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PreprintUltrastructure and distribution of kleptoplasts in benthic foraminifera from shallow-water (photic) habitats( 2017-10) Jauffrais, Thierry ; LeKieffre, Charlotte ; Koho, Karoliina ; Tsuchiya, Masashi ; Schweizer, Magali ; Bernhard, Joan M. ; Meibom, Anders ; Geslin, EmmanuelleAssimilation, sequestration and maintenance of foreign chloroplasts inside an organism is termed “chloroplast sequestration” or “kleptoplasty”. This phenomenon is known in certain benthic foraminifera, in which such kleptoplasts can be found both intact and functional, but with different retention times depending on foraminiferal species. In the present study, seven species of benthic foraminifera (Haynesina germanica, Elphidium williamsoni, E. selseyense, E. oceanense, E. aff. E. crispum, Planoglabratella opercularis and Ammonia sp.) were collected from shallow-water benthic habitats and examined with transmission electron microscope (TEM) for cellular ultrastructure to ascertain attributes of kleptoplasts. Results indicate that all these foraminiferal taxa actively obtain kleptoplasts but organized them differently within their endoplasm. In some species, the kleptoplasts were evenly distributed throughout the endoplasm (e.g., H. germanica, E. oceanense, Ammonia sp.), whereas other species consistently had plastids distributed close to the external cell membrane (e.g., Elphidium williamsoni, E. selseyense, P. opercularis). Chloroplast degradation also seemed to differ between species, as many degraded plastids were found in Ammonia sp. and E. oceanense compared to other investigated species. Digestion ability, along with different feeding and sequestration strategies may explain the differences in retention time between taxa. Additionally, the organization of the sequestered plastids within the endoplasm may also suggest behavioral strategies to expose and/or protect the sequestered plastids to/from light and/or to favor gas and/or nutrient exchange with their surrounding habitats.
PreprintUltrastructural observations on prokaryotic associates of benthic foraminifera : food, mutualistic symbionts, or parasites?( 2017-09) Bernhard, Joan M. ; Tsuchiya, Masashi ; Nomaki, HidetakaBecause prokaryotes (Eubacteria, Archaea) are ubiquitous in the marine realm, it may not be surprising that they are important to the diet of at least some foraminifera. Over recent decades, Transmission Electron Microscopy (TEM) has revealed that, at the ultrastructural level, additional intimate relationships exist between prokaryotes and foraminifera. For example, the cytoplasm of a variety of benthic foraminiferal species contains intact prokaryotes. Other benthic foraminiferal species support prokaryotic populations on their exterior. Some of these prokaryote-foraminifera associations are sufficiently consistent to be considered symbioses. Symbiotic relationships include beneficial associations (mutualism; commensalism) to detrimental associations (parasitism). Here, we provide a synopsis of known foraminiferal- prokaryotic symbioses and TEM micrographs illustrating many specific associations. We further comment on and illustrate additional interactions such as bacterial scavenging on foraminifera and foraminiferal feeding on prokaryotes. Documenting and understanding all of these microbial interactions will contribute to a more comprehensive knowledge of benthic marine ecology and biology.
ArticleIntracellular isotope localization in Ammonia sp. (Foraminifera) of oxygen-depleted environments : results of nitrate and sulfate labeling experiments(Frontiers Media, 2016-02-19) Nomaki, Hidetaka ; Bernhard, Joan M. ; Ishida, Akizumi ; Tsuchiya, Masashi ; Uematsu, Katsuyuki ; Tame, Akihiro ; Kitahashi, Tomo ; Takahata, Naoto ; Sano, Yuji ; Toyofuku, TakashiSome benthic foraminiferal species are reportedly capable of nitrate storage and denitrification, however, little is known about nitrate incorporation and subsequent utilization of nitrate within their cell. In this study, we investigated where and how much 15N or 34S were assimilated into foraminiferal cells or possible endobionts after incubation with isotopically labeled nitrate and sulfate in dysoxic or anoxic conditions. After 2 weeks of incubation, foraminiferal specimens were fixed and prepared for Transmission Electron Microscopy (TEM) and correlative nanometer-scale secondary ion mass spectrometry (NanoSIMS) analyses. TEM observations revealed that there were characteristic ultrastructural features typically near the cell periphery in the youngest two or three chambers of the foraminifera exposed to anoxic conditions. These structures, which are electron dense and ~200–500 nm in diameter and co-occurred with possible endobionts, were labeled with 15N originated from 15N-labeled nitrate under anoxia and were labeled with both 15N and 34S under dysoxia. The labeling with 15N was more apparent in specimens from the dysoxic incubation, suggesting higher foraminiferal activity or increased availability of the label during exposure to oxygen depletion than to anoxia. Our results suggest that the electron dense bodies in Ammonia sp. play a significant role in nitrate incorporation and/or subsequent nitrogen assimilation during exposure to dysoxic to anoxic conditions.
ArticleHydrothermal vent chimney-base sediments as unique habitat for meiobenthos and nanobenthos: observations on millimeter-scale distributions(Frontiers Media, 2023-01-12) Bernhard, Joan M. ; Nomaki, Hidetaka ; Shiratori, Takashi ; Elmendorf, Anastasia ; Yabuki, Akinori ; Kimoto, Katsunori ; Tsuchiya, Masashi ; Shimanaga, MotohiroHydrothermal vents are critical to marine geochemical cycling and ecosystem functioning. Although hydrothermal vent-associated megafauna and chemoautotrophic prokaryotes have received extensive dedicated study, smaller hydrothermal vent-associated eukaryotes such as meiofauna and nanobiota have received much less attention. These communities comprise critical links in trophic flow and carbon cycling of other marine habitats, so study of their occurrence and role in hydrothermal vent ecosystems is warranted. Further, an understudied vent habitat is the thin sediment cover at the base of hydrothermal vent chimneys. An initial study revealed that sediments at the base of vent chimneys of the Izu-Ogawasara Arc system (western North Pacific) support metazoan meiofauna, but very little is known about the taxonomic composition and abundance of the meiobenthic protists and nanobiota, or their millimeter-scale distributions. Using the Fluorescently Labeled Embedded Coring method (FLEC), we describe results on meiofaunal and nanobiota higher-level identifications, life positions and relative abundances within sediments from three habitats (base of vent chimneys, inside caldera but away from chimneys, and outside caldera) of the Myojin-Knoll caldera and vicinity. Results suggest that the chimney-base community is unique and more abundant compared to non-chimney associated eukaryotic communities. Supporting evidence (molecular phylogeny, scanning and transmission electron microscopy imaging) documents first known hydrothermal-vent-associated occurrences for two protist taxa. Collectively, results provide valuable insights into a cryptic component of the hydrothermal vent ecosystem.