Bacterial symbionts and mineral deposits in the branchial chamber of the hydrothermal vent shrimp Rimicaris exoculata: relationship to moult cycle

Abstract

The shrimp Rimicaris exoculata is considered a primary consumer that dominates the fauna of most Mid-Atlantic Ridge hydrothermal ecosystems. The shrimps harbour in their gill chamber an important ectosymbiotic community of chemoautotrophic bacteria associated with iron oxide deposits. The settlement and development of this ectosymbiosis was investigated using microscopy techniques (light microscopy, LM; and scanning, transmission and environmental scanning electron microscopy: SEM and ESEM, respectively) for shrimps from 2 different vent fields (Rainbow, 36°14.0' N and TAG, 26°08.0' N). The results revealed a bacterial re-colonisation after each exuviation and a development of the bacterial community in 5 steps in relation to the moult stages, which were used as a reference time scale. In 287 shrimps from both vent fields, pre-ecdysial stages prevailed in the population, suggesting a short anecdysis and high moulting rate, probably to renew the ectosymbiosis. Comparisons with moult cycles of littoral shrimps suggest that the interval between successive exuviations in R. exoculata may be as short as 10 d. The colours of R. exoculata result from accumulation of iron oxide, which forms a bacteria-associated mineral crust in the gill chambers. The close correspondence between moult stages, the development of the ectosymbiont community and shrimp colours indicate that colour could be used to rapidly determine shrimp moult stages.

Inorganic carbon fixation by chemosynthetic ectosymbionts and nutritional transfers to the hydrothermal vent host-shrimp Rimicaris exoculata

“…Finally, the view that bacterial products are assimilated across the shrimp integument rather than via the DT is strongly supported by: (1) the significant incorporation of both 14 C-acetate and 3 Hlysine after an incubation time as short as 1 h. This is insufficient for uptake by ingestion assimilation, which commonly takes several hours (ingestion assimilation of carbon from bicarbonate, for example, requires prior incorporation by the bacteria, followed by grazing of bacteria from the MP) (Chipps, 1998;Hoyt et al, 2000); (2) the high incorporation levels recorded in the gill chamber integument lining (OB, Gi), as opposed to (3) the much lower levels recorded in the DT (Figure 6). These results are in agreement with the view that the shrimps do not graze on their epibionts (Zbinden et al, 2004;Corbari et al, 2008b), but rather farm them (Segonzac et al, 1993;Polz and Cavanaugh, 1996), although they might also ingest some chimney bacteria along with sulphides (Van Dover et al, 1988;Segonzac, 1992). The low but nevertheless significant incorporation of 14 C from bicarbonate in the DT corroborates the data of Polz et al (1998), although they found higher rates than ours (upon incubating isolated gut segments).…”

“…Several authors propose that organic nutrients might be transferred from epibionts to R. exoculata Zbinden et al, 2004;Corbari et al, 2008b). Others, arguing that the cuticle is impermeable, reject this hypothesis (Segonzac et al, 1993;Gebruk et al, 2000).…”

“…Experiments were carried out only on red-coloured pre-ecdysial specimens (that is, having an established and still-growing bacterial community) (Corbari et al, 2008b). In the IPOCAMP, incubations with isotopic tracers were carried out in flasks filled till to the top with seawater (SW), whose volume (50 or 250 ml) was chosen according to the treatment duration and number of shrimps to ensure shrimp survival in good physiological condition at the end of the experiment (Shillito et al, 2001;Ravaux et al, 2003).…”

“…Yet this evidence of symbiont-host nutritional relationships is indirect, and how carbon is transferred from bacteria to shrimp remains an open question. The hypothesis of direct transfer of dissolved molecules across the shrimp integument, especially the gill chamber lining, has been proposed on the basis of morphological observations (features dedicated to bacteria farming, absence of scrape marks on the biofilm) (Zbinden et al, 2004;Corbari et al, 2008b), but the nature of the transferred molecules and the integument areas involved remain to be discovered.…”

“…C, cuticle; Epi, epidermis; FB, filamentous bacteria; IB, inner branchiostegite; MB, methanotrophic-like bacteria; Mi, mineral particles; RB, rod-shaped bacteria; S, blood sinuses. (Corbari et al, 2008b), each ecdysis causing shedding of the old cuticle with its bacterial mats. The shrimp R. exoculata, listed as a model organism of an extreme deep-sea environment (CAREX, 2010), is exceptional among crustaceans for its association with bacteria.…”