1887

Abstract

Picocyanobacteria are important primary producers in freshwater; however, there is still a knowledge gap regarding their diversity at the strain level. For this reason, the microbial diversity of four lakes with different trophic states was investigated by sequencing of the 16S rRNA gene using universal primers. The study was performed in selected lakes of the Osterseen Lake District, Germany, from 2012 to 2014 (Lake Schiffhuettensee: eutrophic; Lake Ostersee: meso-oligotrophic; Lake Groebensee: oligotrophic; Lake Lustsee: oligotrophic). It was determined that the bacterial community of each of these lakes was characterized by one or more specific phyla. Within the autotrophic plankton, the picocyanobacterium sp. dominated oligotrophic habitats, whereas eukaryotic algae prevailed in eutrophic lakes. The study focused on the occurrence of cyanobacteria, specifically the genus . Genetic analysis of the 16S rRNA gene revealed an extendend diversity of freshwater . The occurrence of the identified operational taxonomic units of did not correlate with the trophic state of their habitat, suggesting that the current, underestimated diversity of picocyanobacteria deserves increased consideration in assessments of microbial and freshwater biodiversity.

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2016-12-21
2019-12-08
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References

  1. Ansorge W. J.. 2009; Next-generation DNA sequencing techniques. N Biotechnol25:195–203 [CrossRef][PubMed]
    [Google Scholar]
  2. Becker S., Fahrbach M., Böger P., Ernst A.. 2002; Quantitative tracing, by Taq nuclease assays, of a Synechococcus ecotype in a highly diversified natural population. Appl Environ Microbiol68:4486–4494 [CrossRef][PubMed]
    [Google Scholar]
  3. Becker S., Singh A. K., Postius C., Böger P., Ernst A.. 2004; Genetic diversity and distribution of periphytic Synechococcus spp. in biofilms and picoplankton of Lake Constance. FEMS Microbiol Ecol49:181–190 [CrossRef][PubMed]
    [Google Scholar]
  4. Becker S., Richl P., Ernst A.. 2007; Seasonal and habitat-related distribution pattern of Synechococcus genotypes in Lake Constance. FEMS Microbiol Ecol62:64–77 [CrossRef][PubMed]
    [Google Scholar]
  5. Becker S., Sánchez-Baracaldo P., Singh A. K., Hayes P. K.. 2012; Spatio-temporal niche partitioning of closely related picocyanobacteria clades and phycocyanin pigment types in Lake Constance (Germany). FEMS Microbiol Ecol80:488–500 [CrossRef][PubMed]
    [Google Scholar]
  6. Callieri C.. 2008; Picophytoplankton in freshwater ecosystems: the importance of small-sized phototrophs. Freshw Rev1:1–28 [CrossRef]
    [Google Scholar]
  7. Callieri C., Stockner J.. 2000; Picocyanobacteria success in oligotrophic lakes: fact or fiction?. J Limnol59:72–76 [CrossRef]
    [Google Scholar]
  8. Callieri C., Stockner J. G.. 2002; Freshwater autotrophic picoplankton: a review. J Limnol61:1–14 [CrossRef]
    [Google Scholar]
  9. Callieri C., Caravati E., Corno G., Bertoni R.. 2012; Picocyanobacterial community structure and space-time dynamics in the subalpine Lake Maggiore (N. Italy). J Limnol71:9 [CrossRef]
    [Google Scholar]
  10. Callieri C., Coci M., Corno G., Macek M., Modenutti B., Balseiro E., Bertoni R.. 2013; Phylogenetic diversity of nonmarine picocyanobacteria. FEMS Microbiol Ecol85:293–301 [CrossRef][PubMed]
    [Google Scholar]
  11. Chisholm S. W., Olson R. J., Zettler E. R., Goericke R., Waterbury J. B., Welschmeyer N. A.. 1988; A novel free-living prochlorophyte abundant in the oceanic euphotic zone. Nature334:340–343 [CrossRef]
