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

Abstract

Until now, the culture of sulphur-oxidizing bacterial symbionts associated with marine invertebrates remains impossible. Therefore, few studies focused on symbiont's physiology under stress conditions. In this study, we carried out a comparative experiment based on two different species of lucinid bivalves (Codakia orbiculata and Lucina pensylvanica) under comparable stress factors. The bivalves were starved for 6 months in sulphide-free filtered seawater. For C. orbiculata only, starved individuals were then put back to the field, in natural sediment. We used in situ hybridization, flow cytometry and X-ray fluorescence to characterize the symbiont population hosted in the gills of both species. In L. pensylvanica, no decrease in symbiont abundance was observed throughout the starvation experiment, whereas elemental sulphur slowly decreased to zero after 3 months of starvation. Conversely, in C. orbiculata, symbiont abundance within bacteriocytes decreased rapidly and sulphur from symbionts disappeared during the first weeks of the experiment. The modifications of the cellular characteristics (SSC--relative cell size and FL1--genomic content) of the symbiotic populations along starvation were not comparable between species. Return to the sediment of starved C. orbiculata individuals led to a rapid (2-4 weeks) recovery of symbiotic cellular characteristics, comparable with unstressed symbionts. These results suggest that endosymbiotic population regulation is host-species-dependent in lucinids.

A trade-off between mucocytes and bacteriocytes in Loripes orbiculatus gills (Bivalvia, Lucinidae): a mixotrophic adaptation to seasonality and reproductive status in a symbiotic species?

“…By extrapolating our results throughout the lifetime of a Loripes bivalve, we suggest that before being able to reproduce, this species relies on the symbionts hosted in bacteriocytes for its nutrition by 'milking' (direct carbon transfer) (Schweimanns and Felbeck 1985;Herry et al 1989;Yuen et al 2019) and 'farming' (host digestion of the symbionts), as has been described for other lucinids (Caro et al 2009;Elisabeth et al 2014;König et al 2015). Then, when sexual maturation occurs in larger individuals, we posit that this triggers an annual cycle of histological gill variation in relation to gametogenesis (summarized in ESM, Fig.…”

Extensive Thioautotrophic Gill Endosymbiont Diversity within a Single Ctena orbiculata (Bivalvia: Lucinidae) Population and Implications for Defining Host-Symbiont Specificity and Species Recognition

“…In contrast, Codakia orbicularis juveniles, presumably with naive bacteriocyte precursors, acquire symbionts from purified gill-symbiont sections of their own species, as well as other lucinid species hosting thioautotrophic symbionts with identical 16S rRNA gene sequences (24, 25). On the other hand, starvation-related symbiont loss has not been observed in Lucina roquesana (referred to as Lucina pensylvanica in references 21 and 73). The contrasting evidence for symbiont acquisition, loss, and reacquisition suggests that such mechanisms could be host species specific in lucinid bivalves (73).…”

“…On the other hand, starvation-related symbiont loss has not been observed in Lucina roquesana (referred to as Lucina pensylvanica in references 21 and 73). The contrasting evidence for symbiont acquisition, loss, and reacquisition suggests that such mechanisms could be host species specific in lucinid bivalves (73). Based on our results, it does not appear that a single symbiont species occupies a single host.…”

Nitrogen fixation in a chemoautotrophic lucinid symbiosis

“…Bacterial symbionts were purified from healthy C. orbicularis gills with a light beige colour using Percoll density gradient centrifugation as described previously 13,49 . Briefly, after dissection of the animals, gill tissue was homogenized in a Dounce homogenizer in cold sterile seawater (salinity 35 g l −1 ) and the resulting homogenate was centrifuged at 30g for 1 min (4°C) to remove crude tissue debris.…”