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中国生物工程杂志

China Biotechnology
China Biotechnology  2022, Vol. 42 Issue (4): 93-101    DOI: 10.13523/j.cb.2110013
    
A Review on Structure and Functions of TonB-dependent Receptors in Gram-negative Bacteria
WANG Ya-ling1,2,3,CHENG An-chun1,2,3,LIU Ma-feng1,2,3,**()
1 Institute of Preventive Veterinary Medicine, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, China
2 Avian Disease Research Center, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, China
3 Key Laboratory of Animal Disease and Human Health of Sichuan Province, Chengdu 611130, China
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Abstract  

Bacteria need to absorb a variety of nutrients from the outer environments for their survival and replication. The small molecules less than 600 Da can freely pass the outer membrane of the gram-negative bacteria. However, for the transportation of the large size of nutrients, the TonB-dependent receptors of gram-negative bacteria are required. TonB-dependent receptors have been found to be present in all the sequenced gram-negative bacteria, but the number of TonB dependent receptors and their functions are various in different bacteria. It has been shown that TonB-dependent receptors were not only involved in the transportation of many different nutrients, such as iron, heme, manganese, zinc, vitamin, and carbohydrate, but also the secretion of protease. This review provided detailed information about the functions and structure of TonB-dependent receptors from different gram-negative bacteria. It will be helpful for the further understanding of the new functions of TonB-dependent receptors.



Key wordsGram-negative bacteria      TonB-dependent receptor      Function     
Received: 13 October 2021      Published: 05 May 2022
ZTFLH:  Q819  
Corresponding Authors: Ma-feng LIU     E-mail: liumafengra@163.com
Cite this article:

WANG Ya-ling,CHENG An-chun,LIU Ma-feng. A Review on Structure and Functions of TonB-dependent Receptors in Gram-negative Bacteria. China Biotechnology, 2022, 42(4): 93-101.

URL:

https://manu60.magtech.com.cn/biotech/10.13523/j.cb.2110013     OR     https://manu60.magtech.com.cn/biotech/Y2022/V42/I4/93

Organism(s) Name Substrate Function PDB ID Reference
Escherichia coli FhuA Iron Transport Fe3+ 1BY3 [53]
FepA Iron Transport Fe3+ 1FEP [54]
FecA Iron Transport Fe3+ 1KMO [55]
BtuB Vitamin B12 Transport Vitamin B12 1NQE [56]
Cir 2HDF [57]
Fiu Iron Transport Fe3+ 6BPM [58]
YddB Ferredoxin Transport Ferredoxin 6OFR [59]
YncD 6V81 [60]
Pseudomonas aeruginosa FptA Iron Transport Fe3+ 1XKW [61]
FpvA Iron Transport Fe3+ 2W75 [62]
PirA Siderophore-drug Transport siderophore-drug molecules 5FP2 [63]
PiuA Siderophore-drug Transport siderophore-drug molecules 5FOK [63]
PiuD Siderophore-drug Transport siderophore-drug molecules 5NEC [64]
PfeA Iron Transport Fe3+ 5M9B [65]
OprC Copper Transport Copper 6FOK
FoxA Iron Transport Fe3+ 6I98 [66]
Yersinia pestis FyuA Iron Transport Fe3+ 4EPA [67]
Neisseria TbpA Transferrin Transport Fe3+ 3V89 [68]
FrpB Iron Transport Fe3+ 4B7O [69]
ZnuD Zinc Transport zinc 4RVW [70]
Pectobacterium carotovorum FusA Ferredoxin Transport Ferredoxin 4ZGV [71]
Serratia marcescens HasR Heme Transport heme 3CSN [26]
Porphyromonas gingivalis RagA oligopeptide Transport oligopeptide 6SLI [72]
Bacteroides polymorpha SusC Starch Transport oligosaccharide 5T3R [73]
Shigella dysenteriae ShuA Heme Transport heme 3FHH [74]
Table 1 Summary of all known TonB-dependent transporter crystal structures in the Gram-negative bacteria
Fig.1 Structure of TonB-dependent receptor FepA (PDB ID:1FEP) (a),(b) A conversed β-barrel domain at C-terminus (blue) and a plug domain at N-terminus (red) of TonB-dependent receptor (c) Top of TonB-dependent receptor
[1]   Schalk I J, Mislin G L A, Brillet K. Structure, function and binding selectivity and stereoselectivity of siderophore-iron outer membrane transporters. Current Topics in Membranes, 2012, 69: 37-66.
