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Impact of long-term cropping of glyphosate-resistant transgenic soybean [Glycine max (L.) Merr.] on soil microbiome

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Abstract

The transgenic soybean [Glycine max (L.) Merrill] occupies about 80 % of the global area cropped with this legume, the majority comprising the glyphosate-resistant trait (Roundup Ready®, GR or RR). However, concerns about possible impacts of transgenic crops on soil microbial communities are often raised. We investigated soil chemical, physical and microbiological properties, and grain yields in long-term field trials involving conventional and nearly isogenic RR transgenic genotypes. The trials were performed at two locations in Brazil, with different edaphoclimatic conditions. Large differences in physical, chemical and classic microbiological parameters (microbial biomass of C and N, basal respiration), as well as in grain production were observed between the sites. Some phyla (Proteobacteria, Actinobacteria, Acidobacteria), classes (Alphaproteobacteria, Actinomycetales, Solibacteres) and orders (Rhizobiales, Burkholderiales, Myxococcales, Pseudomonadales), as well as some functional subsystems (clustering-based subsystems, carbohydrates, amino acids and protein metabolism) were, in general, abundant in all treatments. However, bioindicators related to superior soil fertility and physical properties at Londrina were identified, among them a higher ratio of Proteobacteria:Acidobacteria. Regarding the transgene, the metagenomics showed differences in microbial taxonomic and functional abundances, but lower in magnitude than differences observed between the sites. Besides the site-specific differences, Proteobacteria, Firmicutes and Chlorophyta were higher in the transgenic treatment, as well as sequences related to protein metabolism, cell division and cycle. Although confirming effects of the transgenic trait on soil microbiome, no differences were recorded in grain yields, probably due to the buffering capacity associated with the high taxonomic and functional microbial diversity observed in all treatments.

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References

  • Anderson TH, Domsch KH (1978) A physiological method for the quantitative measurement of microbial biomass in soils. Soil Biol Biochem 10:215–221

    Article  CAS  Google Scholar 

  • Babujia LC, Hungria M, Franchini JC, Brookes PC (2010) Microbial biomass and activity at various soil depths in a Brazilian oxisol after two decades of no-tillage and conventional tillage. Soil Biol Biochem 42:2174–2181

    Article  CAS  Google Scholar 

  • Babujia LC, Silva AP, Nogueira MA, Hungria M (2014) Microbial diversity in an oxisol under no-tillage and conventional tillage in southern Brazil. Rev Ciênc Agron 45:863–870

    Article  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc 57:289–300

    Google Scholar 

  • Blake GR, Hartge KH (1986) Particle density. In: Klute C (ed) Methods of soil analysis: part 1, physical and mineralogical methods, 2nd edn. ASA/SSSAJ, Madison, pp 377–382

    Google Scholar 

  • Brandão-Junior O, Hungria M, Franchini JC, Espindola CR (2008) Comparação ente os métodos de fumigação-extração e fumigação-incubação para determinação do carbono da biomassa microbiana em um latossolo. Rev Bras Ci Solo 32:1911–1919

    Article  Google Scholar 

  • Breitbart M, Rohwer F (2005) Here a virus, there a virus, everywhere the same virus? Trends Microbiol 13:278–284

    Article  CAS  PubMed  Google Scholar 

  • Brookes PC, Landman A, Pruden G, Jenkinson DS (1985) Chloroform fumigation and the release of soil nitrogen: a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol Biochem 17:837–842

    Article  CAS  Google Scholar 

  • Carpenter JE (2010) Peer-reviewed surveys indicate positive impact of commercialized GM crops. Nat Biotechnol 28:319–321

    Article  CAS  PubMed  Google Scholar 

  • Chaparro JM, Sheflin AM, Manter DK, Vivanco JM (2012) Manipulating the soil microbiome to increase soil health and plant fertility. Biol Fertil Soils 48:489–499

    Article  Google Scholar 

  • Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Austral Ecol 18:117–143

    Article  Google Scholar 

  • Coenye T, Vandamme P (2003) Diversity and significance of Burkholderia species occupying diverse ecological niches. Environ Microbiol 5:719–729

    Article  CAS  PubMed  Google Scholar 

  • Delmont TO, Prestat E, Keegan KP, Faubladier M, Robe P, Clark IM (2012) Structure, fluctuation and magnitude of a natural grassland soil metagenome. ISME J 6:1677–1687

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dong L, Meng Y, Wang J (2015) Effects of planting transgenic Bt + CpTI cotton on rhizosphere denitrifier abundance and diversity. Wei Sheng Wu Xue Bao 55:358–365

