Molecular mechanisms of foraminiferal calcification

• Project/Area Number: 17H02978
• Research Category: Grant-in-Aid for Scientific Research (B)
• Allocation Type: Single-year Grants
• Section: 一般
• Research Field: Stratigraphy/Paleontology
• Research Institution: Kochi University
• Principal Investigator: Ujiie Yurika 高知大学, 教育研究部自然科学系理工学部門, 准教授 (20573041)
• Co-Investigator(Kenkyū-buntansha): 豊福 高志 国立研究開発法人海洋研究開発機構, 超先鋭研究開発部門(超先鋭技術開発プログラム), 主任研究員 (30371719) ; 石谷 佳之 筑波大学, 計算科学研究センター, 研究員 (60772043) ; 生田 哲朗 国立研究開発法人海洋研究開発機構, 地球環境部門(海洋生物環境影響研究センター), 技術研究員 (80584846)
• Project Period (FY): 2017-04-01 – 2020-03-31
• Project Status: Completed (Fiscal Year 2019)
• Budget Amount: ¥17,810,000 (Direct Cost: ¥13,700,000、Indirect Cost: ¥4,110,000); Fiscal Year 2019: ¥3,900,000 (Direct Cost: ¥3,000,000、Indirect Cost: ¥900,000); Fiscal Year 2018: ¥4,680,000 (Direct Cost: ¥3,600,000、Indirect Cost: ¥1,080,000); Fiscal Year 2017: ¥9,230,000 (Direct Cost: ¥7,100,000、Indirect Cost: ¥2,130,000)
• Keywords: トランスクリプトーム解析 / バイオミネラリゼーション / 有孔虫 / カルシウムシグナリング / バイミネラリゼーション / 単細胞真核生物 / トランスクリプトーム / ゲノム / RNA-seq / ゲノム解析 / バイオミネラリぜーション / 発現解析 / 進化 / ガラス質石灰殻 / 遺伝子

Outline of Final Research Achievements

Foraminifers, large body-sized unicellular eukaryote, synthesize CaCO3 biominerals as a result of interactions between biological activity and environment and contribute to ~25 % CaCO3 production in the pelagic ocean nowadays. However, the molecular processes of foraminiferal calcification are completely unknown. This study successfully showed the foraminiferal molecular mechanisms that play an important role in calcification associating with cell growth and mitochondrial dynamics. We found calcium ion (Ca2+) is actively taken into a cell as essential element for boosting mitochondrial adenosine triphosphate synthesis. As much positive uptake of Ca2+ leads damaging mitochondria, unnecessary Ca2+ is pumped out at extracellular calcification site. Our results demonstrate that foraminifers have achieved fundamental calcium metabolism, whereas they utilize this function to develop a large cell. CaCO3 biominerals are end products of calcium metabolism.

Academic Significance and Societal Importance of the Research Achievements

有孔虫のバイオミネラリゼーションに関連する生理現象を包括的に捉える事により、石灰化の分子機構を明らかにすることに世界で初めて成功した。進化的な側面も踏まえ、バイオミネラルの新しい機能について提案した。
石灰化に関する遺伝子群の検出は、海洋温暖化や酸性化など、環境変化に対する生物応答を検証する上で、具体的な候補遺伝子を挙げる事ができ、環境問題について遺伝子発現の違いなど異なる切り口で取り組む基盤を本研究は構築した。

Research Products

• [Int'l Joint Research] University of Urbino/University of Siena(イタリア)
• [Journal Article] Nanoparticle-Biological Interactions in a Marine Benthic Foraminifer (2019)
  • Author(s): Ciacci Caterina、Grimmelpont Margot V.、Corsi Ilaria、Bergami Elisa、Curzi Davide、Burini Debora、Bouchet Vincent M. P.、Ambrogini Patrizia、Gobbi Pietro、Ujiie Yurika、Ishitani Yoshiyuki、Coccioni Rodolfo、Bernhard Joan M.、Frontalini Fabrizio
  • Journal Title: Scientific Reports Volume: 9 Issue: 1 Pages: 19441-19441
  • DOI: 10.1038/s41598-019-56037-2
  • Peer Reviewed / Int'l Joint Research
• [Journal Article] Foraminiferal Ultrastructure: A perspective From Fluorescent and Fluorogenic Probes (2019)
  • Author(s): Frontalini F.、Losada M. T.、Toyofuku T.、Tyszka J.、Golen J.、Nooijer L.、Canonico B.、Cesarini E.、Nagai Y.、Bickmeyer U.、Ikuta T.、Tsubaki R.、Besteiro Rodriguez C.、Al‐Enezi E.、Papa S.、Coccioni R.、Bijma J.、Bernhard J. M.
