{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,18]],"date-time":"2026-01-18T22:55:45Z","timestamp":1768776945043,"version":"3.49.0"},"reference-count":41,"publisher":"Springer Science and Business Media LLC","issue":"3","license":[{"start":{"date-parts":[[2021,6,1]],"date-time":"2021-06-01T00:00:00Z","timestamp":1622505600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.springer.com\/tdm"},{"start":{"date-parts":[[2021,6,1]],"date-time":"2021-06-01T00:00:00Z","timestamp":1622505600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/www.springer.com\/tdm"}],"funder":[{"DOI":"10.13039\/501100009027","name":"Advanced Low Carbon Technology Research and Development Program","doi-asserted-by":"publisher","award":["JPMJAL1105"],"award-info":[{"award-number":["JPMJAL1105"]}],"id":[{"id":"10.13039\/501100009027","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Mar Biotechnol"],"published-print":{"date-parts":[[2021,6]]},"DOI":"10.1007\/s10126-021-10037-4","type":"journal-article","created":{"date-parts":[[2021,6,9]],"date-time":"2021-06-09T16:04:33Z","timestamp":1623254673000},"page":"456-462","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":21,"title":["Characterization of a CO2-Concentrating Mechanism with Low Sodium Dependency in the Centric Diatom Chaetoceros gracilis"],"prefix":"10.1007","volume":"23","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-5663-6855","authenticated-orcid":false,"given":"Yoshinori","family":"Tsuji","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"George","family":"Kusi-Appiah","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Noriko","family":"Kozai","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yuri","family":"Fukuda","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6578-8095","authenticated-orcid":false,"given":"Takashi","family":"Yamano","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0963-5662","authenticated-orcid":false,"given":"Hideya","family":"Fukuzawa","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2021,6,9]]},"reference":[{"key":"10037_CR1","doi-asserted-by":"publisher","first-page":"494","DOI":"10.1016\/j.mam.2012.07.009","volume":"34","author":"SL Alper","year":"2013","unstructured":"Alper SL, Sharma AK (2013) The SLC26 gene family of anion transporters and channels. Mol Aspects Med 34:494\u2013515","journal-title":"Mol Aspects Med"},{"key":"10037_CR2","doi-asserted-by":"publisher","first-page":"543","DOI":"10.1016\/0272-7714(84)90089-1","volume":"18","author":"LE Brand","year":"1984","unstructured":"Brand LE (1984) The salinity tolerance of forty-six marine phytoplankton isolates. Estuar Coast Shelf Sci 18:543\u2013556","journal-title":"Estuar Coast Shelf Sci"},{"key":"10037_CR3","doi-asserted-by":"publisher","first-page":"1378","DOI":"10.4319\/lo.2001.46.6.1378","volume":"46","author":"S Burkhardt","year":"2001","unstructured":"Burkhardt S, Amoroso G, Riebesell U (2001) CO2 and HCO3\u2212 uptake in marine diatoms acclimated to different CO2 concentrations. Limnol Oceanogr 46:1378\u20131391","journal-title":"Limnol Oceanogr"},{"key":"10037_CR4","doi-asserted-by":"publisher","first-page":"98","DOI":"10.1016\/j.ecss.2015.05.005","volume":"162","author":"J Carstensen","year":"2015","unstructured":"Carstensen J, Klais R, Cloern JE (2015) Phytoplankton blooms in estuarine and coastal waters: seasonal patterns and key species. Estuar Coast Shelf Sci 162:98\u2013109","journal-title":"Estuar Coast Shelf Sci"},{"key":"10037_CR5","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s41467-017-02426-y","volume":"9","author":"A Chrachri","year":"2018","unstructured":"Chrachri A, Hopkinson BM, Flynn K, Brownlee C, Wheeler GL (2018) Dynamic changes in carbonate chemistry in the microenvironment around