Abstract
Diatoms emerged in the Mesozoic period and presently constitute one of the main primary producers in the world’s ocean and are of a major economic importance. In the current study, using whole genome sequencing of ten accessions of the model diatom Phaeodactylum tricornutum, sampled at broad geospatial and temporal scales, we draw a comprehensive landscape of the genomic diversity within the species. We describe strong genetic subdivisions of the accessions into four genetic clades (A–D) with constituent populations of each clade possessing a conserved genetic and functional makeup, likely a consequence of the limited dispersal of P. tricornutum in the open ocean. We further suggest dominance of asexual reproduction across all the populations, as implied by high linkage disequilibrium. Finally, we show limited yet compelling signatures of genetic and functional convergence inducing changes in the selection pressure on many genes and metabolic pathways. We propose these findings to have significant implications for understanding the genetic structure of diatom populations in nature and provide a framework to assess the genomic underpinnings of their ecological success and impact on aquatic ecosystems where they play a major role. Our work provides valuable resources for functional genomics and for exploiting the biotechnological potential of this model diatom species.
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References
Bowler C, Allen AE, Badger JH, Grimwood J, Jabbari K, Kuo A, et al. The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature. 2008;456:239–44.
Moustafa A, Beszteri B, Maier UG, Bowler C, Valentin K, Bhattacharya D. Genomic footprints of a cryptic plastid endosymbiosis in diatoms. Science. 2009;324:1724–6.
Dorrell RG, Gile G, McCallum G, Meheust R, Bapteste EP, Klinger CM, et al. Chimeric origins of ochrophytes and haptophytes revealed through an ancient plastid proteome. Elife. 2017;6:1–45.
C.G. E: Die Infusionsthierchen als vollkommene Organismen. Ein Blick in das tiefere organische Leben der Natur. Leipzig: Leopold Voss; 1838.
Armbrust EV. The life of diatoms in the world’s oceans. Nature. 2009;459:185–92.
Amin SA, Parker MS, Armbrust EV. Interactions between diatoms and bacteria. Microbiol Mol Biol Rev. 2012;76:667–84.
Malviya S, Scalco E, Audic S, Vincent F, Veluchamy A, Poulain J, et al. Insights into global diatom distribution and diversity in the world’s ocean. Proc Natl Acad Sci USA. 2016;133:1516–25.
Allen AE, Dupont CL, Obornik M, Horak A, Nunes-Nesi A, McCrow JP, et al. Evolution and metabolic significance of the urea cycle in photosynthetic diatoms. Nature. 2011;473:203–7.
Huysman MJ, Fortunato AE, Matthijs M, Costa BS, Vanderhaeghen R, Van den Daele H, et al. AUREOCHROME1a-mediated induction of the diatom-specific cyclin dsCYC2 controls the onset of cell division in diatoms (Phaeodactylum tricornutum). Plant Cell. 2013;25:215–28.
Morrissey J, Sutak R, Paz-Yepes J, Tanaka A, Moustafa A, Veluchamy A, et al. A novel protein, ubiquitous in marine phytoplankton, concentrates iron at the cell surface and facilitates uptake. Curr Biol. 2015;25:364–71.
Tanaka T, Maeda Y, Veluchamy A, Tanaka M, Abida H, Marechal E, et al. Oil accumulation by the oleaginous diatom Fistulifera solaris as revealed by the genome and transcriptome. Plant Cell. 2015;27:162–76.
Fortunato AE, Jaubert M, Enomoto G, Bouly JP, Raniello R, Thaler M, et al. Diatom phytochromes reveal the existence of far-red-light-based sensing in the ocean. Plant Cell. 2016;28:616–28.
Godhe A, Kremp A, Montresor M. Genetic and microscopic evidence for sexual reproduction in the centric diatom Skeletonema marinoi. Protist. 2014;165:401–16.
Moore ER, Bullington BS, Weisberg AJ, Jiang Y, Chang J, Halsey KH. Morphological and transcriptomic evidence for ammonium induction of sexual reproduction in Thalassiosira pseudonana and other centric diatoms. PLoS One. 2017;12:e0181098.
