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Cytologic and Genetic Characteristics of Endobiotic Bacteria and Kleptoplasts of Virgulinella fragilis (Foraminifera)
Authors:Masashi Tsuchiya  Takashi Toyofuku  Katsuyuki Uematsu  Volker Brüchert  John Collen  Hiroyuki Yamamoto  Hiroshi Kitazato
Affiliation:1. Japan Agency for Marine‐Earth Science and Technology, Yokosuka, Kanagawa, Japan;2. Marine Works Japan, Ltd, Yokosuka, Kanagawa, Japan;3. Department of Geology and Geochemistry, Stockholm University, Stockholm, Sweden;4. School of Geography, Environment and Earth Sciences, Victoria University of Wellington, Wellington, New Zealand
Abstract:The benthic foraminifer Virgulinella fragilis Grindell and Collen 1976 has multiple putative symbioses with both bacterial and kleptoplast endobionts, possibly aiding its survival in environments from dysoxia (5–45 μmol‐O2/L) to microxia (0–5 μmol‐O2/L) and in the dark. To clarify the origin and function of V. fragilis endobionts, we used genetic analyses and transmission electron microscope observations. Virgulinella fragilis retained δ‐proteobacteria concentrated at its cell periphery just beneath the cell membranes. Unlike another foraminifer Stainforthia spp., which retains many bacterial species, V. fragilis has a less variable bacterial community. This suggests that V. fragilis maintains a specific intracellular bacterial flora. Unlike the endobiotic bacteria, V. fragilis klepto‐plasts originated from various diatom species and are found in the interior cytoplasm. We found evidence of both retention and digestion of kleptoplasts, and of fragmentation of the kleptoplastid outer membrane that likely facilitates transport of kleptoplastid products to the host. Accumulations of mitochondria were observed encircling endobiotic bacteria. It is likely that the bacteria use host organic material for carbon oxidation. The mitochondria may use oxygen available around the δ‐proteobacteria and synthesize adenosine triphosphate, perhaps for sulfide oxidation.
Keywords:Molecular phylogeny  multiple endosymbiosis  transmission electron microscopy
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