[2]   Zeng X M, Xu F Z, Lin J. Specific TonB-ExbB-ExbD energy transduction systems required for ferric enterobactin acquisition in Campylobacter. FEMS Microbiology Letters, 2013, 347(1): 83-91.
doi: 10.1111/1574-6968.12221
[3]   Gómez-Santos N, Glatter T, Koebnik R, et al. A TonB-dependent transporter is required for secretion of protease PopC across the bacterial outer membrane. Nature Communications, 2019, 10: 1360.
doi: 10.1038/s41467-019-09366-9 pmid: 30911012
[4]   Palmer L D, Skaar E P. Transition metals and virulence in bacteria. Annual Review of Genetics, 2016, 50: 67-91.
doi: 10.1146/annurev-genet-120215-035146
[5]   Klebba P E, Newton S M C, Six D A, et al. Iron acquisition systems of gram-negative bacterial pathogens define TonB-dependent pathways to novel antibiotics. Chemical Reviews, 2021, 121(9): 5193-5239.
doi: 10.1021/acs.chemrev.0c01005
[6]   Khan A, Singh P, Srivastava A. Synthesis, nature and utility of universal iron chelator - siderophore: a review. Microbiological Research, 2018, 212-213: 103-111.
doi: 10.1016/j.micres.2017.10.012
[7]   Majumdar A, Trinh V, Moore K J, et al. Conformational rearrangements in the N-domain of Escherichia coli FepA during ferric enterobactin transport. The Journal of Biological Chemistry, 2020, 295(15): 4974-4984.
doi: 10.1074/jbc.RA119.011850
[8]   Wang Y J, Chen X B, Hu Y M, et al. Evolution and sequence diversity of FhuA in Salmonella and Escherichia. Infection and Immunity, 2018, 86(11): e00573-e00518.
[9]   Carson S D, Klebba P E, Newton S M, et al. Ferric enterobactin binding and utilization by Neisseria gonorrhoeae. Journal of Bacteriology, 1999, 181(9): 2895-2901.
pmid: 10217784
[10]   Bouvier B, Cézard C. Impact of iron coordination isomerism on pyoverdine recognition by the FpvA membrane transporter of Pseudomonas aeruginosa. Physical Chemistry Chemical Physics: PCCP, 2017, 19(43): 29498-29507.
doi: 10.1039/C7CP04529H
[11]   Lan P, Yan R S, Lu Y, et al. Genetic diversity of siderophores and hypermucoviscosity phenotype in Klebsiella pneumoniae. Microbial Pathogenesis, 2021, 158: 105014.
doi: 10.1016/j.micpath.2021.105014
[12]   Rakin A, Schneider L, Podladchikova O. Hunger for iron: the alternative siderophore iron scavenging systems in highly virulent Yersinia. Frontiers in Cellular and Infection Microbiology, 2012, 2: 151.
[13]   Cornelissen C N, Hollander A. TonB-dependent transporters expressed by Neisseria gonorrhoeae. Frontiers in Microbiology, 2011, 2: 117.
doi: 10.3389/fmicb.2011.00117 pmid: 21747812
[14]   Noinaj N, Buchanan S K, Cornelissen C N. The transferrin-iron import system from pathogenic Neisseria species. Molecular Microbiology, 2012, 86(2): 246-257.
doi: 10.1111/mmi.12002
[15]   Ostberg K L, DeRocco A J, Mistry S D, et al. Conserved regions of gonococcal TbpB are critical for surface exposure and transferrin iron utilization. Infection and Immunity, 2013, 81(9): 3442-3450.
doi: 10.1128/IAI.00280-13 pmid: 23836816
[16]   DeRocco A J, Yost-Daljev M K, Kenney C D, et al. Kinetic analysis of ligand interaction with the gonococcal transferrin-iron acquisition system. BioMetals, 2009, 22(3): 439-451.