    [Google Scholar]
  12. Choi D. H., Noh J. H.. 2006; Molecular phylogenetic analyses of three Synechococcus strains isolated from seawater near the ieodo ocean research station. Ocean Sci J41:315–318 [CrossRef]
    [Google Scholar]
  13. Choi D. H., Noh J. H.. 2009; Phylogenetic diversity of Synechococcus strains isolated from the East China Sea and the East Sea. FEMS Microbiol Ecol69:439–448 [CrossRef][PubMed]
    [Google Scholar]
  14. Choi D. H., Noh J. H., Hahm M.-S., Lee C. M.. 2011; Picocyanobacterial abundances and diversity in surface water of the northwestern Pacific Ocean. Ocean Sci J46:265–271 [CrossRef]
    [Google Scholar]
  15. Crosbie N. D., Pockl M., Weisse T.. 2003a; Dispersal and phylogenetic diversity of nonmarine picocyanobacteria, inferred from 16S rRNA gene and cpcBA-intergenic spacer sequence analyses. Appl Environ Microbiol69:5716–5721 [CrossRef]
    [Google Scholar]
  16. Crosbie N. D., Pöckl M., Weisse T.. 2003b; Rapid establishment of clonal isolates of freshwater autotrophic picoplankton by single-cell and single-colony sorting. J Microbiol Methods55:361–370 [CrossRef]
    [Google Scholar]
  17. Crump B. C., Hobbie J. E.. 2005; Synchrony and seasonality in bacterioplankton communities of two temperate rivers. Limnol Oceanogr50:1718–1729 [CrossRef]
    [Google Scholar]
  18. Dokulil M. T., Teubner K.. 2012; Deep living Planktothrix rubescens modulated by environmental constraints and climate forcing. Hydrobiologia698:29–46 [CrossRef]
    [Google Scholar]
  19. Domaizon I., Savichtcheva O., Debroas D., Arnaud F., Villar C., Pignol C., Alric B., Perga M. E.. 2013; DNA from lake sediments reveals the long-term dynamics and diversity of Synechococcus assemblages. Biogeosciences10:3817–3838 [CrossRef]
    [Google Scholar]
  20. Dvořák P., Casamatta D. A., Poulíčková A., Hašler P., Ondřej V., Sanges R.. 2014a; Synechococcus: 3 billion years of global dominance. Mol Ecol23:5538–5551[CrossRef]
    [Google Scholar]
  21. Dvořák P., Hindák F., Hašler P., Hindáková A., Poulíčková A.. 2014b; Morphological and molecular studies of Neosynechococcus sphagnicola, gen. et sp. nov. (Cyanobacteria, Synechococcales). Phytotaxa170:024–034[CrossRef]
    [Google Scholar]
  22. Edgar R. C.. 2010; Search and clustering orders of magnitude faster than blast. Bioinformatics26:2460–2461 [CrossRef][PubMed]
    [Google Scholar]
  23. Edgar R. C., Haas B. J., Clemente J. C., Quince C., Knight R.. 2011; UCHIME improves sensitivity and speed of chimera detection. Bioinformatics27:2194–2200 [CrossRef][PubMed]
    [Google Scholar]
  24. Ernst A.. 1991; Cyanobacterial picoplankton from Lake Constance. I. Isolation by fluorescence characteristics. J Plankton Res13:1307–1312[CrossRef]
    [Google Scholar]
  25. Ernst A., Marschall P., Postius C.. 1995; Genetic diversity among Synechococcus spp. (cyanobacteria) isolated from the pelagial of Lake Constance. FEMS Microbiol Ecol17:197–204[CrossRef]
    [Google Scholar]
  26. Ernst A., Becker S., Wollenzien U., Postius C.. 2003; Ecosystem-dependent adaptive radiations of picocyanobacteria inferred from 16S rRNA and ITS-1 sequence analysis. Microbiology149:217–228 [CrossRef][PubMed]
    [Google Scholar]
  27. Farrant G. K., Doré H., Cornejo-Castillo F. M., Partensky F., Ratin M., Ostrowski M., Pitt F. D., Wincker P., Scanlan D. J. et al. 2016; Delineating ecologically significant taxonomic units from global patterns of marine picocyanobacteria. Proc Natl Acad Sci U S A113:E3365E3374 [CrossRef]
    [Google Scholar]
