All Issue

2022 Vol.44, Issue 3

Article

Differential Expression of Three Novel Carbonic Anhydrases (CAs) Genes in Marine Dinoflagellate Prorocentrum minimum Against Various pH Conditions

해양 와편모조류 Prorocentrum minimum 기원 신규 탄산무수화효소(CAs) 유전자 3종의 차등 pH 대응 발현

Jeongmin Shin1†
,
Ha-Eun Lee1†
,
Han-Sol Kim1
,
Jang-Seu Ki1*
신 정민1†
,
이 하은1†
,
김 한솔1
,
기 장서1*
1Department of Biotechnology, College of Biochemical Engineering, Sangmyung University, Seoul 03016, Korea
1상명대학교 생명화학공학부 생명공학과
*Corresponding Author
†These authors contributed equally to this work.
30 September 2022. pp. 209-220
PDF XML Citation
Abstract

Carbonic anhydrase (CA) is a key controller of the carbon concentrating mechanism (CCM), and is known to be affected by ambient pH and CO2 compositions. Herein, we characterized three novel CAs genes (PmCA1, 2, and 3) from the marine dinoflagellate Prorocentrum minimum, and evaluated the relative expressions of the PmCAs and photosynthetic genes PmatpB and PmrbcL under different pH conditions. Each PmCA was predicted to have amino acid residues constituting the zinc binding site. With signal peptide, PmCA1 and PmCA2 were predicted to be intracellular CAs located in the cytoplasm and chloroplast membrane, respectively. On the other hand, PmCA3 was predicted to be extracellular CA located in the plasma membrane. Also, PmCA1 was classified into the beta family, and PmCA2 and PmCA3 were classified into the alpha family via phylogenic analysis. The photosynthesis efficiency of P. minimum was similar at pH 7 to 9, and decreased significantly at pH 6 and pH 10. Overall, relative gene expression levels of the three PmCAs decreased at low pH, and increased as pH increased. Photosynthesis related genes, PmatpB and PmrbcL, showed similar expression patterns to those of PmCAs. These results suggest that changes in seawater pH may affect photosynthesis and CO2 metabolism in marine dinoflagellates.

Keywords
Prorocentrum minimum
Carbonic Anhydrase (CA)
pH
ocean acidification
Carbon Concentrating Mechanism (CCM)
References
1
Aizawa K, Miyachi S (1986) Carbonic anhydrase and CO2 concentrating mechanisms in microalgae and cyanobacteria. FEMS Microbiol Lett 39(3):215-233 10.1111/j.1574-6968.1986.tb01860.x
2
Alvizo O, Nguyen LJ, Savile CK, Bresson JA, Lakhapatri SL, Solis EOP, Fox RJ, Broering JM, Benoit MR, Zimmerman SA, Novick SJ, Liang J, Lalonde JJ (2014) Directed evolution of an ultrastable carbonic anhydrase for highly efficient carbon capture from flue gas. Proc Natl Acad Sci USA 111(46):16436-16441 10.1073/pnas.141146111125368146PMC4246266
3
Anderson DM, Cembella AD, Hallegraeff GM (2012) Progress in understanding harmful algal blooms: paradigm shifts and new technologies for research, monitoring, and management. Annu Rev Mar Sci 4:143-176 10.1146/annurev-marine-120308-08112122457972PMC5373096
4
Anthony KR, Kline DI, Diaz-Pulido G, Dove S, Hoegh- Guldberg O (2008) Ocean acidification causes bleaching and productivity loss in coral reef builders. Proc Natl Acad Sci USA 105(45):17442-17446 10.1073/pnas.080447810518988740PMC2580748
5
Badger MR (2003) CO2 concentrating mechanisms in cyanobacteria: molecular components, their diversity and evolution. J Exp Bot 54(383):609-622 10.1093/jxb/erg07612554704
6
Badger MR, Hanson D, Price GD (2002) Evolution and diversity of CO2 concentrating mechanisms in cyanobacteria. Funct Plant Biol 29(3):161-173 10.1071/PP0121332689463
7