doi: 10.1007/s10534-008-9179-y pmid: 19048191
[17]   Brooks C L, Arutyunova E, Lemieux M J. The structure of lactoferrin-binding protein B from Neisseria meningitidis suggests roles in iron acquisition and neutralization of host defences. Acta Crystallographica Section F, Structural Biology Communications, 2014, 70(Pt 10): 1312-1317.
doi: 10.1107/S2053230X14019372
[18]   Cash D R, Noinaj N, Buchanan S K, et al. Beyond the crystal structure: insight into the function and vaccine potential of TbpA expressed by Neisseria gonorrhoeae. Infection and Immunity, 2015, 83(11): 4438-4449.
doi: 10.1128/IAI.00762-15
[19]   Farahani M F, Esmaelizad M, Jabbari A R. Investigation of iron uptake and virulence gene factors (fur, tonB, exbD, exbB, hgbA, hgbB1, hgbB2 and tbpA) among isolates of Pasteurella multocida from Iran. Iranian Journal of Microbiology, 2019, 11(3): 191-197.
[20]   Pogoutse A K, Moraes T F. Iron acquisition through the bacterial transferrin receptor. Critical Reviews in Biochemistry and Molecular Biology, 2017, 52(3): 314-326.
doi: 10.1080/10409238.2017.1293606
[21]   Manfredi P, Lauber F, Renzi F, et al. New iron acquisition system in Bacteroidetes. Infection and Immunity, 2015, 83(1): 300-310.
doi: 10.1128/IAI.02042-14 pmid: 25368114
[22]   Liu M F, Huang M, Zhu D K, et al. Identifying the genes responsible for iron-limited condition in Riemerella anatipestifer CH-1 through RNA-seq-based analysis. BioMed Research International, 2017, 2017: 8682057.
[23]   Mosbahi K, Wojnowska M, Albalat A, et al. Bacterial iron acquisition mediated by outer membrane translocation and cleavage of a host protein. Proceedings of the National Academy of Sciences of the United States of America, 2018, 115(26): 6840-6845.
[24]   Huang W L, Wilks A. Extracellular heme uptake and the challenge of bacterial cell membranes. Annual Review of Biochemistry, 2017, 86: 799-823.
doi: 10.1146/annurev-biochem-060815-014214
[25]   Wandersman C, Delepelaire P. Haemophore functions revisited. Molecular Microbiology, 2012, 85(4): 618-631.
doi: 10.1111/j.1365-2958.2012.08136.x pmid: 22715905
[26]   Krieg S, Huché F, Diederichs K, et al. Heme uptake across the outer membrane as revealed by crystal structures of the receptor-hemophore complex. Proceedings of the National Academy of Sciences of the United States of America, 2009, 106(4): 1045-1050.
[27]   Zambolin S, Clantin B, Chami M, et al. Structural basis for haem piracy from host haemopexin by Haemophilus influenzae. Nature Communications, 2016, 7: 11590.
doi: 10.1038/ncomms11590 pmid: 27188378
[28]   Smalley J W, Byrne D P, Birss A J, et al. HmuY haemophore and gingipain proteases constitute a unique syntrophic system of haem acquisition by Porphyromonas gingivalis. PLoS One, 2011, 6(2): e17182.
doi: 10.1371/journal.pone.0017182
[29]   Liu M F, Liu S Q, Huang M, et al. An exposed outer membrane hemin-binding protein facilitates hemin transport by a TonB-dependent receptor in Riemerella anatipestifer. Applied and Environmental Microbiology, 2021, 87(15): e0036721.
doi: 10.1128/AEM.00367-21
[30]   Mokry D Z, Nadia-Albete A, Johnson M K, et al. Spectroscopic evidence for a 5-coordinate oxygenic ligated high spin ferric heme moiety in the Neisseria meningitidis hemoglobin binding receptor. Biochimica et Biophysica Acta (BBA) - General Subjects, 2014, 1840(10): 3058-3066.
doi: 10.1016/j.bbagen.2014.06.009
[31]   Wong C T, Xu Y, Gupta A, et al. Structural analysis of haemoglobin binding by HpuA from the Neisseriaceae family. Nature Communications, 2015, 6: 10172.
doi: 10.1038/ncomms10172 pmid: 26671256
[32]   Bidmos F A, Chan H, Praekelt U, et al. Investigation into the antigenic properties and contributions to growth in blood of the meningococcal haemoglobin receptors, HpuAB and HmbR. PLoS One, 2015, 10(7): e0133855.
doi: 10.1371/journal.pone.0133855
[33]   Kammerman M T, Bera A, Wu R R, et al. Molecular insight into TdfH-mediated zinc piracy from human calprotectin by Neisseria gonorrhoeae. mBio, 2020, 11(3): e00949-e00920.
