title: Cytologic and Genetic Characteristics of Endobiotic Bacteria and Kleptoplasts of Virgulinella fragilis (Foraminifera).
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.
authors.affiliation: Japan Agency for Marine-Earth Science and Technology, 2-15 Natsushima-cho, Yokosuka, Kanagawa, 237-0061, Japan.
authors.forename: Masashi
authors.initials: M
authors.lastname: Tsuchiya
authors.affiliation: Japan Agency for Marine-Earth Science and Technology, 2-15 Natsushima-cho, Yokosuka, Kanagawa, 237-0061, Japan.
authors.forename: Takashi
authors.initials: T
authors.lastname: Toyofuku
authors.affiliation: Marine Works Japan, Ltd, 3-54-1 Oppamahigashi-cho, Yokosuka, Kanagawa, 237-0036, Japan.
authors.forename: Katsuyuki
authors.initials: K
authors.lastname: Uematsu
authors.affiliation: Department of Geology and Geochemistry, Stockholm University, Svante Arrhenius väg 8C, 10691, Stockholm, Sweden.
authors.forename: Volker
authors.initials: V
authors.lastname: Brüchert
authors.affiliation: School of Geography, Environment and Earth Sciences, Victoria University of Wellington, Wellington, New Zealand.
authors.forename: John
authors.initials: J
authors.lastname: Collen
authors.affiliation: Japan Agency for Marine-Earth Science and Technology, 2-15 Natsushima-cho, Yokosuka, Kanagawa, 237-0061, Japan.
authors.forename: Hiroyuki
authors.initials: H
authors.lastname: Yamamoto
authors.affiliation: Japan Agency for Marine-Earth Science and Technology, 2-15 Natsushima-cho, Yokosuka, Kanagawa, 237-0061, Japan.
authors.forename: Hiroshi
authors.initials: H
authors.lastname: Kitazato
mesh_terms: D000255:Adenosine Triphosphate / Q000096:biosynthesis; D000818:Animals; D001419:Bacteria / Q000166:cytology* / Q000235:genetics* / Q000302:isolation & purification / Q000378:metabolism; D002244:Carbon / Q000378:metabolism; D002462:Cell Membrane / Q000382:microbiology; D003593:Cytoplasm / Q000382:microbiology; D020564:Deltaproteobacteria / Q000166:cytology* / Q000235:genetics* / Q000302:isolation & purification; D056908:Foraminifera / Q000382:microbiology*; D019015:Geologic Sediments / Q000382:microbiology; D046529:Microscopy, Electron, Transmission; D008969:Molecular Sequence Data; D010802:Phylogeny; D013559:Symbiosis
chemical_list: D002244:Carbon; D000255:Adenosine Triphosphate
keywords: Molecular phylogeny; multiple endosymbiosis; transmission electron microscopy