Badger MR, Kaplan A, Berry JA (1980) Internal inorganic carbon pool of Chlamydomonas reinhardtii: evidence for a carbon dioxide-concentrating mechanism. Plant Physiol 66(3):407-413 10.1104/pp.66.3.40716661446PMC440644
8
Badger MR, Price GD (1994) The role of carbonic anhydrase in photosynthesis. Annu Rev Plant Biol 45(1):369-392 10.1146/annurev.pp.45.060194.002101
9
Barker S, Ridgwell A (2012) Ocean acidification. Nat Educ Knowl 3(10):21
10
Beardall J, Giordano M (2002) Ecological implications of microalgal and cyanobacterial CO2 concentrating mechanisms and their regulation. Funct Plant Biol 29(3):335-347 10.1071/PP0119532689480
11
Beardall J, Raven JA (2016) Carbon acquisition by microalgae. In: Borowitzka MA, Beardall J, Raven JA (eds) The physiology of microalgae, vol 6. Springer, Cham, pp 89-99 10.1007/978-3-319-24945-2_4
12
Bercovici A, Vellekoop J (2017) Methods in paleopalynology and palynostratigraphy: an application to the K-Pg boundary. An application to the K-Pg Boundary. In: Zeigler KE, Parker W (eds) Terrestrial depositional systems, vol 1. Elsevier, Amsterdam, pp 127-164 10.1016/B978-0-12-803243-5.00003-0
13
Berge T, Daugbjerg N, Andersen BB, Hansen PJ (2010) Effect of lowered pH on marine phytoplankton growth rates. Mar Ecol-Prog Ser 416:79-91 10.3354/meps08780
14
Bobeszko T (2017) Characterisation of carbonic anhydrase in the symbiotic dinoflagellate Symbiodinium. Ph.D Thesis, James Cook University, Douglas, 184 p
15
Boone CD, Gill S, Habibzadegan A, McKenna R (2013) Carbonic anhydrase: an efficient enzyme with possible global implications. Int J Chem Eng 2013:813931. doi:10. 1155/2013/813931 10.1155/2013/813931
16
Boron WF (2004) Regulation of intracellular pH. Adv Physiol Educ 28(4):160-179 10.1152/advan.00045.200415545345
17
Capasso C, Supuran CT (2015) An overview of the alpha-, beta-and gamma-carbonic anhydrases from Bacteria: can bacterial carbonic anhydrases shed new light on evolution of bacteria? J Enzyme Inhib Med Chem 30(2):325-332 10.3109/14756366.2014.91020224766661
18
Chiang TY, Schaal BA, Peng CI (1998) Universal primers for amplification and sequencing a noncoding spacer between the atpB and rbcL genes of chloroplast DNA. Bot Bull Acad Sin 39:245-250
19
Coleman JR, Grossman AR (1984) Biosynthesis of carbonic anhydrase in Chlamydomonas reinhardtii during adaptation to low CO2. Proc Natl Acad Sci USA 81(19):6049-6053 10.1073/pnas.81.19.604916593518PMC391856
20
Costache TA, Acién Fernández FG, Morales MM, Fernández- Sevilla JM, Stamatin I, Molina E (2013) Comprehensive model of microalgae photosynthesis rate as a function of culture conditions in photobioreactors. Appl Microbiol Biotechnol 97(17):7627-7637 10.1007/s00253-013-5035-223793345
21
DiMario RJ, Machingura MC, Waldrop GL, Moroney JV (2018) The many types of carbonic anhydrases in photosynthetic organisms. Plant Sci 268:11-17 10.1016/j.plantsci.2017.12.00229362079
22
Driessen AJ, Nouwen N (2008) Protein translocation across the bacterial cytoplasmic membrane. Annu Rev Biochem 77:643-667 10.1146/annurev.biochem.77.061606.16074718078384
23
Ebenezer V, Ki JS (2013a) Physiological and biochemical responses of the marine dinoflagellate Prorocentrum minimum exposed to the oxidizing biocide chlorine. Ecotoxicol Environ Saf 92:129-134 10.1016/j.ecoenv.2013.03.01423582993
24
Ebenezer V, Ki JS (2013b) Quantification of toxic effects of the herbicide metolachlor on marine microalgae Ditylum brightwellii (Bacillariophyceae), Prorocentrum minimum (Dinophyceae), and Tetraselmis suecica (Chlorophyceae). Microbiology 51(1):136-139 10.1007/s12275-013-2114-023456723