    PubMed  Google Scholar 

  • Dunfield KE, Germida JJ (2004) Impact of genetically modified crops on soil- and plant-associated microbial communities. J Environ Qual 33:806–815

    Article  CAS  PubMed  Google Scholar 

  • EMBRAPA (Empresa Brasileira de Pesquisa Agropecuária) (2009) Manual de análises químicas de solos, plantas e fertilizantes. Embrapa Informação Tecnológica/Embrapa Solos, Brasília

    Google Scholar 

  • Estrada-De Los Santos P, Bustillos-Cristales RO, Caballero-Mellado J (2001) Burkholderia, a genus rich in plant-associated nitrogen fixers with wide environmental and geographic distribution. Appl Environ Microbiol 67:2790–2798

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feigl BJ, Sparling GP, Ross DJ, Cerri CC (1995) Soil microbial biomass in Amazonian soils: evaluation of methods and estimates of pool size. Soil Biol Biochem 27:1467–1472

    Article  CAS  Google Scholar 

  • Feije F, Anger V (1972) Spot tests in inorganic analysis. Elsevier, Amsterdan

    Google Scholar 

  • Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci USA 103:626–631

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fierer N, Leff JW, Adams BJ, Nielsen UN, Bates ST, Lauber CL (2012) Cross-biome metagenomic analyses of soil microbial communities and their functional attributes. Proc Natl Acad Sci USA 109:21390–21395

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fisher WD (1958) On grouping for maximum homogeneity. J Am Stat Assoc 53:789–798

    Article  Google Scholar 

  • Gomez-Alvarez V, Teal TK, Schmidt TM (2009) Systematic artifacts in metagenomes from complex microbial communities. ISME J 3:1314–1317

    Article  PubMed  Google Scholar 

  • Gyaneshwar P, Hirsch AM, Moulin L, Chen WM, Elliott GN, Bontemps C (2011) Legume-nodulating betaproteobacteria: diversity, host range, and future prospects. Mol Plant Microbe Interact 24:1276–1288

    Article  CAS  PubMed  Google Scholar 

  • Hungria M, Mendes IC (2015) Nitrogen fixation with soybean: the perfect symbiosis? In: de Brujin F (ed) Biological nitrogen fixation. Wiley, New Jersey, pp 1005–1019

    Google Scholar 

  • Hungria M, Franchini JC, Campo RJ, Crispino CC, Moraes JZ, Sibaldelli RNR, Mendes IC, Arihara J (2006) Nitrogen nutrition of soybean in Brazil: contributions of biological N2 fixation and of N fertilizer to grain yield. Can J Plant Sci 86:927–939

    Article  Google Scholar 

  • Hungria M, Campo RJ, Mendes IC (2007) A importância do processo de fixação biológica do nitrogênio para a cultura da soja: componente essencial para a competitividade do produto brasileiro. Embrapa Soja, Londrina

    Google Scholar 

  • Hungria M, Franchini JC, Brandão-Junior O, Kaschuk G, Souza RA (2009) Soil microbial activity and crop sustainability in a long-term experiment with three soil-tillage and two crop-rotation systems. Appl Soil Ecol 42:288–296

    Article  Google Scholar 

  • Hungria M, Nogueira MA, Araujo RS (2013) Co-inoculation of soybeans and common beans with rhizobia and azospirilla: strategies to improve sustainability. Biol Fertil Soils 49:791–801

    Article  Google Scholar 

  • Hungria M, Mendes IC, Nakatani AS, Reis-Junior FB, Moraes JZ, Oliveira MC, Fernandes MF (2014) Effects of glyphosate-resistant gene and herbicides on soybean crop: I. Field trials monitoring biological nitrogen fixation and yield. Field Crop Res 158:43–54

    Article  Google Scholar 

  • Hungria M, Nakatani AS, Souza RA, Sei FB, Chueire LM, Arias CA (2015) Impact of the ahas transgene for herbicides resistance on biological nitrogen fixation and yield of soybean. Transgenic Res 24:155–165

    Article  CAS  PubMed  Google Scholar 

  • James C (2014) Global status of commercialized biotech/GM crops. ISAAA, Ithaca

    Google Scholar 

  • Jenkinson DS, Polwson DS (1976) The effect of biocidal treatment on metabolism in soil. V. A method of measuring soil biomass. Soil Biol Biochem 8:209–213

    Article  CAS  Google Scholar 

  • Kakirde KS, Parsley LC, Liles MR (2010) Size does matter: application-driven approaches for soil metagenomics. Soil Biol Biochem 42:1911–1923

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaschuk G, Alberton O, Hungria M (2010) Three decades of soil microbial studies in Brazilian ecosystems: lessons learned about soil quality and indications for improving sustainability. Soil Biol Biochem 42:1–13