Mouget JL, Gastineau R, Davidovich O, Gaudin P, Davidovich NA. Light is a key factor in triggering sexual reproduction in the pennate diatom Haslea ostrearia. FEMS Microbiol Ecol. 2009;69:194–201.
De Martino A, Meichenin A, Shi J, Pan KH, Bowler C. Genetic and phenotypic characterization of Phaeodactylum tricornutum (Bacillariophyceae) accessions. J Phycol. 2007;43:992–1009.
Stanley MS, Callow JA. Whole cell adhesion strength of morphotypes and isolates of Phaeodactylum tricornutum (Bacillariophyceae). Eur J Phycol. 2007;42:191–7.
Bailleul B, Rogato A, de Martino A, Coesel S, Cardol P, Bowler C, et al. An atypical member of the light-harvesting complex stress-related protein family modulates diatom responses to light. Proc Natl Acad Sci USA. 2010;107:18214–9.
Abida H, Dolch LJ, Mei C, Villanova V, Conte M, Block MA, et al. Membrane glycerolipid remodeling triggered by nitrogen and phosphorus starvation in Phaeodactylum tricornutum. Plant Physiol. 2015;167:118–36.
Taddei L, Stella GR, Rogato A, Bailleul B, Fortunato AE, Annunziata R, et al. Multisignal control of expression of the LHCX protein family in the marine diatom Phaeodactylum tricornutum. J Exp Bot. 2016;67:3939–51.
Tirichine L, Rastogi A, Bowler C. Recent progress in diatom genomics and epigenomics. Curr Opin Plant Biol. 2017;36:46–55.
Falciatore A, Casotti R, Leblanc C, Abrescia C, Bowler C. Transformation of nonselectable reporter genes in marine diatoms. Mar Biotechnol. 1999;1:239–51.
Siaut M, Heijde M, Mangogna M, Montsant A, Coesel S, Allen A, et al. Molecular toolbox for studying diatom biology in Phaeodactylum tricornutum. Gene. 2007;406:23–35.
De Riso V, Raniello R, Maumus F, Rogato A, Bowler C, Falciatore A. Gene silencing in the marine diatom Phaeodactylum tricornutum. Nucleic Acids Res. 2009;37:e96.
Huysman MJ, Martens C, Vandepoele K, Gillard J, Rayko E, Heijde M, et al. Genome-wide analysis of the diatom cell cycle unveils a novel type of cyclins involved in environmental signaling. Genome Biol. 2010;11:R17.
Maheswari U, Jabbari K, Petit JL, Porcel BM, Allen AE, Cadoret JP, et al. Digital expression profiling of novel diatom transcripts provides insight into their biological functions. Genome Biol. 2010;11:R85.
Maheswari U, Mock T, Armbrust EV, Bowler C. Update of the diatom EST database: a new tool for digital transcriptomics. Nucleic Acids Res. 2009;37:D1001–5.
Kaur S, Spillane C. Reduction in carotenoid levels in the marine diatom Phaeodactylum tricornutum by artificial microRNAs targeted against the endogenous phytoene synthase gene. Mar Biotechnol. 2015;17:1–7.
Diner RE, Bielinski VA, Dupont CL, Allen AE, Weyman PD. Refinement of the diatom episome maintenance sequence and improvement of conjugation-based DNA delivery methods. Front Bioeng Biotechnol. 2016;4:65.
Nymark M, Sharma AK, Sparstad T, Bones AM, Winge P. A CRISPR/Cas9system adapted for gene editing in marine algae. Sci Rep. 2016;6:24951.
Rastogi A, Murik O, Bowler C, Tirichine L. PhytoCRISP-Ex: a web-based and stand-alone application to find specific target sequences for CRISPR/CAS editing. BMC Bioinf. 2016;17:261.
Veluchamy A, Lin X, Maumus F, Rivarola M, Bhavsar J, Creasy T, et al: Insights into the role of DNA methylation in diatoms by genome-wide profiling in Phaeodactylum tricornutum. Nat Commun. 2013;4:1–9.