25
Emameh RZ, Barker H, Tolvanen ME, Ortutay C, Parkkila S (2014) Bioinformatic analysis of beta carbonic anhydrase sequences from protozoans and metazoans. Parasite Vector 7(1):38. doi:10.1186/1756-3305-7-38 10.1186/1756-3305-7-3824447594PMC3907363
26
Fukuzawa H, Tsuzuki M, Miyachi S (2000) Algal carbonic anhydrase. In: Chegwidden WR, Carter ND, Edwards YH (eds) The carbonic anhydrases, vol 90. Birkhäuser, Basel, pp 535-546 10.1007/978-3-0348-8446-4_2811268535
27
Gattuso JP, Buddemeier RW (2000) Calcification and CO2. Nature 407(6802):311-313 10.1038/3503028011014173
28
Gee CW, Niyogi KK (2017) The carbonic anhydrase CAH1 is an essential component of the carbon-concentrating mechanism in Nannochloropsis oceanica. Proc Natl Acad Sci USA 114(17):4537-4542 10.1073/pnas.170013911428396394PMC5410810
29
Gillham NW, Boynton JE (1986) The sequence of the chloroplast atpB gene and its flanking regions in Chlamydomonas reinhardtii. Gene 44(1):17-28 10.1016/0378-1119(86)90038-7
30
Gonçalves AL, Simões M, Pires JCM (2014) The effect of light supply on microalgal growth, CO2 uptake and nutrient removal from wastewater. Energy Convers Manag 85:530-536 10.1016/j.enconman.2014.05.085
31
Griffiths H, Meyer MT, Rickaby RE (2017) Overcoming adversity through diversity: aquatic carbon concentrating mechanisms. J Exp Bot 68(14):3689-3695 10.1093/jxb/erx27828911058PMC5853259
32
Grzebyk D, Berland B (1996) Influences of temperature, salinity and irradiance on growth of Prorocentrum minimum (Dinophyceae) from the Mediterranean Sea. J Plankton Res 18(10):1837-1849 10.1093/plankt/18.10.1837
33
Guillard RR, Ryther JH (1962) Studies of marine planktonic diatoms: I. Cyclotella nana hustedt, and Detonula confervacea (Cleve) Gran. Can J Microbiol 8(2):229-239 10.1139/m62-02913902807
34
Guo R, Ebenezer V, Ki JS (2014) PmMGST3, a novel microsomal glutathione S-transferase gene in the dinoflagellate Prorocentrum minimum, is a potential biomarker of oxidative stress. Gene 546(2):378-385 10.1016/j.gene.2014.05.04624858638
35
Guo R, Ebenezer V, Wang H, Ki JS (2017) Chlorine affects photosystem II and modulates the transcriptional levels of photosynthesis-related genes in the dinoflagellate Prorocentrum minimum. J Appl Phycol 29(1):153-163 10.1007/s10811-016-0955-8
36
Hansen P (2002) Effect of high pH on the growth and survival of marine phytoplankton: implications for species succession. Aquat Microb Ecol 28:279-288 10.3354/ame028279
37
Harding Jr LW (1988) The time-course of photoadaptation to low-light in Prorocentrum mariae lebouriae (Dinophyceae) 1. J Phycol 24(2):274-281 10.1111/j.1529-8817.1988.tb04243.x
38
Harding Jr LW, Coats DW (1988) Photosynthetic physiology of Prorocentrum mariae-lebouriae (Dinophyceae) during its subpycnocline transport in Chesapeake Bay. J Phycol 24(1):77-89 10.1111/j.1529-8817.1988.tb04458.x
39
Harvey LDD (2008) Mitigating the atmospheric CO2 increase and ocean acidification by adding limestone powder to upwelling regions. J Geophys Res 113(C4):C04028. doi:10.1029/2007JC004373 10.1029/2007JC004373
40
Heil CA, Glibert PM, Fan C (2005) Prorocentrum minimum (Pavillard) Schiller: a review of a harmful algal bloom species of growing worldwide importance. Harmful Algae 4(3):449-470 10.1016/j.hal.2004.08.003
41
Henry RP (1996) Multiple roles of carbonic anhydrase in cellular transport and metabolism. Annu Rev Physiol 58:523-538 10.1146/annurev.ph.58.030196.0025158815807
42
