Dark Respiration and Organic Carbon Loss

Chapter
Part of the Developments in Applied Phycology book series (DAPH, volume 6)

Abstract

The dark respiratory pathways of eukaryotic microalgae are generally similar to those of other eukaryotes. Differences include the Entner-Douderoff pathway replacing the Emden-Meyer-Parnas pathway of glycolysis in diatom plastids, the presence of an alternative pathway from 2-oxoglutarate to succinate in the Tricarboxylic Acid Cycle in Euglena and cyanobacteria, and the constitutive replacement in dinoflagellates of the H+-pumping Complex I in the inner mitochondrial membrane by a matrix NADH –UQ oxidoreductase that does not pump H+. All of these alternative pathways have a lower energetic efficiency than the mechanisms they replace. Widespread among microalgae is the mitochondrial alternate oxidase that facultatively replaces H+-pumping Complexes III and IV with a non-energy conserving pathway. More remains to be established on, for example, the H+:electron ratio and H+:ATP ratios in mitochondrial reactions in algae, and hence the energetic efficiency of ATP synthesis in oxidative phosphophorylation. The main functions of respiration are growth processes, converting photosynthate and exogenous inorganic nutrients into cell material using ATP, NADPH and C skeleton manipulations, and maintenance using ATP. For both processes ATP and NADPH can also be supplied in the light by thylakoid reactions although the extent of dark respiratory processes (other the C skeleton manipulations) is still uncertain. Dissolved organic C loss occurs in algae, though there is net organic C entry in osmo-chemorganotrophic growth. While some functions of dissolved organic molecules lost from cells are known, more remains to be established on the magnitude and role of this loss in photolithotrophic relative to phago-chemorganotrophic and phagomixotrophic growth.

Keywords

Alternate Oxidase ATP C Skeletons Emden-Meyer-Parnas pathway Entner-Douderoff pathway Growth respiration Maintenance respiration Mitochondria NADPH Osmo-chemoorganotrophy Phagochemoorganotrophy Phagomixotrophy Photolithotrophy Dissolved organic compounds Tricarboxylic acid cycle 