Veluchamy A, Rastogi A, Lin X, Lombard B, Murik O, Thomas Y, et al. An integrative analysis of post-translational histone modifications in the marine diatom Phaeodactylum tricornutum. Genome Biol. 2015;16:102.
Daboussi F, Leduc S, Marechal A, Dubois G, Guyot V, Perez-Michaut C, et al. Genome engineering empowers the diatom Phaeodactylum tricornutum for biotechnology. Nat Commun. 2014;5:3831.
Serif M, Dubois G, Finoux AL, Teste MA, Jallet D, Daboussi F. One-step generation of multiple gene knock-outs in the diatom Phaeodactylum tricornutum by DNA-free genome editing. Nat Commun. 2018;9:3924.
Flowers JM, Hazzouri KM, Pham GM, Rosas U, Bahmani T, Khraiwesh B, et al. Whole-genome resequencing reveals extensive natural variation in the model green alga Chlamydomonas reinhardtii. Plant Cell. 2015;27:2353–69.
Cao J, Schneeberger K, Ossowski S, Gunther T, Bender S, Fitz J, et al. Whole-genome sequencing of multiple Arabidopsis thaliana populations. Nat Genet. 2011;43:956–63.
Liti G, Carter DM, Moses AM, Warringer J, Parts L, James SA, et al. Population genomics of domestic and wild yeasts. Nature. 2009;458:337–41.
Lachance J, Tishkoff SA. Population genomics of human adaptation. Annu Rev Ecol Evol Syst. 2013;44:123–43.
Godhe A, Rynearson T. The role of intraspecific variation in the ecological and evolutionary success of diatoms in changing environments. Philos Trans R Soc Lond B Biol Sci. 2017;372:1–10.
Harnstrom K, Ellegaard M, Andersen TJ, Godhe A. Hundred years of genetic structure in a sediment revived diatom population. Proc Natl Acad Sci USA. 2011;108:4252–7.
Whittaker KA, Rynearson TA. Evidence for environmental and ecological selection in a microbe with no geographic limits to gene flow. Proc Natl Acad Sci USA. 2017;114:2651–6.
Rengefors K, Kremp A, Thorsten BH, Reusch A, Wood M. Genetic diversity and evolution in eukaryotic phytoplankton: revelations from population genetic studies. J Plankton Res. 2017;39:165–79.
Matuszewski S, Hermisson J, Kopp M. Catch me if you can: adaptation from standing genetic variation to a moving phenotypic optimum. Genetics. 2015;200:1255–74.
Bailleul B, Berne N, Murik O, Petroutsos D, Prihoda J, Tanaka A, et al. Energetic coupling between plastids and mitochondria drives CO2 assimilation in diatoms. Nature. 2015;524:366–9.
McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 2010;20:1297–303.
Chen G, Rynearson TA. Genetically distinct populations of a diatom co-exist during the North Atlantic spring bloom. Limnol Oceanogr. 2016;61:2165–79.
Blanc-Mathieu R, Krasovec M, Hebrard M, Yau S, Desgranges E, Martin J, et al. Population genomics of picophytoplankton unveils novel chromosome hypervariability. Sci Adv. 2017;3:e1700239.
Tsai IJ, Bensasson D, Burt A, Koufopanou V. Population genomics of the wild yeast Saccharomyces paradoxus: quantifying the life cycle. Proc Natl Acad Sci USA. 2008;105:4957–62.
Alexander DH, Novembre J, Lange K. Fast model-based estimation of ancestry in unrelated individuals. Genome Res. 2009;19:1655–64.
Piganeau G, Eyre-Walker A, Jancek S, Grimsley N, Moreau H. How and why DNA barcodes underestimate the diversity of microbial eukaryotes. PLoS One. 2011;6:e16342.
de Vargas C, Norris R, Zaninetti L, Gibb SW, Pawlowski J. Molecular evidence of cryptic speciation in planktonic foraminifers and their relation to oceanic provinces. Proc Natl Acad Sci USA. 1999;96:2864–8.