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(2):1142-1152 10.1104/pp.113.21773723656892PMC3668045
43
Hopkinson BM, Young JN, Tansik AL, Binder BJ (2014) The minimal CO2-concentrating mechanism of Prochlorococcus spp. MED4 is effective and efficient. Plant Physiol 166(4):2205-2217 10.1104/pp.114.24704925315602PMC4256842
44
Horton P, Park KJ, Obayashi T, Fujita N, Harada H, Adams- Collier CJ, Nakai K (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res 35:W585-W587 10.1093/nar/gkm25917517783PMC1933216
45
IPCC (2014) Summary for policymakers. In: Field CB, Barros VR, Dokken DJ, Mach KJ, Mastrandrea MD, Bilir TE, Chatterjee M, Ebi KL, Estrada YO, Genova RC, Girma B, Kissel ES, Levy AN, MacCracken S, Mastrandrea PR, White LL (eds) Climate change 2014: Impacts, adaptation, and vulnerability. Cambridge University Press, Cambridge and New York, pp 1-32
46
Jeong HJ, Du Yoo Y, Kim JS, Seong KA, Kang NS, Kim TH (2010). Growth, feeding and ecological roles of the mixotrophic and heterotrophic dinoflagellates in marine planktonic food webs. Ocean Sci J 45(2):65-91 10.1007/s12601-010-0007-2
47
Kim H, Wang H, Ki JS (2021) Chloroacetanilides inhibit photosynthesis and disrupt the thylakoid membranes of the dinoflagellate Prorocentrum minimum as revealed with metazachlor treatment. Ecotoxicol Environ Saf 211:111928 10.1016/j.ecoenv.2021.11192833476845
48
Kim W, Park JM, Gim GH, Jeong SH, Kang CM, Kim DJ, Kim SW (2012) Optimization of culture conditions and comparison of biomass productivity of three green algae. Bioprocess Biosyst Eng 35(1-2):19-27 10.1007/s00449-011-0612-121909669
49
Kimpel DL, Togasaki RK, Miyachi S (1983) Carbonic anhydrase in Chlamydomonas reinhardtii I. Localization. Plant Cell Physiol 24(2):255-259 10.1093/pcp/24.2.255
50
Klein U, Salvador ML, Bogorad L (1994) Activity of the Chlamydomonas chloroplast rbcL gene promoter is enhanced by a remote sequence element. Proc Natl Acad Sci USA 91(23):10819-10823 10.1073/pnas.91.23.108197971968PMC45117
51
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35(6):1547–1549 10.1093/molbev/msy09629722887PMC5967553
52
Kupriyanova E, Pronina N, Los D (2017) Carbonic anhydrase - A universal enzyme of the carbon-based life. Photosynthetica 55(1):3-19 10.1007/s11099-017-0685-4
53
Leggat W, Marendy EM, Baillie B, Whitney SM, Ludwig M, Badger MR, Yellowlees D (2002) Dinoflagellate symbioses: strategies and adaptations for the acquisition and fixation of inorganic carbon. Funct Plant Biol 29(3):309-322 10.1071/PP0120232689478
54
Lindskog S (1997) Structure and mechanism of carbonic anhydrase. Pharmacol Ther 74(1):1-20 10.1016/S0163-7258(96)00198-2
55
Mangan NM, Flamholz A, Hood RD, Milo R, Savage DF (2016) pH determines the energetic efficiency of the cyanobacterial CO2 concentrating mechanism. Proc Natl Acad Sci USA 113(36):E5354-E5362 10.1073/pnas.152514511327551079PMC5018799
56
Merrett MJ, Nimer NA, Dong LF (1996) The utilization of bicarbonate ions by the marine microalga Nannochloropsis oculata (Droop) Hibberd. Plant Cell Environ 19(4):478-484 10.1111/j.1365-3040.1996.tb00340.x
57
Mitchell P (1966) Chemiosmotic coupling in oxidative and photosynthetic phosphorylation. Biol Rev Camb Philos Soc 41(3):445-501 10.1111/j.1469-185X.1966.tb01501.x5329743
58
Moroney JV, Somanchi A (1999) How do algae concentrate CO2 to increase the efficiency of photosynthetic carbon fixation? Plant Physiol 119(1):9-16 10.1104/pp.119.1.99880340PMC1539202
59