  • Journal Title: Journal of Geophysical Research: Biogeosciences Volume: 124 Issue: 9 Pages: 2823-2850
  • DOI: 10.1029/2019jg005113
  • Peer Reviewed / Open Access / Int'l Joint Research
• [Journal Article] Shell formation of foraminifera -marine unicellular calcifiers- (2019)
  • Author(s): 豊福 高志、長井 裕季子
  • Journal Title: Journal of the Japanese Association for Crystal Growth Volume: 46 Issue: 3 Pages: n/a
  • DOI: 10.19009/jjacg.46-3-02
  • NAID: 130007744151
  • ISSN: 0385-6275, 2187-8366
  • Peer Reviewed
• [Journal Article] Advanced approach to analyzing calcareous protists for present and past pelagic ecology: comprehensive analysis of 3D-morphology, stable isotopes, and genes of planktic foraminifers (2019)
  • Author(s): Ujiie, U., Kimoto, K., Ishimura, T.
  • Journal Title: PLoS ONE Volume: e0213282 Issue: 3 Pages: 1-19
  • DOI: 10.1371/journal.pone.0213282
  • Peer Reviewed / Open Access
• [Journal Article] Perspective on the response of marine calcifiers to global warming and ocean acidification?Behavior of corals and foraminifera in a high CO2 world “hot house” (2019)
  • Author(s): Kawahata Hodaka、Fujita Kazuhiko、Iguchi Akira、Inoue Mayuri、Iwasaki Shinya、Kuroyanagi Azumi、Maeda Ayumi、Manaka Takuya、Moriya Kazuyoshi、Takagi Haruka、Toyofuku Takashi、Yoshimura Toshihiro、Suzuki Atsushi
  • Journal Title: Progress in Earth and Planetary Science Volume: 6 Issue: 1 Pages: 1-37
  • DOI: 10.1186/s40645-018-0239-9
  • Peer Reviewed / Open Access / Int'l Joint Research
• [Journal Article] Effect of Euxinic Conditions on Planktic Foraminifers: Culture Experiments and Implications for Past and Future Environments (2019)
  • Author(s): Kuroyanagi Azumi、Toyofuku Takashi、Nagai Yukiko、Kimoto Katsunori、Nishi Hiroshi、Takashima Reishi、Kawahata Hodaka
  • Journal Title: Paleoceanography and Paleoclimatology Volume: 34 Issue: 1 Pages: 54-62
  • DOI: 10.1029/2018pa003539
  • Peer Reviewed / Open Access
• [Journal Article] Weaving of biomineralization framework in rotaliid foraminifera: implications for paleoceanographic proxies (2018)
  • Author(s): Nagai Yukiko、Uematsu Katsuyuki、Chen Chong、Wani Ryoji、Tyszka Jaroslaw、Toyofuku Takashi
  • Journal Title: Biogeosciences Volume: 15 Issue: 22 Pages: 6773-6789
  • DOI: 10.5194/bg-15-6773-2018
  • Peer Reviewed / Open Access / Int'l Joint Research