    Article  CAS  Google Scholar 

  • Kaschuk G, Alberton O, Hungria M (2011) Quantifying effects of different agricultural land uses on soil microbial biomass and activity in Brazilian biomes: inferences to improve soil quality. Plant Soil 338:467–481

    Article  CAS  Google Scholar 

  • Kersters K, Lisdiyanti P, Komagata K, Swings J (2006) The family Acetobacteraceae: the genera Acetobacter, Acidomonas, Asaia, Gluconacetobacter, Gluconobacter, and Kozakia. In: Falkow S, Rosenberg E, Schleifer H, Stackebrandt E (eds) Prokaryotes, vol 5. Springer, Berlin, pp 163–200

    Chapter  Google Scholar 

  • Kuramae EE, Yergeau E, Wong LC, Pijl AS, van Veen JA, Kowalchuk GA (2012) Soil characteristics more strongly influence soil bacterial communities than land-use type. FEMS Microbiol Ecol 79:12–24

    Article  CAS  PubMed  Google Scholar 

  • Lauber CL, Strickland MS, Bradford MA, Fierer N (2008) The influence of soil properties on the structure of bacterial and fungal communities across land-use types. Soil Biol Biochem 40:2407–2415

    Article  CAS  Google Scholar 

  • Lauber CL, Hamady M, Knight R, Fierer N (2009) Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol 75:5111–5120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lavery TJ, Roudnew B, Seymour J, Mitchell JG, Jeffries T (2012) High nutrient transport and cycling potential revealed in the microbial metagenome of Australian sea lion (Neophoca cinerea) faeces. PLoS One 7:e36478

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liles MR, Manske BF, Handelsman J, Goodman RM (2003) A census of rRNA genes and linked genomic sequences within a soil metagenomic library. Appl Environ Microbiol 69:2684–2691

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lladó S, Žifčákpvá L, Vĕtrovský T, Eichlerová I, Baldrian P (2016) Functional screening of abundant bacteria from acidic forest soil indicates the metabolic potential of Acidobacteria subdivision I for polysaccharide decomposition. Biol Fertil Soils 42:251–260

    Article  Google Scholar 

  • Lopes AAC, Souza DMG, Chaer GM, Reis Junior FB, Goedert WJ, Mendes IC (2013) Interpretation of microbial soil indicators as a function of crop yield andorganic carbon. Soil Sci Soc Am J 77:461–472

    Article  CAS  Google Scholar 

  • Ma A, Zhuang X, Wu J, Cui M, Lv D, Liu C, Zhuang G (2013) Ascomycota members dominate fungal communities during straw residue decomposition in arable soil. PLoS One 8:e66146

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Manzoni S, Taylor P, Richter A, Porporato A, Ågren GI (2012) Environmental and stoichiometric controls on microbial carbon-use efficiency in soils. New Phytol 196:79–91

    Article  CAS  PubMed  Google Scholar 

  • McCune B, Mefford MJ (2011) PC-ORD multivariate analysis of ecological data. MJM, Gleneden Beach

    Google Scholar 

  • Meyer F, Parmann D, D’Souza M, Olson R, Glass EM, Kubal M, Paczian T, Rodriguez A, Stevens R, Wilke A, Wilkening H, Edwards RA (2008) The metagenomics RAST server—a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinform 19:386

    Article  Google Scholar 

  • Mulder C, Wouterse M, Raubuch M, Roelofs W, Rutgers M (2006) Can transgenic maize affect soil microbial communities? PLoS Comput Biol 2:1165–1172

    Article  CAS  Google Scholar 

  • Nakatani AS, Fernandes MF, Souza RA, Silva AP, Reis-Junior FB, Mendes IC, Hungria M (2014) Effects of the glyphosate-resistance gene and of herbicides applied to the soybean crop on soil microbial biomass and enzymes. Field Crop Res 162:20–29

    Article  Google Scholar 

  • Nelson DW, Sommers LE (1996) Total carbon, organic carbon, and organic matter. In: Black CA (ed) Methods of soil analysis. Part 3. Chemical methods. ASA/SSSAJ, Madison, pp 961–1010

    Google Scholar 

  • Newcombe RG (1998) Interval estimation for the difference between independent proportions: comparison of eleven methods. Stat Med 17:873–890

    Article  CAS  PubMed  Google Scholar 

  • O’Donnell AG, Gorres H (1999) 16S rDNA methods in soil microbiology. Curr Opin Biotechnol 10:225–229

