Effects of Long-Term Starvation on a Host Bivalve (Codakia orbicularis, Lucinidae) and Its Symbiont Population

Abstract

The bivalve Codakia orbicularis, hosting sulfur-oxidizing gill endosymbionts, was starved (in artificial seawater filtered through a 0.22-m-pore-size membrane) for a long-term experiment (4 months). The effects of starvation were observed using transmission electron microscopy, fluorescence in situ hybridization and catalyzed reporter deposition (CARD-FISH), and flow cytometry to monitor the anatomical and physiological modifications in the gill organization of the host and in the symbiotic population housed in bacteriocytes. The abundance of the symbiotic population decreased through starvation, with a loss of one-third of the bacterial population each month, as shown by CARD-FISH. At the same time, flow cytometry revealed significant changes in the physiology of symbiotic cells, with a decrease in cell size and modifications to the nucleic acid content, while most of the symbionts maintained a high respiratory activity (measured using the 5-cyano-2,3-ditolyl tetrazolium chloride method). Progressively, the number of symbiont subpopulations was reduced, and the subsequent multigenomic state, characteristic of this symbiont in freshly collected clams, turned into one and five equivalent genome copies for the two remaining subpopulations after 3 months. Concomitant structural modifications appeared in the gill organization. Lysosymes became visible in the bacteriocytes, while large symbionts disappeared, and bacteriocytes were gradually replaced by granule cells throughout the entire lateral zone. Those data suggested that host survival under these starvation conditions was linked to symbiont digestion as the main nutritional source.

Thioautotrophic bacterial endosymbionts are degraded by enzymatic digestion during starvation: Case study of two lucinids Codakia orbicularis and C. orbiculata

“…In the laboratory, it is possible to maintain adult bivalves under starvation conditions for up to 6 months and minimize the number of symbionts inside the gills. During our experiments, the appearance of the lucinid gills changed from thick and lightly beige in freshly collected bivalves (containing large symbiont populations with a large quantity of elemental sulfur) to thin and dark brown in starved bivalve individuals (containing fewer symbionts without elemental sulfur) (personal observations) (Caro et al, ; Lechaire et al, ; Pflugfelder et al, ). We suggest that the host can use this large amount of bacteria as a nutrient source through lysosomal degradation (Johnson and Fernandez, ).…”

“…In deep sea bivalves, it was suggested that lysosomal symbiont digestion is a way of controlling symbiont populations (Fiala‐Medioni et al, ). During starvation, lysosomes in the gills of both Codakia species become larger and more abundant (Caro et al, ). Moreover, Elisabeth et al () described a massive decrease in the area occupied by bacteriocytes in C. orbiculata during starvation.…”

Lipid characteristics of a seep clam, Mesolinga soliditesta : Comparison with those of two coastal clams, Meretrix lamarckii and Ruditapes philippinarum

“…Examples of the latter include Lucinoma borealis , Myrtea spinifera, Lucinoma aequizonata, and Lucina floridana (Anderson, 1995), Thyasira sp. (Southward et al, 2001), Lucinoma aequizonata and Parvilucina tenuisculpta , and Codakia orbicularis (Caro et al, 2009). The chemical components, such as glycerolipids, have yet to be elucidated for these clams, except in the case of R. philippinarum from European coastal waters (Kraffe et al, 2004;Delaporte et al, 2005;Fernández-Reiriz et al, 2006).…”

Comparative modifications in bacterial gill-endosymbiotic populations of the two bivalvesCodakia orbiculataandLucina pensylvanicaduring bacterial loss and reacquisition

“…Recent morphological and molecular analyses (Elisabeth et al ., ; Gros et al ., ) support the conclusion that it is possible to induce complete or nearly complete loss of symbionts in adult lucinids by depriving their symbionts of their energy source (mainly in sulphide‐free environment). Decreases in endosymbiont abundance within gill cells have been shown according to structural investigations of the gill tissue in other chemosynthetic bivalves such as thyasirids (Dufour & Felbeck, ), vesicomyids (Goffredi et al ., ), bathymodiolin (Kádár et al ., ) and two lucinids (Caro et al ., ; Gros et al ., ). However, no data are available concerning the modifications undergone by the endosymbionts themselves (at the metabolic or genomic level) during increase or decrease of their populations within the gill tissue either in the frame of starvation laboratory experiments or in their natural habitats.…”