Notes

Acknowledgements

The University of Dundee is a registered Scottish charity, NO 015096

References

  1. Atteia A, van Lis R, Tielens AGM, Martin WF (2013) Anaerobic energy metabolism in unicellular photosynthetic eukaryotes. Biochim Biophys Acta 1827:210–213CrossRefPubMedGoogle Scholar
  2. Beardall J, Raven JA (1990) Pathways and mechanisms of respiration in microalgae. Mar Microb Food Webs 4:7–30Google Scholar
  3. Beardall J, Raven JA (2016) Carbon acquisition by microalgae. In: Borowitzka MA, Beardall J, Raven J, Beardall J (eds) The physiology of microalgae. Springer, Dordrecht, pp 89–99Google Scholar
  4. Beardall J, Burger-Wiersma T, Rijkboer M, Sukenik A, Lemoalle J, Dubinsky Z, Fontvielle D (1994) Studies on enhanced post-illumination respiration in microalgae. J Plankton Res 16:1401–1410CrossRefGoogle Scholar
  5. Beardall J, Quigg A, Raven JA (2003) Oxygen consumption: photorespiration and chlororespiration. In: Larkum AWD, Douglas SE, Raven JA (eds) Photosynthesis in algae. Kluwer, Dordrecht, pp 157–181CrossRefGoogle Scholar
  6. Beardall J, Ihnkken S, Quigg A (2009) Gross and net primary production: closing the gap between concepts and measurements. Aquat Microb Ecol 56:113–122CrossRefGoogle Scholar
  7. Betschke T, Schaller D, Melkonian M (1992) Identification and characterization of glycolate oxidase and related enzymes for the endocyanote alga Cyanophora paradoxa and for pea leaves. Plant Physiol 98:287–293CrossRefGoogle Scholar
  8. Borowitzka MA (2016) Systematics, taxonomy and species names: do they matter? In: Borowitzka MA, Beardall J, Raven JA (eds) The physiology of microalgae. Springer, Dordrecht, pp 655–681Google Scholar
  9. Cardol P, González-Halphen D, Reyes-Prieto A, Baurarin D, Matagne RE, Ramacle C (2005) The mitochondrial oxidative phosphorylation proteome of Chlamydomonas reinhardtii deduced from the genome sequencing project. Plant Physiol 137:447–459CrossRefPubMedPubMedCentralGoogle Scholar
  10. Cardol P, Ballieul B, Rappaport F, Derelle E, Béal D, Breyton C, Bailey S, Wallman FA, Grossman A, Moreau H, Rinnazi G (2008) An original adaptation of photosynthesis in the marine green alga Ostreococcus. Proc Natl Acad Sci U S A 105:7581–7586CrossRefGoogle Scholar
  11. Carvalho MC, Eyre BD (2012) Measurement of planktonic respiration in the light. Limnol Oceanogr Methods 10:167–178CrossRefGoogle Scholar
  12. Chautin MS, Winge P, Brembu T, Vadstein O, Bones AT (2013) Gene regulation of carbon fixation, storage and utilization in the diatom Phaeodactylum tricornutum acclimated to light-dark cycles. Plant Physiol 161:1034–1048CrossRefGoogle Scholar
  13. Chrétionnot-Dinet M-J, Courties C, Vacquer A, Neveux J, Claustre H, Lautier J, Machado MC (1995) A new marine picoeukaryote: Ostreococcus tauri gen et sp. nov (Chlorophyta, Prasinophyceae). Phycologia 34:285–292CrossRefGoogle Scholar
  14. Cid A, Herrero C, Abalde J (1996) Functional analysis of phytoplankton by flow cytometry: a study of the effect of copper on a marine diatom. Sci Mar 60(Suppl 1):303–308Google Scholar
  15. Cosper E (1982) Influence of light intensity on dial variations in rates of growth, respiration and organic release of a marine diatom: comparison of diurnally constant and fluctuating light. J Plankton Res 4:705–724CrossRefGoogle Scholar
  16. Cuhel RL, Ortner PB, Lean RS (1984) Night synthesis of protein by algae. Limnol Oceanogr 29:731–744CrossRefGoogle Scholar
  17. Danne JC, Gornik SG, MacRae JI, McComville MJ, Waller RF (2012) Alveolate mitochondrial metabolic evolution: dinoflagellates force reassessment of the role of parasitism as a driver of change in apicomplexans. Mol Biol Evol 30:123–139CrossRefPubMedGoogle Scholar
  18. Droop MR (1974) Heterotrophy. In: Stewart WDP (ed) Algal physiology and biochemistry. Blackwell Scientific Publications, Oxford, pp 530–559Google Scholar
  19. Eisenhut M, Ruth W, Haimovitch M, Bauwe M, Kaplan A, Hagemann M (2006) The plant-like C2 glycolate pathway and the bacterial-like glycerate pathway cooperate in phosphoglycolate metabolism in cyanobacteria. Plant Physiol 142:333–342CrossRefPubMedPubMedCentralGoogle Scholar