Moroney JV, Ynalvez RA (2007) Proposed carbon dioxide concentrating mechanism in Chlamydomonas reinhardtii. Eukaryot Cell 6(8):1251-1259 10.1128/EC.00064-0717557885PMC1951128
60
Mustaffa NIH, Striebel M, Wurl O (2017) Enrichment of extracellular carbonic anhydrase in the sea surface microlayer and its effect on air-sea CO2 exchange. Geophys Res Lett 44(24):12,324-12,330 10.1002/2017GL075797
61
Nimer NA, Warren M, Merrett MJ (1998) The regulation of photosynthetic rate and activation of extracellular carbonic anhydrase under CO2-limiting conditions in the marine diatom Skeletonema costatum. Plant Cell Environ 21(8): 805-812 10.1046/j.1365-3040.1998.00321.x
62
Oukarroum A, El Madidi S, Schansker G and Strasser RJ (2007) Probing the responses of barley cultivars (Hordeum vulgare L.) by chlorophyll a fluorescence OLKJIP under drought stress and re-watering. Environ Exp Bot 60(3): 438-446 10.1016/j.envexpbot.2007.01.002
63
Parry MA, Andralojc PJ, Scales JC, Salvucci ME, Carmo- Silva AE, Alonso H, Whitney SM (2013) Rubisco activity and regulation as targets for crop improvement. J Exp Bot 64(3):717-730 10.1093/jxb/ers33623162118
64
Pörtner HO, Langenbuch M, Reipschläger A (2004) Biological impact of elevated ocean CO2 concentrations. lessons from animal physiology and earth history. J Oceanogr 60(4):705-718 10.1007/s10872-004-5763-0
65
Prabhu C, Wanjari S, Gawande S, Das S, Labhsetwar N, Kotwal S, Puri AK, Satyanarayana T, Rayalu S (2009) Immobilization of carbonic anhydrase enriched microorganism on biopolymer based materials. J Mol Catal B Enzym 60(1-2):13-21 10.1016/j.molcatb.2009.02.022
66
Raven JA, Ball LA, Beardall J, Giordano M, Maberly SC (2005) Algae lacking carbon-concentrating mechanisms. Can J Bot 83(7):879-890 10.1139/b05-074
67
Raven JA, Beardall J (2003) Carbon acquisition mechanisms of algae: carbon dioxide diffusion and carbon dioxide concentrating mechanisms. In: Larkum AWD, Douglas SE, Raven JA (eds) Photosynthesis in Algae, vol 14. Springer, Dordrecht, pp 225-244 10.1007/978-94-007-1038-2_11
68
Raven JA, Beardall J, Giordano M (2014) Energy costs of carbon dioxide concentrating mechanisms in aquatic organisms. Photosynth Res 121(2-3):111-124 10.1007/s11120-013-9962-724390639
69
Rickaby REM, Hubbard MRE (2019) Upper ocean oxygenation, evolution of RuBisCO and the Phanerozoic succession of phytoplankton. Free Radic Biol Med 140:295-304 10.1016/j.freeradbiomed.2019.05.00631075497PMC6856715
70
Rost B, Richter KU, Riebesell ULF, Hansen PJ (2006) Inorganic carbon acquisition in red tide dinoflagellates. Plant Cell Environ 29(5):810-822 10.1111/j.1365-3040.2005.01450.x17087465
71
Rowlett RS, Hoffmann KM, Failing H, Mysliwiec MM, Samardzic D (2010) Evidence for a bicarbonate "escort" site in Haemophilus influenzae β-carbonic anhydrase. Biochem 49(17):3640-3647 10.1021/bi100328j20359198PMC2861718
72
Shimizu Y (1978) Dinoflagellate toxins. In: Scheuer PJ (ed) Marine natural products, vol 1. Academic Press, New York, pp 1-42 10.1016/B978-0-12-624001-6.50006-0
73
Smith KS, Ferry JG (2000) Prokaryotic carbonic anhydrases. Fems Microbiol Rev 24(4):335-366 10.1111/j.1574-6976.2000.tb00546.x10978542
74
So AK, Meryl JM, George SE (2002) Characterization of a mutant lacking carboxysomal carbonic anhydrase from the cyanobacterium Synechocystis PCC6803. Planta 214(3):456-467 10.1007/s00425010063811859847
75
Stein JL, Felbeck H (1993) Kinetic and physical properties of a recombinant RuBisCO from a chemoautotrophic endosymbiont. Mol Mar Biol Biotechnol 2(5):280-290
76