single marine phytoplankton cells. Nat Commun 9:74","journal-title":"Nat Commun"},{"key":"10037_CR6","doi-asserted-by":"publisher","first-page":"423","DOI":"10.1042\/BJ20081634","volume":"417","author":"E Cordat","year":"2009","unstructured":"Cordat E, Casey JR (2009) Bicarbonate transport in cell physiology and disease. Biochem J 417:423\u2013439","journal-title":"Biochem J"},{"key":"10037_CR7","doi-asserted-by":"publisher","first-page":"34","DOI":"10.1007\/BF00240893","volume":"191","author":"Z Drechsler","year":"1993","unstructured":"Drechsler Z, Beer S (1991) Utilization of inorganic carbon by\u00a0Ulva lactuca. Plant Physiol. 97:1439\u20131440","journal-title":"Planta"},{"key":"10037_CR8","doi-asserted-by":"publisher","first-page":"5990","DOI":"10.1073\/pnas.0812885106","volume":"106","author":"D Duanmu","year":"2009","unstructured":"Duanmu D, Miller AR, Horken KM, Weeks DP, Spalding MH (2009) Knockdown of limiting-CO2-induced gene HLA3 decreases HCO3- transport and photosynthetic Ci affinity in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 106:5990\u20135995","journal-title":"Proc Natl Acad Sci USA"},{"key":"10037_CR9","doi-asserted-by":"publisher","first-page":"237","DOI":"10.1126\/science.281.5374.237","volume":"281","author":"CB Field","year":"1998","unstructured":"Field CB, Behrenfeld MJ, Randerson JT, Falkowski P (1998) Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281:237\u2013240","journal-title":"Science"},{"key":"10037_CR10","doi-asserted-by":"publisher","first-page":"759","DOI":"10.1093\/oxfordjournals.pcp.a078819","volume":"36","author":"S Fujii","year":"1995","unstructured":"Fujii S, Nishimoto N, Notoya A, Hellebust JA (1995) Growth and osmoregulation of Chaetoceros muelleri in relation to salinity. Plant Cell Physiol 36:759\u2013764","journal-title":"Plant Cell Physiol"},{"key":"10037_CR11","doi-asserted-by":"publisher","first-page":"99","DOI":"10.1146\/annurev.arplant.56.032604.144052","volume":"56","author":"M Giordano","year":"2005","unstructured":"Giordano M, Beardall J, Raven JA (2005) CO2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. Annu Rev Plant Biol 56:99\u2013131","journal-title":"Annu Rev Plant Biol"},{"key":"10037_CR12","doi-asserted-by":"publisher","first-page":"349","DOI":"10.1007\/BF00349158","volume":"113","author":"A Goyal","year":"1992","unstructured":"Goyal A, Shiraiwa Y, Husic HD, Tolbert NE (1992) External and internal carbonic anhydrases in Dunaliella species. Mar Biol 113:349\u2013355","journal-title":"Mar Biol"},{"key":"10037_CR13","doi-asserted-by":"publisher","first-page":"229","DOI":"10.1139\/m62-029","volume":"8","author":"RR Guillard","year":"1962","unstructured":"Guillard RR, Ryther JH (1962) Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt, and Detonula confervacea (cleve) Gran. Can J Microbiol 8:229\u2013239","journal-title":"Can J Microbiol"},{"key":"10037_CR14","first-page":"28","volume":"16","author":"PJ Harrison","year":"1980","unstructured":"Harrison PJ, Waters RE, Taylor FJR (1980) A broad spectrum artificial seawater medium for coastal and open ocean phytoplankton. J Phycol 16:28\u201335","journal-title":"J Phycol"},{"key":"10037_CR15","doi-asserted-by":"publisher","first-page":"1142","DOI":"10.1104\/pp.113.217737","volume":"162","author":"BM Hopkinson","year":"2013","unstructured":"Hopkinson BM, Meile C, Shen C (2013) Quantification of extracellular carbonic anhydrase activity in two marine diatoms and investigation of its role. Plant Physiol 162:1142\u20131152","journal-title":"Plant Physiol"},{"key":"10037_CR16","doi-asserted-by":"publisher","first-page":"1107","DOI":"10.1111\/tpj.14745","volume":"102","author":"A Kono","year":"2020","unstructured":"Kono A, Chou T, Radhakrishnan A, Bolla JR, Sankar