[34]   Gaddy J A, Radin J N, Loh J T, et al. The host protein calprotectin modulates the Helicobacter pylori cag type IV secretion system via zinc sequestration. PLoS Pathogens, 2014, 10(10): e1004450.
doi: 10.1371/journal.ppat.1004450
[35]   Maurakis S, Keller K, Maxwell C N, et al. The novel interaction between Neisseria gonorrhoeae TdfJ and human S100A 7 allows gonococci to subvert host zinc restriction. PLoS Pathogens, 2019, 15(8): e1007937.
doi: 10.1371/journal.ppat.1007937
[36]   Si M, Zhao C, Burkinshaw B, et al. Manganese scavenging and oxidative stress response mediated by type VI secretion system in Burkholderia thailandensis. Proceedings of the National Academy of Sciences of the United States of America, 2017, 114(11): E2233-E2242.
[37]   Si M R, Wang Y, Zhang B, et al. The type VI secretion system engages a redox-regulated dual-functional heme transporter for zinc acquisition. Cell Reports, 2017, 20(4): 949-959.
doi: 10.1016/j.celrep.2017.06.081
[38]   Han Y Y, Wang T T, Chen G K, et al. A Pseudomonas aeruginosa type VI secretion system regulated by CueR facilitates copper acquisition. PLoS Pathogens, 2019, 15(12): e1008198.
doi: 10.1371/journal.ppat.1008198
[39]   Gao P, Guo K, Pu Q Q, et al. oprC impairs host defense by increasing the quorum-sensing-mediated virulence of Pseudomonas aeruginosa. Frontiers in Immunology, 2020, 11: 1696.
doi: 10.3389/fimmu.2020.01696
[40]   Gu W Y, Farhan Ul Haque M, Baral B S, et al. A TonB-dependent transporter is responsible for methanobactin uptake by Methylosinus trichosporium OB3b. Applied and Environmental Microbiology, 2016, 82(6): 1917-1923.
doi: 10.1128/AEM.03884-15
[41]   de Reuse H, Vinella D, Cavazza C. Common themes and unique proteins for the uptake and trafficking of nickel, a metal essential for the virulence of Helicobacter pylori. Frontiers in Cellular and Infection Microbiology, 2013, 3: 94.
[42]   Stoof J, Kuipers E J, Vliet A H M. Characterization of NikR-responsive promoters of urease and metal transport genes of Helicobacter mustelae. BioMetals, 2009, 23(1): 145-159.
doi: 10.1007/s10534-009-9275-7
[43]   Nilaweera T D, Nyenhuis D A, Cafiso D S. Structural intermediates observed only in intact Escherichia coli indicate a mechanism for TonB-dependent transport. eLife, 2021, 10: e68548.
doi: 10.7554/eLife.68548
[44]   Balusek C, Gumbart J C. Role of the native outer-membrane environment on the transporter BtuB. Biophysical Journal, 2016, 111(7): 1409-1417.
doi: S0006-3495(16)30755-X pmid: 27705764
[45]   Cramer W A, Sharma O, Zakharov S D. On mechanisms of colicin import: the outer membrane quandary. The Biochemical Journal, 2018, 475(23): 3903-3915.
doi: 10.1042/BCJ20180477
[46]   Ding T, Schloss P D. Dynamics and associations of microbial community types across the human body. Nature, 2014, 509(7500): 357-360.
doi: 10.1038/nature13178
[47]   Bolam D N, van den Berg B. TonB-dependent transport by the gut microbiota: novel aspects of an old problem. Current Opinion in Structural Biology, 2018, 51: 35-43.
doi: 10.1016/j.sbi.2018.03.001
[48]   Pollet R M, Martin L M, Koropatkin N M. TonB-dependent transporters in the Bacteroidetes: unique domain structures and potential functions. Molecular Microbiology, 2021, 115(3): 490-501.