Saez AG, Probert I, Geisen M, Quinn P, Young JR, Medlin LK. Pseudo-cryptic speciation in coccolithophores. Proc Natl Acad Sci USA. 2003;100:7163–8.
Wolf M, Chen S, Song J, Ankenbrand M, Muller T. Compensatory base changes in ITS2 secondary structures correlate with the biological species concept despite intragenomic variability in ITS2 sequences—a proof of concept. PLoS One. 2013;8:e66726.
Kaczmarska I, Mather L, Luddington I, Muise F, Ehrman J. Cryptic diversity in a cosmopolitan diatom known as Asterionellopsis glacialis (Fragilariaceae): implications for ecology, biogeography, and taxonomy. Am J Bot. 2014;101:267–86.
Amato A, Kooistra WH, Ghiron JH, Mann DG, Proschold T, Montresor M. Reproductive isolation among sympatric cryptic species in marine diatoms. Protist. 2007;158:193–207.
Medlin LK. A timescale for diatom evolution based on four molecular markers: reassessment of ghost lineages and major steps defining diatom evolution. Vie Milieu/Life Environ. 2015;65:219–38.
Bitarello BD, de Filippo C, Teixeira JC, Schmidt JM, Kleinert P, Meyer D, et al. Signatures of long-term balancing selection in human genomes. Genome Biol Evol. 2018;10:939–55.
Rastogi A, Maheswari U, Dorrell RG, Vieira FRJ, Maumus F, Kustka A, et al. Integrative analysis of large scale transcriptome data draws a comprehensive landscape of Phaeodactylum tricornutum genome and evolutionary origin of diatoms. Sci Rep. 2018;8:4834.
Lescot M, Hingamp P, Kojima KK, Villar E, Romac S, Veluchamy A, et al. Reverse transcriptase genes are highly abundant and transcriptionally active in marine plankton assemblages. ISME J. 2016;10:1134–46.
Gu Z, Steinmetz LM, Gu X, Scharfe C, Davis RW, Li WH. Role of duplicate genes in genetic robustness against null mutations. Nature. 2003;421:63–6.
Ogura T, Wilkinson AJ. AAA+ superfamily ATPases: common structure—diverse function. Genes Cells. 2001;6:575–97.
Zeytuni N, Zarivach R. Structural and functional discussion of the tetra-trico-peptide repeat, a protein interaction module. Structure. 2012;20:397–405.
Helliwell KE, Wheeler GL, Leptos KC, Goldstein RE, Smith AG. Insights into the evolution of vitamin B12 auxotrophy from sequenced algal genomes. Mol Biol Evol. 2011;28:2921–33.
Bertrand EM, Allen AE, Dupont CL, Norden-Krichmar TM, Bai J, Valas RE, et al. Influence of cobalamin scarcity on diatom molecular physiology and identification of a cobalamin acquisition protein. Proc Natl Acad Sci USA. 2012;109:E1762–71.
Helliwell KE, Collins S, Kazamia E, Purton S, Wheeler GL, Smith AG. Fundamental shift in vitamin B12 eco-physiology of a model alga demonstrated by experimental evolution. ISME J. 2015;9:1446–55.
Quadrana L, Bortolini Silveira A, Mayhew GF, LeBlanc C, Martienssen RA, Jeddeloh JA, et al. the Arabidopsis thaliana mobilome and its impact at the species level. Elife. 2016;5:1–25.
Bonchev G, Parisod C. Transposable elements and microevolutionary changes in natural populations. Mol Ecol Resour. 2013;13:765–75.
Thiel MaG L. The ecology of rafting in the marine environment. II. The rafting organisms and community. Oceanogr Mar Biol: Annu Rev. 2005;43:279–418.
Nikula R, Spencer HG, Waters JM. Passive rafting is a powerful driver of transoceanic gene flow. Biol Lett. 2013;9:20120821.
Schlichting HE. The rôle of waterfowl in the dispersal of algae. Trans Am Microsc Soc. 1960;79:160–6.