  20. Eisenhut M, Ruth W, Haimovitch M, Bauwe M, Kaplan A, Hagemann M (2008) The photorespiratory glycolate metabolism is essential for cyanobacteria and may have been conveyed endosymbiotically to plants. Proc Natl Acad Sci U S A 105:17199–17204CrossRefPubMedPubMedCentralGoogle Scholar
  21. Engel A, Thoms S, Rebesell U, Rochell-Newall R, Zondervan I (2004) Polysaccharide aggregation as potential sink for dissolved organic carbon. Nature 428:929–932CrossRefPubMedGoogle Scholar
  22. Fabris M, Matthijs M, Rombautsm SM, Goossens A, Baart GJE (2012) The metabolic blueprint of Phaeodactylum tricornutum reveals a eukaryotic Entner-Doudoroff glycolytic pathway. Plant J 70:1004–1014CrossRefPubMedGoogle Scholar
  23. Falkowski PG, Raven JA (2007) Aquatic photosynthesis, 2nd edn. Princeton University Press, Princeton, pp xiii + 484Google Scholar
  24. Fietz S, Nicklisch A (2002) Acclimation of the diatom Stephanodiscus neoastraeae and the cyanobacterium Planktothrix agardhii to simulated natural light fluctuations. Photosynth Res 72:95–106CrossRefPubMedGoogle Scholar
  25. Flamholz A, Noor E, Bar-Even A, Liebermeister W, Milo R (2013) Glycolytic strategy as a trade off between energy yield and protein cost. Proc Natl Acad Sci U S A 110:10039–10044CrossRefPubMedPubMedCentralGoogle Scholar
  26. Flynn KJ, Raven JA, Rees TAV, Finkel Z, Quigg A, Beardall J (2010) Is the growth rate hypothesis applicable to microalgae? J Phycol 46:1–12CrossRefGoogle Scholar
  27. Flynn KJ, Stoecker DK, Mitra A, Raven JA, Glibert PM, Hansen PJ, Granéli E, Burkholder JM (2013) A case of mistaken identification: the importance of mixotrophs and the clarification of plankton functional-classification. J Plankton Res 35:3–11CrossRefGoogle Scholar
  28. Gaffron H (1944) Photosynthesis, photoreduction and dark reduction of carbon dioxide by certain algae. Biol Rev 19:1–20CrossRefGoogle Scholar
  29. Geider RJ, Osborne BA (1989) Respiration and microalgal growth: a review of the quantitative relationship between dark respiration and growth. New Phytol 112:327–341CrossRefGoogle Scholar
  30. Giordano M, Norici A, Forssen M, Eriksson M, Raven JA (2003) An anaplerotic role for mitochondrial carbonic anhydrase in Chlamydomonas reinhardtii. Plant Physiol 132:2126–2134CrossRefPubMedPubMedCentralGoogle Scholar
  31. Granum E, Myklestad SM (1999) Effects of NH4 + assimilation on dark carbon fixation and β-1,3-glucan metabolism in the marine diatom Skeletonema costatum (Bacillariophyceae). J Phycol 35:1191–1199CrossRefGoogle Scholar
  32. Granum E, Roberts K, Raven JA, Leegood RC (2009) Primary carbon and nitrogen metabolic gene expression in the diatom Thalassiosira pseudonana (Bacillariophyceae): diel periodicity and effects of inorganic carbon and nitrogen. J Phycol 45:1083–1092CrossRefGoogle Scholar
  33. Hartz AJ, Aaron J, Sherr BJ, Sherr EB (2011) Photoresponse in the heterotrophic marine dinoflagellate Oxyrrhis marina. J Eukaryot Microbiol 58:171–177CrossRefPubMedGoogle Scholar
  34. Hellebust JA (1974) Extracellular products. In: Stewart WDP (ed) Algal physiology and biochemistry. Blackwell Scientific Publications, Oxford, pp 828–863Google Scholar
  35. Iluz D, Alexandrovitch I, Dubinsky Z (2012) The enhancement of photosynthesis by fluctuating light. In: Najaalpour M (ed) Artificial photosynthesis. Intech Europe, Rijeka, pp 110–134Google Scholar
  36. Janke C, Scholz F, Becker-Haldus J, G;aubitz C, Wood PG, Bamberg E, Wachtveitl J, Bamann C (2013) Photocycle and vectorial proton transfer in a rhodopsin from a eukaryote Oxyrrhis marina. Biochemistry 52:2750–2763CrossRefPubMedGoogle Scholar
  37. Jarmuszkiewicz W, Woyda-Plosczyka A, Antos-Krzeminska N, Sluse FE (2010) Mitochondrial uncoupling proteins in unicellular eukaryotes. Biochem Biophys Acta 1797:792–799PubMedGoogle Scholar