Strasser RJ, Srivastava A, Tsimilli-Michael M (2000) The fluorescence transient as a tool to characterize and screen photosynthetic samples. In: Yunus M, Pathre U, Mohanty P (eds) Probing photosynthesis: mechanisms, regulation and adaptation, CRC Press, Florida, pp 445-483
77
Stumm W, Morgan JJ (2012) Aquatic chemistry: chemical equilibria and rates in vatural waters. John Wiley & Sons, Toronto, 1040 p
78
Suggett DJ, Warner ME, Leggat W (2017) Symbiotic dinoflagellate functional diversity mediates corals survival under ecological crisis. Trends Ecol Evol 32:735-745 10.1016/j.tree.2017.07.01328843439
79
Supuran CT (2016) Structure and function of carbonic anhydrases. Biochem J 473(14):2023-2032 10.1042/BCJ2016011527407171
80
Tang D, Han W, Li P, Miao X, Zhong J (2011) CO2 biofixation and fatty acid composition of Scenedesmus obliquus and Chlorella pyrenoidosa in response to different CO2 levels. Bioresource Technol 102(3):3071-3076 10.1016/j.biortech.2010.10.04721041075
81
Tuteja R (2005) Type I signal peptidase: an overview. Arch Biochem Biophys 441(2):107-111 10.1016/j.abb.2005.07.01316126156
82
Tyler MA, Seliger HH (1981) Selection for a red tide organism: physiological responses to the physical environment 1, 2. Limnol Oceanogr 26(2):310-324 10.4319/lo.1981.26.2.0310
83
van Roosmalen ML, Geukens N, Jongbloed JD, Tjalsma H, Dubois JY, Bron S, van Dijl JM, Anné J (2004) Type I signal peptidases of Gram-positive bacteria. Biochim Biophys Acta 1694(1-3):279-297 10.1016/j.bbamcr.2004.05.00615546672
84
von Heijne G (1990) The signal peptide. J Membr Biol 115(3):195-201 10.1007/BF018686352197415
85
Wang H, Guo R, Ki JS (2018) 6.0 K microarray reveals differential transcriptomic responses in the dinoflagellate Prorocentrum minimum exposed to polychlorinated biphenyl (PCB). Chemosphere 195:398-409 10.1016/j.chemosphere.2017.12.06629274579
86
Wang X, Wang M, Jia Z, Qiu L, Wang L, Zhang A, Song L (2017) A Carbonic anhydrase serves as an important acid-base regulator in Pacific oyster Crassostrea gigas exposed to elevated CO2: implication for physiological responses of mollusk to ocean acidification. J Mar Biotechnol 19(1):22-35 10.1007/s10126-017-9734-z28204970
87
Widdicombe S, Blackford JC, Spicer JI (2013) Assessing the environmental consequences of CO2 leakage from geological CCS: generating evidence to support environmental risk assessment. Mar Pollut Bull 73(2):399-401 10.1016/j.marpolbul.2013.05.04423809332
88
Xu Y, Feng L, Jeffrey PD, Shi Y, Morel FM (2008) Structure and metal exchange in the cadmium carbonic anhydrase of marine diatoms. Nature 452(7183):56-61 10.1038/nature0663618322527
89
Yamano T, Fukuzawa H (2009) Carbon-concentrating mechanism in a green alga, Chlamydomonas reinhardtii, revealed by transcriptome analyses. J Basic Microbiol 49(1):42-51 10.1002/jobm.20080035219253331
Information
  • Publisher :Korea Institute of Ocean Science and Technology
  • Publisher(Ko) :한국해양과학기술원
  • Journal Title :Ocean and Polar Research
  • Journal Title(Ko) :Ocean and Polar Research
  • Volume : 44
  • No :3
  • Pages :209-220
  • Received Date : 2021-11-16
  • Revised Date : 2021-12-03
  • Accepted Date : 2021-12-07
  • DOI :https://doi.org/10.4217/OPR.2022015
Journal Informaiton Ocean and Polar Research Ocean and Polar Research
Online Submission
Archives
: 2019 ~ 이전
  • scopus_OPR
  • NRF
  • KISTI Current Status
  • KISTI Cited-by
  • KCI 문헌 유사도 검사
  • orcid
  • open access
  • ccl
Journal Informaiton Journal Informaiton - close