  28. Findenegg I.. 1973; Vorkommen und biologisches Verhalten der Blaualge Oscillatoria rubescens DC. in den östereichischen Alpenseen. Carinthia II163:317–330
    [Google Scholar]
  29. Flombaum P., Gallegos J. L., Gordillo R. A., Rincon J., Zabala L. L., Jiao N., Karl D. M., Li W. K. W., Lomas M. W. et al. 2013; Present and future global distributions of the marine Cyanobacteria Prochlorococcus and Synechococcus. Proc Natl Acad Sci U S A110:9824–9829 [CrossRef]
    [Google Scholar]
  30. Fuller N. J., Marie D., Partensky F., Vaulot D., Post A. F., Scanlan D. J.. 2003; Clade-specific 16S ribosomal DNA oligonucleotides reveal the predominance of a single marine Synechococcus clade throughout a stratified water column in the Red Sea. Appl Environ Microbiol69:2430–2443 [CrossRef][PubMed]
    [Google Scholar]
  31. Garneau M.-È., Posch T., Hitz G., Pomerleau F., Pradalier C., Siegwart R., Pernthaler J.. 2013; Short-term displacement of Planktothrix rubescens (cyanobacteria) in a pre-alpine lake observed using an autonomous sampling platform. Limnol Oceanogr58:1892–1906[CrossRef]
    [Google Scholar]
  32. Garneau M.-È., Posch T., Pernthaler J.. 2015; Seasonal patterns of microcystin-producing and non-producing Planktothrix rubescens genotypes in a deep pre-alpine lake. Harmful Algae50:21–31[CrossRef]
    [Google Scholar]
  33. Greisberger S., Dokulil M. T., Teubner K.. 2008; A comparison of phytoplankton size-fractions in Mondsee, an alpine lake in Austria: distribution, pigment composition and primary production rates. Aquat Ecol42:379–389 [CrossRef]
    [Google Scholar]
  34. Hammer Ø., Harper D. A. T., Ryan P. D.. 2001; PAST: Paleontological Statistics Software Package for education and data analysis. Palaeontol Electronica4:1–92
    [Google Scholar]
  35. Haverkamp T. H., Schouten D., Doeleman M., Wollenzien U., Huisman J., Stal L. J.. 2009; Colorful microdiversity of Synechococcus strains (picocyanobacteria) isolated from the Baltic Sea. ISME J3:397–408 [CrossRef][PubMed]
    [Google Scholar]
  36. Hiorns W. D., Methé B. A., Nierzwicki-Bauer S. A., Zehr J. P.. 1997; Bacterial diversity in Adirondack mountain lakes as revealed by 16S rRNA gene sequences. Appl Environ Microbiol63:2957–2960[PubMed]
    [Google Scholar]
  37. Honda D., Yokota A., Sugiyama J.. 1999; Detection of seven major evolutionary lineages in cyanobacteria based on the 16S rRNA gene sequence analysis with new sequences of five marine Synechococcus strains. J Mol Evol48:723–739 [CrossRef][PubMed]
    [Google Scholar]
  38. Huang S., Wilhelm S. W., Harvey H. R., Taylor K., Jiao N., Chen F.. 2012; Novel lineages of Prochlorococcus and Synechococcus in the global oceans. ISME J6:285–297 [CrossRef][PubMed]
    [Google Scholar]
  39. Ivanikova N. V., Popels L. C., McKay R. M., Bullerjahn G. S.. 2007; Lake Superior supports novel clusters of cyanobacterial picoplankton. Appl Environ Microbiol73:4055–4065 [CrossRef][PubMed]
    [Google Scholar]
  40. Jacquet S., Kerimoglu O., Rimet F., Paolini G., Anneville O.. 2014; Cyanobacterial bloom termination: the disappearance of Planktothrix rubescens from Lake Bourget (France) after restoration. Freshw Biol59:2472–2487 [CrossRef]
    [Google Scholar]
  41. Jasser I., Królicka A., Karnkowska-Ishikawa A.. 2011; A novel phylogenetic clade of picocyanobacteria from the Mazurian lakes (Poland) reflects the early ontogeny of glacial lakes. FEMS Microbiol Ecol75:89–98 [CrossRef][PubMed]
    [Google Scholar]
  42. Jeppesen E., Peder Jensen J., SØndergaard M., Lauridsen T., Landkildehus F.. 2000; Trophic structure, species richness and biodiversity in Danish lakes: changes along a phosphorus gradient. Freshw Biol45:201–218 [CrossRef]