Proctor VW. Dispersal of desmids by birds. Phycologia. 1966;5:227–32.
Foissner W. Biogeography and dispersal of micro-organisms: a review emphasizing protists. Acta Protozool. 2006;45:111–36.
Liti G. The fascinating and secret wild life of the budding yeast S. cerevisiae. Elife. 2015;4:1–9.
Blanc-Mathieu R, Verhelst B, Derelle E, Rombauts S, Bouget FY, Carre I, et al. An improved genome of the model marine alga Ostreococcus tauri unfolds by assessing Illumina de novo assemblies. BMC Genom. 2014;15:1103.
Hirakawa MP, Martinez DA, Sakthikumar S, Anderson MZ, Berlin A, Gujja S, et al. Genetic and phenotypic intra-species variation in Candida albicans. Genome Res. 2015;25:413–25.
Filatov DA. Extreme lewontin’s paradox in ubiquitous marine phytoplankton species. Mol Biol Evol. 2019;36:4–14.
Mock T, Otillar RP, Strauss J, McMullan M, Paajanen P, Schmutz J, et al. Evolutionary genomics of the cold-adapted diatom Fragilariopsis cylindrus. Nature. 2017;541:536–40.
Read BA, Kegel J, Klute MJ, Kuo A, Lefebvre SC, Maumus F, et al. Pan genome of the phytoplankton Emiliania underpins its global distribution. Nature. 2013;499:209–13.
Koester JA, Berthiaume CT, Hiranuma N, Parker MS, Iverson V, Morales R, et al. Sexual ancestors generated an obligate asexual and globally dispersed clone within the model diatom species Thalassiosira pseudonana. Sci Rep. 2018;8:10492.
Patil S, Moeys S, von Dassow P, Huysman MJ, Mapleson D, De Veylder L, et al. Identification of the meiotic toolkit in diatoms and exploration of meiosis-specific SPO11 and RAD51 homologs in the sexual species Pseudo-nitzschia multistriata and Seminavis robusta. BMC Genomics. 2015;16:930.
Allen DE, Lynch M. The effect of variable frequency of sexual reproduction on the genetic structure of natural populations of a cyclical parthenogen. Evolution. 2012;66:919–26.
Becker C, Hagmann J, Muller J, Koenig D, Stegle O, Borgwardt K, et al. Spontaneous epigenetic variation in the Arabidopsis thaliana methylome. Nature. 2011;480:245–9.
Rahbari R, Wuster A, Lindsay SJ, Hardwick RJ, Alexandrov LB, Al Turki S, et al. Timing, rates and spectra of human germline mutation. Nat Genet. 2016;48:126–33.
Shoemaker R, Deng J, Wang W, Zhang K. Allele-specific methylation is prevalent and is contributed by CpG-SNPs in the human genome. Genome Res. 2010;20:883–9.
Huff JT, Zilberman D. Dnmt1-independent CG methylation contributes to nucleosome positioning in diverse eukaryotes. Cell. 2014;156:1286–97.
Kanai Y, Ushijima S, Tsuda H, Sakamoto M, Hirohashi S. Aberrant DNA methylation precedes loss of heterozygosity on chromosome 16 in chronic hepatitis and liver cirrhosis. Cancer Lett. 2000;148:73–80.
Clark DP, Flynn KJ, Ownes NJ. The large capacity for dark nitrate-assimilation in diatoms may overcome nitrate limitation of growth. New Phytologist. 2002;155:101–8.
Ivanikova NV, McKay R, Bullerjahn GS. Construction and characterization of a cyanobacterial bioreporter capable of assessing nitrate assimilatory capacity in freshwaters. Limnol Oceanogr. 2005;3:86–93.
Li W, Wang J. Influence of light and nitrate assimilation on the growth strategy in clonal weed Eichhornia crassipes. Aquat Ecol. 2011;45:1–9.
Pickett-Heaps JD, Forer A. Pac-Man does not resolve the enduring problem of anaphase chromosome movement. Protoplasma. 2001;215:16–20.
Doyle JJaJLD. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytoch Bull. 1987;19:11–5.