doi: 10.1111/mmi.14683
[49]   Larsbrink J, Rogers T E, Hemsworth G R, et al. A discrete genetic locus confers xyloglucan metabolism in select human gut Bacteroidetes. Nature, 2014, 506 (7489): 498-502.
doi: 10.1038/nature12907
[50]   Ndeh D, Rogowski A, Cartmell A, et al. Complex pectin metabolism by gut bacteria reveals novel catalytic functions. Nature, 2017, 544 (7648): 65-70.
doi: 10.1038/nature21725
[51]   Rolbetzki A, Ammon M, Jakovljevic V, et al. Regulated secretion of a protease activates intercellular signaling during fruiting body formation in M. xanthus. Developmental Cell, 2008, 15(4): 627-634.
doi: 10.1016/j.devcel.2008.08.002 pmid: 18854146
[52]   Ferguson A D, Hofmann E, Coulton J W, et al. Siderophore-mediated iron transport: crystal structure of FhuA with bound lipopolysaccharide. Science, 1998, 282(5397): 2215-2220.
pmid: 9856937
[53]   Locher K P, Rees B, Koebnik R, et al. Transmembrane signaling across the ligand-gated FhuA receptor: crystal structures of free and ferrichrome-bound states reveal allosteric changes. Cell, 1998, 95(6): 771-778.
pmid: 9865695
[54]   Buchanan S K, Smith B S, Venkatramani L, et al. Crystal structure of the outer membrane active transporter FepA from Escherichia coli. Nature Structural Biology, 1999, 6 (1): 56-63.
pmid: 9886293
[55]   Ferguson A D, Chakraborty R, Smith B S, et al. Structural basis of gating by the outer membrane transporter FecA. Science, 2002, 295(5560): 1715-1719.
pmid: 11872840
[56]   Chimento D P, Mohanty A K, Kadner R J, et al. Substrate-induced transmembrane signaling in the cobalamin transporter BtuB. Nature Structural & Molecular Biology, 2003, 10 (5): 394-401.
doi: 10.1038/nsb914
[57]   Buchanan S K, Lukacik P, Grizot S, et al. Structure of colicin I receptor bound to the R-domain of colicin Ia: implications for protein import. The EMBO Journal, 2007, 26(10): 2594-2604.
doi: 10.1038/sj.emboj.7601693
[58]   Grinter R, Lithgow T. The structure of the bacterial iron-catecholate transporter Fiu suggests that it imports substrates via a two-step mechanism. Journal of Biological Chemistry, 2019, 294(51): 19523-19534.
doi: 10.1074/jbc.RA119.011018 pmid: 31712312
[59]   Grinter R, Leung P M, Wijeyewickrema L C, et al. Protease-associated import systems are widespread in Gram-negative bacteria. PLoS Genetics, 2019, 15(10): e1008435.
doi: 10.1371/journal.pgen.1008435
[60]   Grinter R, Lithgow T. The crystal structure of the TonB-dependent transporter YncD reveals a positively charged substrate-binding site. Acta Crystallographica Section D, Structural Biology, 2020, 76(Pt 5): 484-495.
doi: 10.1107/S2059798320004398
[61]   Cobessi D, Celia H, Pattus F. Crystal structure at high resolution of ferric-pyochelin and its membrane receptor FptA from Pseudomonas aeruginosa. Journal of Molecular Biology, 2005, 352(4): 893-904.
pmid: 16139844
[62]   Greenwald J, Nader M, Celia H, et al. FpvA bound to non-cognate pyoverdines: molecular basis of siderophore recognition by an iron transporter. Molecular Microbiology, 2009, 72(5): 1246-1259.
pmid: 19504741
[63]   Moynié L, Luscher A, Rolo D, et al. Structure and function of the PiuA and PirA siderophore-drug receptors from Pseudomonas aeruginosa and Acinetobacter baumannii. Antimicrobial Agents and Chemotherapy, 2017, 61(4): e02531-e02516.
[64]   Luscher A, Moynié L, Auguste P S, et al. TonB-dependent receptor repertoire of Pseudomonas aeruginosa for uptake of siderophore-drug conjugates. Antimicrobial Agents and Chemotherapy, 2018, 62(6): e00097-e00018.