    Article  PubMed  Google Scholar 

  • OECD/Food and Agriculture Organization of the United Nations (2015) OECD-FAO agricultural outlook 2015. OECD Publishing, Paris. doi:10.1787/agr_outlook-2015-en. Accessed 03 December 2015

  • Oliveira JRA, Mendes IC, Vivaldi L (2001) Carbono da biomassa microbiana em solos de cerrado sob vegetação nativa e sob cultivo: avaliação dos métodos fumigação-incubação e fumigação-extração. Rev Bras Ci Solo 25:863–871

    Article  Google Scholar 

  • Osborne CA, Zwart AB, Broadhurst LM, Young AG, Richardson AE (2011) The influence of sampling strategies and spatial variation on the detected soil bacterial communities under three different land-use types. FEMS Microbiol Ecol 78:70–79

    Article  CAS  PubMed  Google Scholar 

  • Overbeek R, Begley T, Butler RM, Choudhuri JV, Chuang HY, Cohoon M, de Crecy-Lagard V, Diaz N, Disz T, Edwards R et al (2005) The subsystems approach to genome annotation and its use in the project to annotate 1000 genomes. Nucleic Acids Res 33:5691–5702

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parks DH, Beiko RG (2010) Identifying biologically relevant differences between metagenomic communities. Bioinformatics 26:715–721

    Article  CAS  PubMed  Google Scholar 

  • Pawlowski J, Holzmann M, Berney C, Fahrni J, Gooday AJ, Cedhagen T, Habura A, Bowser SS (2003) The evolution of early Foraminifera. Proc Natl Acad Sci USA 100:11494–11498

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pylro VS, Roesch LFW, Ortega JM, Amaral AM, Tótola MR, Hirsch PR, Rosado AS, Góes-Neto A, Silva ALC, Rosa CA, Morais DK, Andreote FD, Duarte GF, Melo IS, Seldin L, Lambais MR, Hungria M, Peixoto RS, Kruger RH, Tsai SM, Azevedo VAC (2014) Brazilian microbiome project: revealing the unexplored microbial diversity—challenges and prospects. Microbial Ecol 67:237–241

    Article  Google Scholar 

  • Quaiser A, Ochsenreiter T, Lanz C, Schuster SC, Treusch AH, Eck J, Schleper C (2003) Acidobacteria form a coherent but highly diverse group within the bacterial domain: evidence from environmental genomics. Mol Microbiol 50:563–575

    Article  CAS  PubMed  Google Scholar 

  • Reichenbach H (2003) The Myxococcales. In: Garrity GM (ed) Bergey’s manual of systematic bacteriology, part 3: the alpha-, beta-, delta-, and epsilon-proteobacteria, 2nd edn. Springer, New York, pp 1059–1143

    Google Scholar 

  • Reyes A, Haynes M, Hanson N, Angly FE, Heath AC (2010) Viruses in the faecal microbiota of monozygotic twins and their mothers. Nature 466:334–338

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Silva AP, Franchini JC, Babujia LC, Souza RA, Hungria M (2010) Microbial biomass under different soil and crop managements in short- to long-term experiments performed in Brazil. Field Crop Res 119:20–26

    Article  Google Scholar 

  • Silva AP, Babujia LC, Matsumoto LS, Guimarães MF, Hungria M (2013) Microbial diversity under different soil tillage and crop rotation systems in an oxisol of southern Brazil. TOASJ 7:40–47

    Article  Google Scholar 

  • Silva AP, Babujia LC, Franchini JC, Ralisch R, Hungria M, Guimarães MF (2014) Soil structure and its influence on microbial biomass in different soil and crop management systems. Soil Till Res 142:42–53

    Article  Google Scholar 

  • Smit E, Leeflang P, Gommans S, van den Broek J, van Mil S, Wernars K (2001) Diversity and seasonal fluctuations of the dominant members of the bacterial soil community in a wheat field as determined by cultivation and molecular methods. Appl Environ Microbiol 67:2284–2291

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sokal RR (1979) Testing statistical significance of geographic variation patterns. Syst Zool 28:227–231

    Article  Google Scholar 

  • Souza RA, Babujia LC, Silva AP, Guimarães MF, Arrabal CA, Hungria M (2013a) Impact of the ahas transgene and of herbicides associated with the soybean crop on soil microbial communities. Transgenic Res 22:877–892

    Article  CAS  PubMed  Google Scholar 

  • Souza RC, Cantão ME, Vasconcelos ATR, Nogueira M, Hungria M (2013b) Soil metagenomics reveals differences under conventional and no-tillage with crop rotation or succession. Appl Soil Ecol 72:49–61