Nei M, Li WH. Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci USA. 1979;76:5269–73.
Vartanian M, Descles J, Quinet M, Douady S, Lopez PJ. Plasticity and robustness of pattern formation in the model diatom Phaeodactylum tricornutum. New Phytol. 2009;182:429–42.
Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol. 2016;33:1870–4.
Lorenz R, Bernhart SH, Honer Zu Siederdissen C, Tafer H, Flamm C, Stadler PF, et al. ViennaRNA Package 2.0. Algorithms Mol Biol. 2011;6:26.
Seibel PN, Muller T, Dandekar T, Schultz J, Wolf M. 4SALE–a tool for synchronous RNA sequence and secondary structure alignment and editing. BMC Bioinf. 2006;7:498.
Auton A, McVean G. Recombination rate estimation in the presence of hotspots. Genome Res. 2007;17:1219–27.
Etherington GJ, Dicks J, Roberts IN. Recombination Analysis Tool (RAT): a program for the high-throughput detection of recombination. Bioinformatics. 2005;21:278–81.
Weir BS, Cockerham CC. Estimating F-statistics for the analysis of population structure. Evolution. 1984;38:1358–70.
Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, Bender D, et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet. 2007;81:559–75.
Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA, et al. The variant call format and VCFtools. Bioinformatics. 2011;27:2156–8.
Alexander DH, Lange K. Enhancements to the ADMIXTURE algorithm for individual ancestry estimation. BMC Bioinf. 2011;12:246.
Cingolani P, Platts A, Wang le L, Coon M, Nguyen T, Wang L. et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strainw1118; iso-2; iso-3. Fly. 2012;6:80–92.
Zhang Z, Li J, Zhao XQ, Wang J, Wong GK, Yu J. KaKs_Calculator: calculating Ka and Ks through model selection and model averaging. Genomics Proteom Bioinform. 2006;4:259–63.
Cheong WH, Tan YC, Yap SJ, Ng KP. ClicO FS: an interactive web-based service of Circos. Bioinformatics. 2015;31:3685–7.
Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003;13:2498–504.
Robinson JT, Thorvaldsdottir H, Winckler W, Guttman M, Lander ES, Getz G, et al. Integrative genomics viewer. Nat Biotechnol. 2011;29:24–6.
Acknowledgements
HH acknowledges support from National Natural Science Foundation of China (grant no. 91751117). GW acknowledges the Strategic Priority Research Program of the Chinese Academy of Sciences (grant no. XDA17010502). CB acknowledges funding from the ERC Advanced Award ‘Diatomite’, the LouisD Foundation of the Institut de France, the Gordon and Betty Moore Foundation, and the French Government ‘Investissements d’Avenir’ programs MEMO LIFE (ANR-10-LABX-54), PSL* Research University (ANR-1253 11-IDEX-0001-02), and OCEANOMICS (ANR-11-BTBR-0008). CB also thanks the Radcliffe Institute of Advanced Study at Harvard University for a scholar’s fellowship during the 2016–2017 academic year. LT acknowledges funds from the CNRS, MEMO LIFE (ANR-10-LABX-54) and the region of Pays de la Loire (ConnecTalent EPIALG project). AR was supported by an International PhD fellowship from MEMO LIFE (ANR-10-LABX-54).
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LT, HH, and CB conceived the study. LT, AR, and GP designed the study. GW, PV, AFDC, CC and LT did the experiments. AR, FRJV, AV, and GP developed and performed the bioinformatics analysis. AR, GP, FRJV, and LT interpreted the results. AR and LT wrote the paper with input from all the authors. LT supervised the study. LT, CB, HH and GP coordinated the study.
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Rastogi, A., Vieira, F.R.J., Deton-Cabanillas, AF. et al. A genomics approach reveals the global genetic polymorphism, structure, and functional diversity of ten accessions of the marine model diatom Phaeodactylum tricornutum. ISME J 14, 347–363 (2020). https://doi.org/10.1038/s41396-019-0528-3
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DOI: https://doi.org/10.1038/s41396-019-0528-3
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