    [Google Scholar]
  43. Klindworth A., Pruesse E., Schweer T., Peplies J., Quast C., Horn M., Glöckner F. O.. 2012; Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res1-:11
    [Google Scholar]
  44. Komárek J.. 2016; Review of the cyanobacterial genera implying planktic species after recent taxonomic revisions according to polyphasic methods: state as of 2014. Hydrobiologia764:259–270 [CrossRef]
    [Google Scholar]
  45. Lavín P. L., Lourenço S. O.. 2005; An evaluation of the accumulation of intracellular inorganic nitrogen pools by marine microalgae in batch cultures. BrazJ Oceanogr53:55–68 [CrossRef]
    [Google Scholar]
  46. Li W. K. W.. 1994; Primary production of prochlorophytes, cyanobacteria, and eucaryotic ultraphytoplankton: measurements from flow cytometric sorting. Limnol Oceanogr39:169–175 [CrossRef]
    [Google Scholar]
  47. Li W. K. W., Rao D. V. S., Harrison W. G., Smith J. C., Cullen J. J., Irwin B., Platt T.. 1983; Autotrophic picoplankton in the tropical ocean. Science (Washington)219:292–295 [CrossRef]
    [Google Scholar]
  48. Lindström E. S.. 2001; Investigating influential factors on bacterioplankton community composition: results from a field study of five mesotrophic lakes. Microb Ecol42:598–605 [CrossRef][PubMed]
    [Google Scholar]
  49. Lindström E. S., Leskinen E.. 2002; Do neighboring lakes share common taxa of bacterioplankton? Comparison of 16S rDNA fingerprints and sequences from three geographic regions. Microb Ecol44:1–9 [CrossRef][PubMed]
    [Google Scholar]
  50. Lindström E. S., Kamst-Van Agterveld M. P., Zwart G.. 2005; Distribution of typical freshwater bacterial groups is associated with pH, temperature, and lake water retention time. Appl Environ Microbiol71:8201–8206 [CrossRef][PubMed]
    [Google Scholar]
  51. Liu H., Nolla H. A., Campbell L.. 1997; Prochlorococcus growth rate and contribution to primary production in the equatorial and subtropical North Pacific Ocean. Aquatic Microbial Ecology12:39–47 [CrossRef]
    [Google Scholar]
  52. Ludwig W., Strunk O., Westram R., Richter L., Meier H., Buchner A., Lai T., Steppi S., Jobb G. et al. 2004; ARB: a software environment for sequence data. Nucleic Acids Res32:1363–1371 [CrossRef][PubMed]
    [Google Scholar]
  53. Maeda H., Kawai A., Tilzer M. M.. 1992; The water bloom of cyanobacterial picoplankton in Lake Biwa, Japan. Hydrobiologia248:93–103 [CrossRef]
    [Google Scholar]
  54. Mazard S., Ostrowski M., Partensky F., Scanlan D. J.. 2012; Multi-locus sequence analysis, taxonomic resolution and biogeography of marine Synechococcus. Environ Microbiol14:372–386 [CrossRef][PubMed]
    [Google Scholar]
  55. Melzer A.. 1999; Aquatic macrophytes as tools for lake management. Hydrobiologia396:181–190[CrossRef]
    [Google Scholar]
  56. Metzker M. L.. 2010; Sequencing technologies – the next generation. Nat Rev Genet11:31–46 [CrossRef][PubMed]
    [Google Scholar]
  57. Newton R. J., Jones S. E., Eiler A., McMahon K. D., Bertilsson S.. 2011; A guide to the natural history of freshwater lake bacteria. Microbiol Mol Biol Rev75:14–49 [CrossRef][PubMed]
    [Google Scholar]
  58. Oberhaus L., Briand J. F., Leboulanger C., Jacquet S., Humbert J. F.. 2007; Comparative effects of the quality and quantity of light and temperature on the growth of Planktothrix agardhii and P. rubescens. J Phycol43:1191–1199 [CrossRef]
    [Google Scholar]