[65]   Moynié L, Milenkovic S, Mislin G L A, et al. The complex of ferric-enterobactin with its transporter from Pseudomonas aeruginosa suggests a two-site model. Nature Communications, 2019, 10: 3673.
doi: 10.1038/s41467-019-11508-y
[66]   Josts I, Veith K, Tidow H. Ternary structure of the outer membrane transporter FoxA with resolved signalling domain provides insights into TonB-mediated siderophore uptake. eLife, 2019, 8: e48528.
doi: 10.7554/eLife.48528
[67]   Lukacik P, Barnard T J, Keller P W, et al. Structural engineering of a phage lysin that targets gram-negative pathogens. Proceedings of the National Academy of Sciences of the United States of America, 2012, 109(25): 9857-9862.
[68]   Noinaj N, Easley N C, Oke M, et al. Structural basis for iron piracy by pathogenic Neisseria. Nature, 2012, 483 (7387): 53-58.
doi: 10.1038/nature10823
[69]   Saleem M, Prince S M, Rigby S E J, et al. Use of a molecular decoy to segregate transport from antigenicity in the FrpB iron transporter from Neisseria meningitidis. PLoS One, 2013, 8(2): e56746.
doi: 10.1371/journal.pone.0056746
[70]   Calmettes C, Ing C, Buckwalter C M, et al. The molecular mechanism of Zinc acquisition by the neisserial outer-membrane transporter ZnuD. Nature Communications, 2015, 6: 7996.
doi: 10.1038/ncomms8996 pmid: 26282243
[71]   Grinter R, Josts I, Mosbahi K, et al. Structure of the bacterial plant-ferredoxin receptor FusA. Nature Communications, 2016, 7: 13308.
doi: 10.1038/ncomms13308 pmid: 27796364
[72]   Madej M, White J B R, Nowakowska Z, et al. Structural and functional insights into oligopeptide acquisition by the RagAB transporter from Porphyromonas gingivalis. Nature Microbiology, 2020, 5 (8): 1016-1025.
doi: 10.1038/s41564-020-0716-y
[73]   Glenwright A J, Pothula K R, Bhamidimarri S P, et al. Structural basis for nutrient acquisition by dominant members of the human gut microbiota. Nature, 2017, 541 (7637): 407-411.
doi: 10.1038/nature20828
[74]   Cobessi D, Meksem A, Brillet K. Structure of the heme/hemoglobin outer membrane receptor ShuA from Shigella dysenteriae: heme binding by an induced fit mechanism. Proteins, 2010, 78(2): 286-294.
doi: 10.1002/prot.22539
[75]   Gresock M G, Postle K. Going outside the TonB box: identification of novel FepA-TonB interactions in vivo. Journal of Bacteriology, 2017, 199(10): e00649-e00616.
[76]   Mills A, Le H T, Duong F. TonB-dependent ligand trapping in the BtuB transporter. Biochimica et Biophysica Acta (BBA) - Biomembranes, 2016, 1858(12): 3105-3112.
doi: 10.1016/j.bbamem.2016.09.019
[77]   Nyenhuis D A, Nilaweera T D, Cafiso D S. Native cell environment constrains loop structure in the Escherichia coli cobalamin transporter BtuB. Biophysical Journal, 2020, 119(8): 1550-1557.
doi: 10.1016/j.bpj.2020.08.034 pmid: 32946767
[78]   Zhang L, Huang L, Huang M, et al. Effect of nutritional determinants and TonB on the natural transformation of Riemerella anatipestifer. Frontiers in Microbiology, 2021, 12: 644868.
doi: 10.3389/fmicb.2021.644868
[79]   Wang M Y, Zhang P Y, Zhu D K, et al. Identification of the ferric iron utilization gene B739_1208 and its role in the virulence of R. anatipestifer CH-1. Veterinary Microbiology, 2017, 201: 162-169.
doi: 10.1016/j.vetmic.2017.01.027
[80]   Liu M F, Huang M, Shui Y, et al. Roles of B739_ 1343 in iron acquisition and pathogenesis in Riemerella anatipestifer C...H-1 and eva...luation of the RA-CH-1ΔB739_1343 mutant as an attenuated vaccine. PLoS One, 2018, 13(5): e0197310.
doi: 10.1371/journal.pone.0197310
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