• [Journal Article] Decalcification and survival of benthic foraminifera under the combined impacts of varying pH and salinity (2018)
  • Author(s): Charrieau Laurie M.、Filipsson Helena L.、Nagai Yukiko、Kawada Sachiko、Ljung Karl、Kritzberg Emma、Toyofuku Takashi
  • Journal Title: Marine Environmental Research Volume: 138 Pages: 36-45
  • DOI: 10.1016/j.marenvres.2018.03.015
  • Peer Reviewed / Int'l Joint Research
• [Journal Article] Reading the Fine Print: Ultra-Microstructures of Foraminiferal Calcification Revealed Using Focused Ion Beam Microscopy (2018)
  • Author(s): Nagai Yukiko、Uematsu Katsuyuki、Wani Ryoji、Toyofuku Takashi
  • Journal Title: Frontiers in Marine Science Volume: 5 Pages: 1-15
  • DOI: 10.3389/fmars.2018.00067
  • Peer Reviewed / Open Access
• [Journal Article] Hierarchical textures on aragonitic shells of the hyaline radial foraminifer Hoeglundina elegans (2017)
  • Author(s): Nakajima, K., M. Suzuki, Y. Nagai, K. Izumida, Y. Oaki, T. Toyofuku, J. Bijma, G. Nehrke, M. Raitzsch, K. Tani and H. Imai
  • Journal Title: CrystEngComm Volume: 19 Issue: 47 Pages: 7191-7196
  • DOI: 10.1039/c7ce01870c
  • Peer Reviewed / Int'l Joint Research
• [Journal Article] The Impacts of Seawater Mg/Ca and Temperature on Element Incorporation in Benthic Foraminiferal Calcite (2017)
  • Author(s): de Nooijer L. J.、van Dijk I.、Toyofuku T.、Reichart G. J.
  • Journal Title: Geochemistry, Geophysics, Geosystems Volume: 18 Issue: 10 Pages: 3617-3630
  • DOI: 10.1002/2017gc007183
  • Peer Reviewed / Int'l Joint Research
• [Presentation] トランスクリプーム解析に基づく有孔虫の石灰化分子機構 (2020)
  • Author(s): 氏家由利香，石谷佳之，石井俊一，長井裕季子，高木義弘，生田哲朗，豊福高志
  • Organizer: 日本古生物学会2020年例会
• [Presentation] 有孔虫の大規模分岐年代推定 (2020)
  • Author(s): 石谷佳之，矢崎裕規，氏家由利香，稲垣祐司
  • Organizer: 日本古生物学会2020年例会
• [Presentation] Transcript assembly and quantification identify candidate genes for foraminiferal calcification (2019)
  • Author(s): Ujiie, Y., Ishitani, Y., Ishii, S., Nagai,Y., Takaki, Y., Ikuta T., and Toyofuku, T.
  • Organizer: JpGU meeting 2019
  • Int'l Joint Research
• [Presentation] 有孔虫Ammonia beccariiのミトコンドリアに局在するDNA分子群 (2019)
  • Author(s): 石谷佳之，久米慶太郎，稲垣祐司
  • Organizer: 日本共生生物学会2019年度大会
• [Presentation] Estimation of foraminiferal calcification process from live imaging and FIB-SEM approach (2019)
  • Author(s): Toyofuku T., Nagai, Y.
