author(s) Piquet Berenice1, 2, Shillito Bruce2, Lallier Francois H.1, Duperron Sebastien2, 3, 4, Andersen Ann C.1
Affiliation(s) 1 : Sorbonne Univ, CNRS,SBR, Team Adaptat & Biol Invertebres Marins Condit Ext, Lab Adaptat & Divers Milieu Marin,AD2M,ABICE,UMR, Roscoff, France.
2 : Sorbonne Univ, CNRS, Lab Biol Organismes & Ecosyst Aquat BOREA,UMR 720, Team Adaptat Milieux Extremes,AMEX,IRD,UCN,UA,MNH, 7 Quai St Bernard, Paris, France.
3 : CNRS, Team Cyanobacteries Cyanotoxines & Environm, Lab Mecanismes Commun & Adaptat Microorganismes, Museum Natl Hist Nat,CCE,UMR 7245, 12 Rue Buffon, Paris, France.
4 : Inst Univ France, Paris, France.
Source Plos One (1932-6203) (Public Library Science), 2019-02 , Vol. 14 , N. 2 , P. e0211499 (21p.)
DOI 10.1371/journal.pone.0211499
WOS© Times Cited 6

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 hydro thermal 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.

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Publisher's official version 21 2 MB Open access
S1 Table. Median percentage of apoptosis in all individuals from the four species in this study, with their shell measurements, collection site, and method of recovery. 3 322 KB Open access
S1 Fig. Measurements of mussel shells. 1 MB Open access
S2 Fig. Gills of Bathymodiolus spp. 3 MB Open access
S3 Fig. Percentage of apoptotic nuclei in the ciliated (A), hemolymph (B) and bacteriocyte (C) zones in individual specimens of B. azoricus and B. puteoserpentis from the three site 3 MB Open access
S4 Fig. TUNEL labelling on gill filaments of Bathymodiolus azoricus. 539 KB Open access
S5 Fig. Percentage of apoptotic nuclei in the ciliated (A) and hemolymph zones (B) of B. azoricus and B. puteoserpentis from the three sites. 2 MB Open access
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