Plasticity of symbiont acquisition throughout the life cycle of the shallow‐water tropical lucinid Codakia orbiculata (Mollusca: Bivalvia)

Abstract

In marine invertebrates that acquire their symbionts from the environment, these are generally only taken up during early developmental stages. In the symbiosis between lucinid clams and their intracellular sulfur-oxidizing bacteria, it has been shown that the juveniles acquire their symbionts from an environmental stock of free-living symbiont forms, but it is not known if adult clams are still competent to take up symbiotic bacteria from the environment. In this study, we investigated symbiont acquisition in adult specimens of the lucinid clam Codakia orbiculata, using transmission electron microscopy, fluorescence in situ hybridization, immunohistochemistry and PCR. We show here that adults that had no detectable symbionts after starvation in aquaria for 6 months, rapidly reacquired symbionts within days after being returned to their natural environments in the field. Control specimens that were starved and then exposed to seawater aquaria with sulfide did not reacquire symbionts. This indicates that the reacquisition of symbionts in the starved clams returned to the field was not caused by high division rates of a small pool of remaining symbionts that we were not able to detect with the methods used here. Immunohistochemistry with an antibody against actin, a protein involved in the phagocytosis of intracellular bacteria, showed that actin was expressed at the apical ends of the gill cells that took up symbionts, providing further evidence that the symbionts were acquired from the environment. Interestingly, actin expression was also observed in symbiont-containing cells of untreated lucinids freshly collected from the environment, indicating that symbiont acquisition from the environment occurs continuously in these clams throughout their lifetime.

Magnetosome-containing bacteria living as symbionts of bivalves

“…The few T. cf. gouldi symbionts with intact chains of magnetosomes may be recently acquired individuals, suggesting that symbiont uptake in thyasirids can occur more than once in their adult life, as in lucinids (Gros et al, 2012).…”

Growth rate and survival of terrestrial isopods is related to possibility to acquire symbionts

“…In general, the establishment of the symbiont-host relationship can be facilitated through three transmission mechanisms: vertically transmitted symbionts are passed from mother to progeny by infecting milk glands, eggs or embryos [14], horizontally transmitted symbionts may be acquired through feeding on infected corpses, faeces, exuviae or through physical contact between conspecifics [14,15], and environmentally transmitted symbionts are acquired through contact with or uptake of any matter [14,16,17]. The present understanding of the mechanisms that mediate symbiont transmission is based on empirical evidence available from only a few model systems.…”

“…The present understanding of the mechanisms that mediate symbiont transmission is based on empirical evidence available from only a few model systems. Vertical transmission appears as the predominant mechanisms for symbiont acquisition in insects [2,18], and environmental transmission is described for species living in aqueous environment [4,17]. The horizontal transmission of microbial species through faecal-oral contact in ruminant herbivores has received the most attention [19].…”

An overview of chemosynthetic symbioses in bivalves from the North Atlantic and Mediterranean Sea

“…Bacteria replicate their genomic DNA but do not divide actively within hosts cells (Caro et al, 2007), and are not released by adult bivalves (Brissac et al, 2009), suggesting a strong host control. Further, symbiont reacquisition after starvation is not by within-host division of bacterial cells, but rather by capture of new bacteria courtesy of a life-long continuous ability to acquire symbionts (Gros et al, 2012). In oxygen-depleted environments, symbionts of some species can avoid competition with their host for oxygen resources by growing on nitrate (Duplessis et al, 2004).…”