  38. Kamjunke N, Tittel J (2009) Mixotrophic algae constrain the loss of organic carbon by exudation. J Phycol 45:807–811CrossRefGoogle Scholar
  39. Knoop H, Gründel H, Zilliges Y, Lehman R, Hoffman R, Lockau W, Steuers R (2013) Flux analysis of cyanobacterial metabolism: the metabolic network of Synechocystis sp. PCC 6803. PLoS Comput Biol 9(6):e1003081CrossRefPubMedPubMedCentralGoogle Scholar
  40. Kroth PG, Chiovitti A, Gruber A, Martin-Jezequel V, Mock T, Parker MS, Stanley MS, Kaplan A, Caron L, Weber T, Maheswari U, Armbrust EV, Bowler C (2008) A model for carbohydrate metabolism in the diatom Phaeodactylum tricornutum deduced from comparative whole genome analysis. PLoS One 3(1):e1426CrossRefPubMedPubMedCentralGoogle Scholar
  41. Kübler JE, Raven JA (1996) Inorganic carbon acquisition by red algae grown under dynamic light regimes. Hydrobiologia 326/327:401–406Google Scholar
  42. Liaud M-F, Lichtlé C, Apt K, Martin W, Cerff R (2000) Compartment-specific isoforms of TPI and GAPDH are imported into mitochondria as a fusion protein: evidence in favor of a mitochondrial origin of the eukaryotic glycolytic pathway. Mol Biol Evol 17:13–223CrossRefGoogle Scholar
  43. Lloyd D (1974) Dark respiration. In: Stewart WDP (ed) Algal physiology and biochemistry. Blackwell Scientific Publications, Oxford, pp 505–520Google Scholar
  44. López-Sandorval DC, Rodríguez-Ramosm T, Cermeño P, Marañón E (2013) Exudation of organic carbon by marine phytoplankton dependence on taxon and cell size. Mar Ecol Prog Ser 477:53–60CrossRefGoogle Scholar
  45. Luinenberg L, Coleman JR (1990) A requirement for phosphoenolpyruvate carboxylase in the cyanobacterium Synechococcus PPC 7942. Arch Microbiol 154:471–474CrossRefGoogle Scholar
  46. Luinenberg L, Coleman JR (1993) Expression of Escherichia coli phosphoenolpyruvate carboxylase in a cyanobacterium. Plant Physiol 101:121–126CrossRefGoogle Scholar
  47. Luz B, Barkan E (2000) Assessment of oceanic productivity with triple-isotope composition of dissolved oxygen. Science 288:2028–2031CrossRefPubMedGoogle Scholar
  48. Marchetti A, Schruth DM, Durkin CA, Parker MS, Kodner RB, Berthiaume CT, Morales R, Allen AE, Armbrust EV (2012) Comparative metagenomics identifies molecular bases for the physiological responses of phytoplankton to varying iron availability. Proc Natl Acad Sci U S A 109:E317–E325CrossRefPubMedPubMedCentralGoogle Scholar
  49. Mayer SM, Beale SI (1992) Succinyl-Coenzyme A synthetase and its role in δ-amino levulinic acid biosynthesis in Euglena gracilis. Plant Physiol 99:482–487CrossRefPubMedPubMedCentralGoogle Scholar
  50. Needoba JA, Harrison PJ (2004) Influence of low light and light: dark cycle on NO3 uptake, intracellular NO3 , and nitrogen isotope discrimination by marine phytoplankton. J Phycol 40:505–516CrossRefGoogle Scholar
  51. Nicklisch A, Steinberg CEW (2009) RNA/protein and RNA/DNA ratios by flow cytometry and their relationship to growth limitation of selected planktonic algae in culture. Eur J Phycol 44:297–308CrossRefGoogle Scholar
  52. Petersen J, Förster K, Turina P, Gräber P (2012) Comparison of the H+/ATP ratios of the H+-ATP synthases from yeast and from chloroplasts. Proc Natl Acad Sci U S A 109:11150–11155CrossRefPubMedPubMedCentralGoogle Scholar
  53. Prihoda J, Tanaka A, de Paula WBM, Allen JF, Tirichine L, Bowler C (2012) Chloroplast-mitochondria cross-talk in diatoms. J Exp Bot 63:1543–1557CrossRefPubMedGoogle Scholar
  54. Quigg A, Beardall J (2003) Protein turnover in relation to maintenance metabolism at low photon flux in two marine microalgae. Plant Cell Environ 26:693–703CrossRefGoogle Scholar
  55. Quigg A, Kevekordes K, Raven JA, Beardall J (2006) Limitations on microalgal growth at very low photon fluence rates: the role of energy slippage. Photosynth Res 88:299–310CrossRefPubMedGoogle Scholar
  56. Quigg A, Kotabová E, Jarešová J, Kaňa R, Šetlik J, Šedová B, Komárek O, Prášil O (2012) Photosynthesis in Chromera velia represents a simple system with high efficiency. PLoS One 7(10):e47036CrossRefPubMedPubMedCentralGoogle Scholar
