Distribution of bacteria and associated minerals in the gill chamber of the vent shrimp Rimicaris exoculata and related biogeochemical processes

Abstract

The shrimp Rimicaris exoculata dominates the megafauna of some Mid-Atlantic Ridge hydrothermal vent fields. This species harbours a rich bacterial epibiosis inside its gill chamber. At the 'Rainbow' vent site (36°14.0' N), the epibionts are associated with iron oxide deposits. Investigation of both bacteria and minerals by scanning electron microscopy (SEM) and X-ray microanalysis (EDX) revealed 3 distinct compartments in the gill chamber: (1) the lower pre-branchial chamber, housing bacteria but devoid of minerals; (2) the 'true' branchial chamber, containing the gills and devoid of both bacteria and minerals; and (3) the upper pre-branchial chamber, housing the main ectosymbiotic bacterial community and associated mineral deposits. Our chemical and temperature data indicated that abiotic iron oxidation appears to be kinetically inhibited in the environment of the shrimps, which would explain the lack of iron oxide deposits in the first 2 compartments. We propose that iron oxidation is microbially promoted in the third area. The discrepancy between the spatial distribution of bacteria and minerals suggests that different bacterial metabolisms are involved in the first and third compartments. A possible explanation lies in the modification of physico-chemical conditions downstream of the gills that would reduce the oxygen content and favours the development of bacterial iron-oxidizers in this Fe II -rich environment. A potential role of such iron-oxidizing symbionts in the shrimp diet is suggested. This would be unusual for hydrothermal ecosystems, in which most previously described symbioses rely on sulphide or methane as an energy source.

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

“…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).…”

“…Furthermore, whether CH 4 -or H 2 -metabolic genes are actively expressed or not has not been determined. Biotic iron oxidation by R. exoculata epibionts has been proposed (Zbinden et al, 2004(Zbinden et al, , 2008Corbari et al, 2008a) on the basis of the close association of these bacteria with heavy iron-oxyhydroxide deposits. Our results support this hypothesis, but evidence is lacking as to the ability of the bacterial phylotypes identified so far to oxidise iron.…”

“…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. Recent studies suggest that R. exoculata gill chamber epibionts constitute a diversified community with various morphotypes, phylotypes and metabolisms (Zbinden et al, 2004(Zbinden et al, , 2008Petersen et al, 2009;Hü gler et al, 2011;Guri et al, 2012), but no study has directly demonstrated which substrate(s) the bacteria oxidise to fuel their 'chemosynthetic' metabolism(s). This shrimp also harbours a digestive bacterial community (Zbinden and Cambon-Bonavita, 2003;Durand et al, 2010) whose role remains hypothetical (detoxification, nutrition and/or pathogen control).…”

“…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.…”

“…The shrimp R. exoculata (Williams and Rona, 1986) dominates the megafauna of several deep-sea hydrothermal vent sites of the Mid-Atlantic Ridge, forms dense aggregates around active chimneys (Segonzac, 1992) and harbours a luxuriant bacterial community in its enlarged gill chamber (Van Dover et al, 1988;Casanova et al, 1993;Segonzac et al, 1993;Polz and Cavanaugh, 1995;Zbinden et al, 2004) (Figure 1). The integument surfaces are periodically re-colonised during the moult cycle Figure 1 Illustration of the shrimp Rimicaris exoculata gill chamber with the associated bacterial community.…”