  • Organizer: JpGU meeting 2019
• [Presentation] 超微細構造などから推測される底生有孔虫Ammoniaの殻形成機序 (2019)
  • Author(s): 豊福高志, 長井裕季子
  • Organizer: 第14回バイオミネラリゼーションワークショップ
• [Presentation] 微化石ができる最初の一歩-ここまでわかった現生有孔虫の殻形成- (2019)
  • Author(s): 豊福高志
  • Organizer: 日本古生物学会2019年年会
  • Invited
• [Presentation] Independent evolution between cell shape and shell materials in foraminifers (2018)
  • Author(s): Ujiie Yurika, Ishitani Yoshiyuki
  • Organizer: JpGU Meeting 2018
• [Presentation] Transcript assembly and quantification by RNA-seq identified candidate genes for foraminiferal biomineralization of Ammonia beccarii (2018)
  • Author(s): Ujiie Yurika, Ishitani Yoshiyuki, Ishii Shunichi, Nagai Yukiko, Takaki Yoshihiro, Toyofuku Takashi
  • Organizer: International Symposium on Foraminifera (FORAMS 2018)
  • Int'l Joint Research
• [Presentation] 有孔虫の炭酸塩の殻形成に関する分子機構－トランスクリプトーム解析から－ (2018)
  • Author(s): 氏家由利香，石谷佳之，石井俊一，長井裕季子，高木義弘，豊福高志，生田哲朗
  • Organizer: バイオミネラリゼーション研究会
• [Presentation] 有孔虫における殻形成機構の解明－石灰化のブラックボックスを開く－ (2018)
  • Author(s): 氏家由利香，石井俊一，石谷佳之，高木義弘，細将貴，Salvatore Cosentino，岩崎渉
  • Organizer: 新学術領域研究 先進ゲノム解析研究推進プラットフォーム 先進ゲノム支援 拡大班会議
• [Presentation] Phylogenomic approach to the early evolution of Foraminifera (2018)
  • Author(s): Ishitani Yoshiyuki, Ujiie Yurika, Yazaki Euki, Toyofuku Takashi, Nagai Yukiko, Inagaki Yuji
  • Organizer: International Symposium on Foraminifera (FORAMS 2018)
  • Int'l Joint Research
• [Presentation] Calcite precipitation rate in foraminiferal calcite and impact on element incorporation (2018)
  • Author(s): Esmee Geerken, Lennart de Nooijer, Takashi Toyofuku, Anne Roepert, Lubos Polerecky, Gert-Jan Reichart
  • Organizer: International Symposium on Foraminifera (FORAMS 2018)
  • Int'l Joint Research
• [Presentation] Proton pumping accompanies calcification in foraminifera (2018)
  • Author(s): Takashi Toyofuku, Miki Y. Matsuo, Lennart Jan de Nooijer, Yukiko Nagai, Tetsuro Ikuta
  • Organizer: International Symposium on Foraminifera (FORAMS 2018)
  • Int'l Joint Research
• [Presentation] Formation Process of Organic membrane within calcareous test and early calcium carbonate deposition of benthic foraminifera Ammonia (2018)
  • Author(s): Yukiko Nagai, Takashi Toyofuku, Chong Chen, Katsunori Uematsu
  • Organizer: International Symposium on Foraminifera (FORAMS 2018)
  • Int'l Joint Research
• [Presentation] Foraminiferal calcification and CO2 (2018)
  • Author(s): Lennart de Nooijer, Takashi Toyofuku, Gert-Jan Reichart
  • Organizer: International Symposium on Foraminifera (FORAMS 2018)
  • Int'l Joint Research
• [Presentation] Foraminiferal ultrastructure: a perspective from fluorescent and fluorogenic probes (2018)
  • Author(s): Fabrizio Frontalini, Maria Teresa Losada, Takashi Toyofuku, Jaroslaw Tyszka, Jan Golen, Lennart de Nooijer, Barbara Canonico, Erica Cesarini, Yukiko Nagai, Tetsuro Ikuta, Remi Tsubaki, Stefano Papa, Rodolfo Coccioni, Jelle Bijma, Joan M. Bernhard
  • Organizer: International Symposium on Foraminifera (FORAMS 2018)
  • Int'l Joint Research
• [Presentation] Combined impacts of ocean acidification and desalination: culture experiments on the coastal species Ammonia sp. and Elphidium crispum (2018)
  • Author(s): Laurie Charrieau, Helena Filipsson, Yukiko Nagai, Sachiko Kawada, Karl Ljung, Emma Kritzberg, Takashi Toyofuku
  • Organizer: International Symposium on Foraminifera (FORAMS 2018)
  • Int'l Joint Research
• [Presentation] Fantastic voyage to the cellular functions of foraminiferal chamber formation (2018)
  • Author(s): Toyofuku Takashi
  • Organizer: International Symposium on Foraminifera (FORAMS 2018)
  • Int'l Joint Research / Invited
• [Presentation] Test density of Ammonia sp. under variable pH (2018)
  • Author(s): Toyofuku Takashi, Nagai Yukiko, Kimono Katsunori, Sasaki Osamu
  • Organizer: JpGU meeting 2018
• [Presentation] Ultra-microstructures of foraminiferal calcification observed using focused ion beam microscopy (2018)
  • Author(s): Nagai Yukiko, Toyofuku Takashi,
  • Organizer: JpGU meeting 2018
• [Presentation] 浮遊性有孔虫１個体による同時３要素（遺伝子・形態・同位体）の分析法の新規開発 (2017)
  • Author(s): 氏家 由利香，石村 豊穂，木元 克典
  • Organizer: JpGU-AGU Joint Meeting
• [Presentation] 原生生物・有孔虫の殻は当てにならないのか？ (2017)
  • Author(s): 氏家 由利香，石谷 佳之
  • Organizer: 日本進化学会
• [Presentation] Synthetical Analysis for Morphology, biological Species,and stable Isotopes (SAMSI) of single-cell planktonic foraminifer (2017)
  • Author(s): Ujiie, Y., Ishimura, T., Kimoto, K.