    Article  Google Scholar 

  • Souza RC, Hungria M, Cantão ME, Vasconcelos ATR, Nogueira MA, Vicente VA (2014) Metagenomic analysis reveals microbial functional redundancies and specificities in a soil under different tillage and crop-management regimes. Appl Soil Ecol 86:106–112

    Article  Google Scholar 

  • Spang A, Saw JH, Jorgensen SL, Zaremba-Niedzwiedzka K, Martijn J, Lind AE, Eijk JK, Schleper C, Guy L, Ettema TJG (2015) Complex archaea that bridge the gap between prokaryotes and eukaryotes. Nature 521:173–184

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Steven B, Gallegos-Graves LV, Yeager CM, Belnap J, Evans RD, Kuske CR (2012) Dryland biological soil crust cyanobacteria show unexpected decreases in abundance under long-term elevated CO2. Environ Microbiol 14:3247–3258

    Article  CAS  PubMed  Google Scholar 

  • Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707

    Article  CAS  Google Scholar 

  • Vargas MAT, Hungria M (1997) Biologia dos solos dos cerrados. EMBRAPA Cerrados, Planaltina

    Google Scholar 

  • Wang B, Shen H, Yang X, Guo T, Zhang B, Yan W (2013) Effects of chitinase-transgenic (McChit1) tobacco on the rhizospheric microflora and enzyme activities of the purple soil. Plant Soil Environ 59:241–246

    Google Scholar 

  • Wilke A, Harrison T, Wilkening J, Field D, Glass EM, Kyrpides N, Mavrommatis K, Meyer F (2012) The M5nr: a novel non-redundant database containing protein sequences and annotations from multiple sources and associated tools. BMC Bioinform 13:141

    Article  CAS  Google Scholar 

  • Wilke A, Glass E, Bischof J, Braithwaite D, Souza M, Gerlach W (2013) MG-RAST technical report and manual for version 3.3.6–Rev 1. http://www.mcs.anl.gov/papers/ANL/MCS-TM-333_1.pdf. Accessed 03 December 2015

  • Zhalnina K, Dias R, Quadros PD, Davis-Richardson A, Camargo FOA, Clark IM, McGrath SP, Hirsch PR, Triplett EW (2015) Soil pH determines microbial diversity and composition in the park grass experiment. Microb Ecol 69:395–406

    Article  CAS  PubMed  Google Scholar 

  • Zuleta LFG, Cunha CO, Carvalho FM, Almeida LGP, Clapina LP, Souza RC, Mercante FM, Faria SM, Baldani JI, Hungria M, Vasconcelos ATR (2014) The complete genome of the symbiotic nitrogen-fixing Burkholderia phenoliruptrix strain BR3459a: is it possible to delineate the borders between symbiosis and pathogenicity? BMC Genom 15:535

    Article  Google Scholar 

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Acknowledgments

The project was partially financed by Embrapa (02.13.08.003.00.00) and CNPq (National Council for Scientific and Technological Development) (Universal, 470515/2012-0). L. C. Babujia acknowledges a PhD fellowship from CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior), A.P. Silva a pos-doc fellow from CPNq, and A. Nakatani a pos-doc fellow from Fundação Araucária. A. T. R. Vasconcelos, M. A. Nogueira, J. V. Visentainer and M. Hungria are grateful for research fellowships from CNPq. We also thank Dr. Donovan Parks and M.Sc. Santiago Revale for help with the software STAMP and Dr. Allan R. J. Eaglesham for reviewing the manuscript.

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    1. Department of Chemistry, Universidade Estadual de Maringá, Av. Colombo 5790, Maringá, Paraná, 87020-900, Brazil

      Letícia Carlos Babujia & Jesuí Vergilio Visentainer

    2. Embrapa Soja, C.P. 231, Londrina, Paraná, 86001-970, Brazil

      Letícia Carlos Babujia, Adriana Pereira Silva, André Shigueyoshi Nakatani & Mariangela Hungria

    3. Embrapa Suínos e Aves, C.P. 21, Concórdia, Santa Catarina, 89700-000, Brazil

      Mauricio Egidio Cantão

    4. Laboratório Nacional de Computação Científica, Rua Getúlio Vargas 333, Petrópolis, Rio de Janeiro, 25651-071, Brazil

      Ana Tereza Ribeiro Vasconcelos

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    Jesuí Vergilio Visentainer and Mariangela Hungria have equally contributed to this work.

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    Babujia, L.C., Silva, A.P., Nakatani, A.S. et al. Impact of long-term cropping of glyphosate-resistant transgenic soybean [Glycine max (L.) Merr.] on soil microbiome. Transgenic Res 25, 425–440 (2016). https://doi.org/10.1007/s11248-016-9938-4

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