Persistence, morphology, and nutritional state of a gastropod hosted bacterial symbiosis in different levels of hydrothermal vent flux
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The limpet, Lepetodrilus fucensis McLean, is found in prominent stacks around hydrothermal vents on the Juan de Fuca Ridge. L. fucensis hosts a filamentous episymbiont on its gill lamellae that may be ingested directly by the gill epithelium. To assess the persistence of this symbiosis I used microscopy to examine the gills of L. fucensis from sites representing its geographic range and different habitats. The symbiosis is present on all the specimens examined in this study, including both sexes and a range of juvenile and adult sizes. Next, I aimed to determine if patterns in bacterial abundance, host condition, and gill morphology support the hypotheses that the bacteria are chemoautotrophic and provide limpets with a food resource. To do so, I compared specimens from high and low flux locations at multiple vents. My results support the above hypotheses: (1) gill bacteria are significantly less abundant in low flux where the concentrations of reduced chemicals (for chemoautotrophy) are negligible, (2) low flux specimens have remarkably poor tissue condition, and (3) the lamellae of high flux limpets have greater surface area: the blood space and bacteria-hosting epithelium are deeper and have more folds than low flux lamellae, modifications that support higher symbiont abundances. I next asked if the morphology of the lamellae could change. To test this, I moved high flux limpets away from a vent and after 1 year the lamellar depth and shape of the transplanted specimens resembled low flux gills. Last, I was interested in whether bacterial digestion by the gill epithelium is a significant feeding mechanism. As bacteria-like cells are rarely apparent in lysosomes of the gill epithelium, I predicted that lysosome number would be unrelated to bacterial abundance. My data support this prediction, suggesting that digestion of bacteria by the gill epithelium probably contributes only minimally to the limpet’s nutrition. Overall, the persistence and morphology of the L. fucensis gill symbiosis relates to the intensity of vent flux and indicates that specimens from a variety of habitats may be necessary to characterize the morphological variability of gill-hosted symbioses in other molluscs.
KeywordsShell Length Bacterial Abundance Gill Epithelium Gill Lamella Flux Location
V. Tunnicliffe provided samples, financial support, and comments on the manuscript. R. Campbell performed the lipid analyses. Technical support from the ROPOS team and the crew of the RV Thompson is especially appreciated. Research cruise scientists, in particular S. K. Juniper, made this work possible. Special effort by B. Embley, J. Delaney, and D. Kelly was made to recover samples and the experiment during rough weather. T. Bird, R. Campbell, L. Page, J. Rose, and C.L. Singla provided technical support. NSERC Canada, the NOAA Vents Program, and graduate student scholarships to A. Bates from NSERC Canada and the families of Gordon Fields and Maureen de Burgh provided funding for this study.
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