  59. Partensky F., Blanchot J., Vaulot D.. 1999; Differential distribution and ecology of Prochlorococcus and Synechococcus in oceanic waters: a review. Bulletin-Institut Oceanographique Monaco-Numero Special-19:457–476
    [Google Scholar]
  60. Pittera J., Humily F., Thorel M., Grulois D., Garczarek L., Six C.. 2014; Connecting thermal physiology and latitudinal niche partitioning in marine Synechococcus. ISME J8:1221–1236 [CrossRef]
    [Google Scholar]
  61. Pruesse E., Peplies J., Glöckner F. O.. 2012; SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics28:1823–1829 [CrossRef][PubMed]
    [Google Scholar]
  62. Raeder U., Ruzicka J., Goos C.. 2010; Characterization of the light attenuation by periphyton in lakes of different trophic state. Limnologica40:40–46 [CrossRef]
    [Google Scholar]
  63. Robertson B. R., Tezuka N., Watanabe M. M.. 2001; Phylogenetic analyses of Synechococcus strains (cyanobacteria) using sequences of 16S rDNA and part of the phycocyanin operon reveal multiple evolutionary lines and reflect phycobilin content. Int J Syst Evol Microbiol51:861–871 [CrossRef][PubMed]
    [Google Scholar]
  64. Sánchez-Baracaldo P., Hayes P. K., Blank C. E.. 2005; Morphological and habitat evolution in the Cyanobacteria using a compartmentalization approach. Geobiology3:145–165 [CrossRef]
    [Google Scholar]
  65. Sánchez-Baracaldo P., Handley B. A., Hayes P. K.. 2008; Picocyanobacterial community structure of freshwater lakes and the Baltic Sea revealed by phylogenetic analyses and clade-specific quantitative PCR. Microbiology154:3347–3357 [CrossRef][PubMed]
    [Google Scholar]
  66. Savichtcheva O., Debroas D., Perga M. E., Arnaud F., Villar C., Lyautey E., Kirkham A., Chardon C., Alric B. et al. 2015; Effects of nutrients and warming on Planktothrix dynamics and diversity: a palaeolimnological view based on sedimentary DNA and RNA. Freshw Biol60:31–49 [CrossRef]
    [Google Scholar]
  67. Scanlan D. J., West N. J.. 2002; Molecular ecology of the marine cyanobacterial genera Prochlorococcus and Synechococcus. FEMS Microbiol Ecol40:1–12 [CrossRef][PubMed]
    [Google Scholar]
  68. Scanlan D. J., Ostrowski M., Mazard S., Dufresne A., Garczarek L., Hess W. R., Post A. F., Hagemann M., Paulsen I. et al. 2009; Ecological genomics of marine picocyanobacteria. Microbiol Mol Biol Rev73:249–299 [CrossRef][PubMed]
    [Google Scholar]
  69. Schmidt T. M., DeLong E. F., Pace N. R.. 1991; Analysis of a marine picoplankton community by 16S rRNA gene cloning and sequencing. J Bacteriol173:4371–4378 [CrossRef][PubMed]
    [Google Scholar]
  70. Schuster S. C.. 2007; Next-generation sequencing transforms today’s biology. Nature5:16–18
    [Google Scholar]
  71. Shannon C. E., Weaver W.. 1948; A mathematical theory of communication. Bell System Technical Journal27:379–423 [CrossRef]
    [Google Scholar]
  72. Sohm J. A., Ahlgren N. A., Thomson Z. J., Williams C., Moffett J. W., Saito M. A., Webb E. A., Rocap G.. 2016; Co-occurring Synechococcus ecotypes occupy four major oceanic regimes defined by temperature, macronutrients and iron. ISME J10:333–345 [CrossRef][PubMed]
    [Google Scholar]
  73. Steinberg C. E. W., Hartmann H. M.. 1988; Planktonic bloom-forming Cyanobacteria and the eutrophication of lakes and rivers. Freshw Biol20:279–287 [CrossRef]
    [Google Scholar]
  74. Stockner J. G., Shortreed K. S.. 1991; Autotrophic picoplankton: community composition, abundance and distribution across a gradient of oligotrophic British Columbia and Yukon Territory lakes. Internationale Revue der gesamten Hydrobiologie und Hydrographie76:581–601 [CrossRef]
    [Google Scholar]