  • Organizer: AGU Fall meeting
  • Int'l Joint Research
• [Presentation] “いがい” と流されない海の原生生物 (2017)
  • Author(s): 石谷佳之
  • Organizer: 原生生物学会＆共生生物学会合同シンポジウム
  • Invited
• [Presentation] Molecular marker to identify radiolarian species -toward establishment of paleo-environmental proxy- (2017)
  • Author(s): Ishitani, Y.
  • Organizer: AGU Fall Meeting
  • Int'l Joint Research
• [Presentation] Various imaging approaches revealing the secrets of foraminiferal calcification process (2017)
  • Author(s): Toyofuku, T., Nagai, Y.
  • Organizer: 15th Meeting of the International Association of Radiolarists
  • Int'l Joint Research
• [Presentation] Proton transportation of foraminifera for calcification (2017)
  • Author(s): Toyofuku, T., Matsuo, Y. M., de Nooijer, J. L., Ikuta, T., Nagai, Y.
  • Organizer: 14th International Symposium on Biomineralization
  • Int'l Joint Research
• [Presentation] Visualization of pH distribution around dissolving/growing calcium carbonate crystals in inorganic solution: a baseline to understand vital effect in biomineralization (2017)
  • Author(s): Kawano, J., Toyofuku, T., Nishimura, K., Nagai, Y., Kawada, S., Teng, H., Nagai, T.
  • Organizer: 14th International Symposium on Biomineralization
  • Int'l Joint Research
• [Presentation] Structure analysis and property evaluation of spines of planktonic foraminifera (2017)
  • Author(s): Izumida, K., Takasaki, M., Nagai, Y., Okai, Y., Naito, K., Tanaka, Y., Toyofuku, T., Imai, H.
  • Organizer: 14th International Symposium on Biomineralization
  • Int'l Joint Research
• [Presentation] Soft and hard tissue simultaneous observation on site of calcification in calcareous foraminifera. 14th International Symposium on Biomineralization (2017)
  • Author(s): Nagai, Y., Uematsu, K., Toyofuku, T.
  • Organizer: 14th International Symposium on Biomineralization
  • Int'l Joint Research
• [Presentation] Magical Proton Usage on Calcification of Ammonia beccarii -Acidify Environment to Realize Favorable pH at Calcification Site-, (2017)
  • Author(s): Toyofuku, T.
  • Organizer: JpGU-AGU Joint meeting 2017
  • Int'l Joint Research
• [Book] Oceanography and Marine Biology: An annual Review (2019)
  • Author(s): Fitzer, S.C., Chan, V.B.S., Meng, Y., Chandra Rajan, K., Suzuki, M., Not, C.A., Toyofuku, T., Falkenberg, L., Byrne, M., Harvey, B.P., De Wit, P., Cusak, M., Gao, K.S., Taylor, P., Dupont, S., Hall-Spencer, J., Vengatesen, T.
  • Total Pages: 442
  • Publisher: CRC Press
• [Book] アメーバのはなし (2018)
  • Author(s): 石谷佳之、土屋正史
  • Total Pages: 152
  • Publisher: 朝倉書店
  • ISBN: 9784254171686