K, Shome S, Su C, Jernigan RL, Robinson CV, Yu EW, Spalding MH (2020) Structure and function of LCI1: a plasma membrane CO2 channel in the Chlamydomonas CO2 concentrating mechanism. Plant J 102:1107\u20131126","journal-title":"Plant J"},{"key":"10037_CR17","doi-asserted-by":"publisher","first-page":"371","DOI":"10.1016\/j.tibtech.2010.04.004","volume":"28","author":"A Kumar","year":"2010","unstructured":"Kumar A, Ergas S, Yuan X, Sahu A, Zhang Q, Dewulf J, Malcata FX, van Langenhove H (2010) Enhanced CO2 fixation and biofuel production via microalgae: recent developments and future directions. Trends Biotechnol 28:371\u2013380","journal-title":"Trends Biotechnol"},{"key":"10037_CR18","doi-asserted-by":"publisher","first-page":"54","DOI":"10.1111\/nph.14749","volume":"217","author":"LCM Mackinder","year":"2018","unstructured":"Mackinder LCM (2018) The Chlamydomonas CO2-concentrating mechanism and its potential for engineering photosynthesis in plants. New Phytol 217:54\u201361","journal-title":"New Phytol"},{"key":"10037_CR19","doi-asserted-by":"publisher","first-page":"20160403","DOI":"10.1098\/rstb.2016.0403","volume":"372","author":"Y Matsuda","year":"2017","unstructured":"Matsuda Y, Hopkinson BM, Nakajima K, Dupont CL, Tsuji Y (2017) Mechanisms of carbon dioxide acquisition and CO2 sensing in marine diatoms: a gateway to carbon metabolism. Philos Trans R Soc Lond B Biol Sci 372:20160403","journal-title":"Philos Trans R Soc Lond B Biol Sci"},{"key":"10037_CR20","doi-asserted-by":"publisher","first-page":"177","DOI":"10.1104\/pp.79.1.177","volume":"79","author":"JV Moroney","year":"1985","unstructured":"Moroney JV, Husic HD, Tolbert NE (1985) Effect of carbonic anhydrase inhibitors on inorganic carbon accumulation by Chlamydomonas reinhardtii. Plant Physiol 79:177\u2013183","journal-title":"Plant Physiol"},{"key":"10037_CR21","doi-asserted-by":"publisher","first-page":"1767","DOI":"10.1073\/pnas.1216234110","volume":"110","author":"K Nakajima","year":"2013","unstructured":"Nakajima K, Tanaka A, Matsuda Y (2013) SLC4 family transporters in a marine diatom directly pump bicarbonate from seawater. Proc Natl Acad Sci USA 110:1767\u20131772","journal-title":"Proc Natl Acad Sci USA"},{"key":"10037_CR22","doi-asserted-by":"publisher","first-page":"359","DOI":"10.1029\/95GB01070","volume":"9","author":"DM Nelson","year":"1995","unstructured":"Nelson DM, Tr\u00e9guer P, Brzezinski MA, Leynaert A, Qu\u00e9guiner B (1995) Production and dissolution of biogenic silica in the ocean: revised global estimates, comparison with regional data and relationship to biogenic sedimentation. Global Biogeochem Cycles 9:359\u2013372","journal-title":"Global Biogeochem Cycles"},{"key":"10037_CR23","doi-asserted-by":"publisher","first-page":"625","DOI":"10.1111\/j.0022-3646.1997.00625.x","volume":"33","author":"NA Nimer","year":"1997","unstructured":"Nimer NA, Iglesias-Rodriguez MD, Merrett MJ (1997) Bicarbonate utilization by marine phytoplankton species. J Phycol 33:625\u2013631","journal-title":"J Phycol"},{"key":"10037_CR24","doi-asserted-by":"publisher","first-page":"322","DOI":"10.3390\/biom9080322","volume":"9","author":"T Nonoyama","year":"2019","unstructured":"Nonoyama T, Kazamia E, Nawaly H, Gao X, Tsuji Y, Matsuda Y, Bowler C, Tanaka T, Dorrell RG (2019) Metabolic innovations underpinning the origin and diversification of the diatom chloroplast. Biomolecules 9:322","journal-title":"Biomolecules"},{"key":"10037_CR25","doi-asserted-by":"publisher","first-page":"3105","DOI":"10.1105\/tpc.109.071811","volume":"22","author":"N Ohnishi","year":"2010","unstructured":"Ohnishi N, Mukherjee B, Tsujikawa T, Yanase M, Nakano H, Moroney JV, Fukuzawa H (2010) Expression of a low CO2\u2013inducible protein, LCI1, increases