  75. Stockner J., Callieri C., Cronberg G.. 2000; Picoplankton and other non-bloom-forming cyanobacteria in lakes. In The Ecology of Cyanobacteria pp.195–231 Netherland: Springer;
    [Google Scholar]
  76. Sudek S., Everroad R. C., Gehman A. L., Smith J. M., Poirier C. L., Chavez F. P., Worden A. Z.. 2015; Cyanobacterial distributions along a physico-chemical gradient in the Northeastern Pacific Ocean. Environ Microbiol17:3692–3707 [CrossRef][PubMed]
    [Google Scholar]
  77. Tai V., Palenik B.. 2009; Temporal variation of Synechococcus clades at a coastal Pacific Ocean monitoring site. ISME J3:903–915 [CrossRef][PubMed]
    [Google Scholar]
  78. Tai V., Burton R. S., Palenik B.. 2011; Temporal and spatial distributions of marine Synechococcus in the Southern California Bight assessed by hybridization to bead-arrays. Mar Ecol Prog Ser426:133–147 [CrossRef]
    [Google Scholar]
  79. Urbach E., Scanlan D. J., Distel D. L., Waterbury J. B., Chisholm S. W.. 1998; Rapid diversification of marine picophytoplankton with dissimilar light-harvesting structures inferred from sequences of Prochlorococcus and Synechococcus (Cyanobacteria). J Mol Evol46:188–201 [CrossRef][PubMed]
    [Google Scholar]
  80. Van den Wyngaert S., Salcher M. M., Pernthaler J., Zeder M., Posch T.. 2011; Quantitative dominance of seasonally persistent filamentous cyanobacteria (Planktothrix rubescens) in the microbial assemblages of a temperate lake. Limnol Oceanogr56:97–109 [CrossRef]
    [Google Scholar]
  81. Veldhuis M. J. W., Kraay G. W., Van Bleijswijk J. D. L., Baars M. A.. 1997; Seasonal and spatial variability in phytoplankton biomass, productivity and growth in the northwestern Indian Ocean: the southwest and northeast monsoon, 1992–1993. Deep Sea Research Part I: Oceanographic Research Papers44:425–449 [CrossRef]
    [Google Scholar]
  82. Vörös L., Callieri C., Katalin V., Bertoni R.. 1998; Freshwater picocyanobacteria along a trophic gradient and light quality range. In Phytoplankton and Trophic Gradients pp.117–125 Netherland: Springer;[CrossRef]
    [Google Scholar]
  83. Waterbury J. B., Watson S. W., Guillard R. R., Brand L. E.. 1979; Widespread occurrence of a unicellular, marine, planktonic, cyanobacterium. Nature277:293–294 [CrossRef]
    [Google Scholar]
  84. Weisse T.. 1988; Dynamics of autotrophic picoplankton in Lake Constance. J Plankton Res10:1179–1188 [CrossRef]
    [Google Scholar]
  85. Zwart G., Crump B. C., Kamst-van Agterveld M. P., Hagen F., Han S. K.. 2002; Typical freshwater bacteria: an analysis of available 16S rRNA gene sequences from plankton of lakes and rivers. Aquat Microbial Ecol28:141–155 [CrossRef]
    [Google Scholar]
  86. Zwirglmaier K., Heywood J. L., Chamberlain K., Woodward E. M., Zubkov M., Scanlan D. J.. 2007; Basin-scale distribution patterns of picocyanobacterial lineages in the Atlantic Ocean. Environ Microbiol9:1278–1290 [CrossRef][PubMed]
    [Google Scholar]
  87. Zwirglmaier K., Jardillier L., Ostrowski M., Mazard S., Garczarek L., Vaulot D., Not F., Massana R., Ulloa O. et al. 2008; Global phylogeography of marine Synechococcus and Prochlorococcus reveals a distinct partitioning of lineages among oceanic biomes. Environ Microbiol10:147–161 [CrossRef][PubMed]
    [Google Scholar]
  88. Zwirglmaier K., Keiz K., Engel M., Geist J., Raeder U.. 2015; Seasonal and spatial patterns of microbial diversity along a trophic gradient in the interconnected lakes of the Osterseen Lake District, Bavaria. Front Microbiol6:1–18 [CrossRef][PubMed]
    [Google Scholar]
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