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 (36degrees 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.