inorganic carbon uptake in the green alga Chlamydomonas reinhardtii. Plant Cell 22:3105\u20133117","journal-title":"Plant Cell"},{"key":"10037_CR26","doi-asserted-by":"publisher","first-page":"18228","DOI":"10.1073\/pnas.0405211101","volume":"101","author":"GD Price","year":"2004","unstructured":"Price GD, Woodger FJ, Badger MR, Howitt SM, Tucker L (2004) Identification of a SulP-type bicarbonate transporter in marine cyanobacteria. Proc Natl Acad Sci USA 101:18228\u201318233","journal-title":"Proc Natl Acad Sci USA"},{"key":"10037_CR27","doi-asserted-by":"publisher","first-page":"332","DOI":"10.1093\/jxb\/35.3.332","volume":"35","author":"TAV Rees","year":"1984","unstructured":"Rees TAV (1984) Sodium dependent photosynthetic oxygen evolution in a marine diatom. J Exp Bot 35:332\u2013337","journal-title":"J Exp Bot"},{"key":"10037_CR28","doi-asserted-by":"publisher","first-page":"291","DOI":"10.1146\/annurev-marine-120709-142720","volume":"3","author":"JR Reinfelder","year":"2011","unstructured":"Reinfelder JR (2011) Carbon concentrating mechanisms in eukaryotic marine phytoplankton. Ann Rev Mar Sci 3:291\u2013315","journal-title":"Ann Rev Mar Sci"},{"key":"10037_CR29","doi-asserted-by":"publisher","first-page":"845","DOI":"10.1111\/j.0022-3646.1997.00845.x","volume":"33","author":"SB Roberts","year":"1997","unstructured":"Roberts SB, Lane TW, Morel FMM (1997) Carbonic anhydrase in the marine diatom Thalassiosira weissflogii (Bacillariophyceae). J Phycol 33:845\u2013850","journal-title":"J Phycol"},{"key":"10037_CR30","doi-asserted-by":"publisher","first-page":"913","DOI":"10.1111\/j.1365-3040.1995.tb00600.x","volume":"18","author":"C Rotatore","year":"1995","unstructured":"Rotatore C, Colman B, Kuzma M (1995) The active uptake of carbon dioxide by the marine diatoms Phaeodactylum tricornutum and Cyclotella sp. Plant, Cell Environ 18:913\u2013918","journal-title":"Plant, Cell Environ"},{"key":"10037_CR31","doi-asserted-by":"publisher","first-page":"235","DOI":"10.1007\/s11120-014-9967-x","volume":"121","author":"M Samukawa","year":"2014","unstructured":"Samukawa M, Shen C, Hopkinson BM, Matsuda Y (2014) Localization of putative carbonic anhydrases in the marine diatom, Thalassiosira pseudonana. Photosynth Res 121:235\u2013249","journal-title":"Photosynth Res"},{"key":"10037_CR32","doi-asserted-by":"publisher","first-page":"3937","DOI":"10.1093\/jxb\/erx163","volume":"68","author":"C Shen","year":"2017","unstructured":"Shen C, Dupont CL, Hopkinson BM (2017) The diversity of CO2-concentrating mechanisms in marine diatoms as inferred from their genetic content. J Exp Bot 68:3937\u20133948","journal-title":"J Exp Bot"},{"key":"10037_CR33","doi-asserted-by":"publisher","first-page":"18658","DOI":"10.1074\/jbc.M112468200","volume":"277","author":"M Shibata","year":"2002","unstructured":"Shibata M, Katoh H, Sonoda M, Ohkawa H, Shimoyama M, Fukuzawa H, Kaplan A, Ogawa T (2002) Genes essential to sodium-dependent bicarbonate transport in cyanobacteria: function and phylogenetic analysis. J Biol Chem 277:18658\u201318664","journal-title":"J Biol Chem"},{"key":"10037_CR34","doi-asserted-by":"publisher","first-page":"1159","DOI":"10.1111\/jpy.12572","volume":"53","author":"TJ Smith-Harding","year":"2017","unstructured":"Smith-Harding TJ, Beardall J, Mitchell JG (2017) The role of external carbonic anhydrase in photosynthesis during growth of the marine diatom Chaetoceros muelleri. J Phycol 53:1159\u20131170","journal-title":"J Phycol"},{"key":"10037_CR35","doi-asserted-by":"publisher","first-page":"205","DOI":"10.1007\/s11120-011-9634-4","volume":"109","author":"M Tachibana","year":"2011","unstructured":"Tachibana M, Allen AE, Kikutani S, Endo Y, Bowler C, Matsuda Y (2011) Localization of putative