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Cytoenzymatic investigation of intracellular digestion in the symbiont-bearing hydrothermal bivalve Bathymodiolus azoricus

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Abstract

Invertebrates harbouring endosymbiotic chemoautotrophic bacteria are widely distributed in a variety of reducing marine habitats, including deep-sea hydrothermal vents. Bathymodiolids are dominants of the biomass at geochemically distinct vent sites of the Mid Atlantic Ridge (MAR) and thus are good candidates to study biological processes in response to site-specific conditions. To satisfy their nutritional requirements, these organisms depend to varying extent on two types of chemoautotrophic symbionts and on filterfeeding. The quantitative relationships of the nutritional modes are poorly understood. Using enzyme cytochemistry, electron microscopy and X-ray microanalysis, the structural and functional aspects of the cellular equipment necessary for lysosomal digestion was studied. We provide evidence for the following: (1) the basis of intracellular digestion of symbionts in Bathymodiolus azoricus from two geochemically distinct vent sites was not mainly in the large lysosomal bodies as previously thought (based on the membranous content resembling bacteria); (2) senescent bacteria are autolysed, possibly by bacterial acid phosphatase, that is more likely a cell cycling of the symbionts rather than an active lysosomal digestion by the host; (3) the consistent absence of hydrolases may indicate the improper use of the name “lysosome” for large vesicles at the base of the gill bacteriocytes (4) nutrient transfer in B. azoricus, therefore, may more likely be accomplished through leaking of metabolites from the symbiont to the host, not excluding lysosomal resorption of dead bacteria as an auxiliary strategy for organic molecule transfer; (5) evidence is provided for microvillar transfer of substances from the seawater that may indicate filter-feeding, in non-symbiotic ciliated gill cells of mussels from Lucky Strike; (6) two types of lysosomal vesicles can be distinguished in digestive cells based on their enzymatic content and their elemental composition.

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Acknowledgments

The research was undertaken under the scope of the research project FISIOVENT (Physiological adaptations to extreme conditions at deep sea hydrothermal vents) funded by FCT (PDCTM/P/MAR/15281/1999). Postdoctoral fellowship was offered by the Portuguese Science Foundation (FCT) to Eniko Kadar (SFRH-BPD-19625/2004). The Pluriannual and Programatic funding schemes of FCT-MCTES and DRCT-Azores to the R&D Unit #531 are acknowledged. The authors acknowledge the ROV team, the Atalante Arquipelago crews for their contribution in sampling. Jon Jones from the Chemistry Department of the University of Bristol is acknowledged for his technical assistance during X-ray microanalysis. We are indebted to Horst Felbeck for his critical review, which certainly improved the quality of this paper.

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Authors and Affiliations

  1. Department of Oceanography and Fisheries, IMAR Centre of the University of Azores, Rua Cais de Santa Cruz, 9900, Horta, Portugal

    Enikö Kádár

  2. Chemistry Department, University of Bristol, Bristol, UK

    Sean A. Davis

  3. Laboratory of Cell Biology, Institute of Biomedical Sciences Abel Salazar, University of Porto, and CIIMAR, Porto, Portugal

    Alexandre Lobo-da-Cunha

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  1. Enikö Kádár
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  2. Sean A. Davis
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  3. Alexandre Lobo-da-Cunha
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Correspondence to Enikö Kádár.

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Communicated by M. Kühl.

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Kádár, E., Davis, S.A. & Lobo-da-Cunha, A. Cytoenzymatic investigation of intracellular digestion in the symbiont-bearing hydrothermal bivalve Bathymodiolus azoricus . Mar Biol 153, 995–1004 (2008). https://doi.org/10.1007/s00227-007-0872-0

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