carbonic anhydrases in two marine diatoms, Phaeodactylum tricornutum and Thalassiosira pseudonana. Photosynth Res 109:205\u2013221","journal-title":"Photosynth Res"},{"key":"10037_CR36","doi-asserted-by":"publisher","first-page":"235","DOI":"10.1186\/s13068-016-0649-0","volume":"9","author":"H Tokushima","year":"2016","unstructured":"Tokushima H, Inoue-Kashino N, Nakazato Y, Masuda A, Ifuku K, Kashino Y (2016) Advantageous characteristics of the diatom Chaetoceros gracilis as a sustainable biofuel producer. Biotechnol Biofuels 9:235","journal-title":"Biotechnol Biofuels"},{"key":"10037_CR37","doi-asserted-by":"publisher","first-page":"3949","DOI":"10.1093\/jxb\/erx102","volume":"68","author":"Y Tsuji","year":"2017","unstructured":"Tsuji Y, Mahardika A, Matsuda Y (2017a) Evolutionarily distinct strategies for the acquisition of inorganic carbon from seawater in marine diatoms. J Exp Bot 68:3949\u20133958","journal-title":"J Exp Bot"},{"key":"10037_CR38","doi-asserted-by":"publisher","first-page":"3763","DOI":"10.1093\/jxb\/erx173","volume":"68","author":"Y Tsuji","year":"2017","unstructured":"Tsuji Y, Nakajima K, Matsuda Y (2017b) Molecular aspects of the biophysical CO2-concentrating mechanism and its regulation in marine diatoms. J Exp Bot 68:3763\u20133772","journal-title":"J Exp Bot"},{"key":"10037_CR39","doi-asserted-by":"publisher","first-page":"42","DOI":"10.1002\/jobm.200800352","volume":"49","author":"T Yamano","year":"2009","unstructured":"Yamano T, Fukuzawa H (2009) Carbon-concentrating mechanism in a green alga, Chlamydomonas reinhardtii, revealed by transcriptome analyses. J Basic Microbiol 49:42\u201351","journal-title":"J Basic Microbiol"},{"key":"10037_CR40","doi-asserted-by":"publisher","first-page":"7315","DOI":"10.1073\/pnas.1501659112","volume":"112","author":"T Yamano","year":"2015","unstructured":"Yamano T, Sato E, Iguchi H, Fukuda Y, Fukuzawa H (2015) Characterization of cooperative bicarbonate uptake into chloroplast stroma in the green alga Chlamydomonas reinhardtii. Proc Natl Acad Sci U S A 112:7315\u20137320","journal-title":"Proc Natl Acad Sci U S A"},{"key":"10037_CR41","doi-asserted-by":"publisher","first-page":"3445","DOI":"10.1093\/jxb\/erw163","volume":"67","author":"JN Young","year":"2016","unstructured":"Young JN, Heureux AMC, Sharwood RE, Rickaby REM, Morel FMM, Whitney SM (2016) Large variation in the Rubisco kinetics of diatoms reveals diversity among their carbon-concentrating mechanisms. J Exp Bot 67:3445\u20133456","journal-title":"J Exp Bot"}],"container-title":["Marine Biotechnology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s10126-021-10037-4.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1007\/s10126-021-10037-4\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s10126-021-10037-4.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,4,18]],"date-time":"2022-04-18T05:24:58Z","timestamp":1650259498000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1007\/s10126-021-10037-4"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,6]]},"references-count":41,"journal-issue":{"issue":"3","published-print":{"date-parts":[[2021,6]]}},"alternative-id":["10037"],"URL":"https:\/\/doi.org\/10.1007\/s10126-021-10037-4","relation":{},"ISSN":["1436-2228","1436-2236"],"issn-type":[{"value":"1436-2228","type":"print"},{"value":"1436-2236","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,6]]},"assertion":[{"value":"16 March 2021","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"13 May 2021","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"9 June 2021","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"The authors declare no competing interests.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Conflict of interest"}}]}}