  57. Raven JA (1974) Carbon dioxide fixation. In: Stewart WDP (ed) Algal physiology and biochemistry. Blackwell Scientific Publications, Oxford, pp 433–455Google Scholar
  58. Raven JA (1976a) Division of labour between chloroplasts and cytoplasm. In: Barber J (ed) The intact chloroplast. Elsevier, Amsterdam, pp 403–443Google Scholar
  59. Raven JA (1976b) The quantitative role of ‘dark’ respiratory processes in heterotrophic and photolithotrophic plant growth. Ann Bot 40:587–602Google Scholar
  60. Raven JA (1984) Energetics and transport in aquatic plants. A.R. Liss, New York, pp xi + 587Google Scholar
  61. Raven JA (2001) A role for mitochondrial carbonic anhydrase in limiting CO2 leakage from low CO2-grown cells of Chlamydomonas reinhardtii? Plant Cell Environ 24:261–265CrossRefGoogle Scholar
  62. Raven JA (2009) Functional evolution of photochemical energy transformation in oxygen- producing organisms. Funct Plant Biol 36:505–515CrossRefGoogle Scholar
  63. Raven JA (2010) Cyanotoxins: a poison that frees phosphate. Curr Biol 20:R850–R852CrossRefPubMedGoogle Scholar
  64. Raven JA (2011) The cost of photoinhibition. Physiol Plant 142:87–104CrossRefPubMedGoogle Scholar
  65. Raven JA (2012a) Protein turnover and plant RNA and phosphorus requirements in relation to nitrogen fixation. Plant Sci 188–189:25–35CrossRefPubMedGoogle Scholar
  66. Raven JA (2012b) Carbon. In: Whitton BA (ed) Ecology of cyanobacteria II: their diversity in space and time. Springer, Berlin, pp 443–460CrossRefGoogle Scholar
  67. Raven JA (2013) RNA function and P use by photosynthetic organisms. Front Plant Sci 4(536):1–13. doi: 10.3389/fpls.2013.00536 Google Scholar
  68. Raven JA, Beardall J (1981a) Respiration and photorespiration. In: Platt T (ed) Physiological bases of phytoplankton ecology, pp 55–82. Government of Canada Publications, Ottawa, Canada No. 210, pp 55–82Google Scholar
  69. Raven JA, Beardall J (1981b) The intrinsic permeability of biological membranes to H+: significance for low rates of energy transformation. FEMS Microbiol Lett 10:1–5CrossRefGoogle Scholar
  70. Raven JA, Beardall J (1982) The lower limit of photon fluence rate for phototrophic growth: the significance of ‘slippage’ reactions. Plant Cell Environ 5:117–124Google Scholar
  71. Raven JA, Beardall J (2003) Carbohydrate metabolism and respiration in algae. In: Larkum AWD, Douglas SE, Raven JA (eds) Photosynthesis in algae. Kluwer, Dordrecht, pp 205–224CrossRefGoogle Scholar
  72. Raven JA, Beardall J (2005) Respiration in aquatic photolithotrophs. In: del Gioirgio PA, Williams PJLB (eds) Respiration in aquatic ecosystems. Oxford University Press, Oxford, pp 36–46CrossRefGoogle Scholar
  73. Raven JA, Farquhar GD (1990) The influence of N metabolism and organic acid synthesis on the natural abundance of C isotopes in plants. New Phytol 116:505–529CrossRefGoogle Scholar
  74. Raven JA, Ralph PJ (2015) Enhanced biofuel production using optimality, pathway modification and waste minimization. J Appl Phycol 27:1–31CrossRefGoogle Scholar
  75. Raven JA, Smith FA (1978) Effect of temperature on the ion content, ion fluxes and energy metabolism in Chara corallina. Plant Cell Environ 1:231–238CrossRefGoogle Scholar
  76. Raven JA, Smith FA, Glidewell SM (1979) Photosynthetic capacities and biological strategies of giant-celled and small-celled macroalgae. New Phytol 83:299–309CrossRefGoogle Scholar
  77. Raven JA, Johnston AM, MacFarlane JJ (1990) Carbon metabolism. In: Sheath RG, Cole KM (eds) The biology of the red algae. Cambridge University Press, Cambridge, pp 171–202Google Scholar
  78. Raven JA, Kübler JI, Beardall J (2000) Put out the light, and then put out the light. J Mar Biol Assoc U K 80:1–25CrossRefGoogle Scholar
  79. Raven JA, Brown K, Mackay M, Beardall J, Giordano M, Granum E, Leegood RC, Kilminster K, Walker DI (2005) Iron, nitrogen, phosphorus and zinc cycling and consequences for primary productivity in the oceans. In: Gadd GM, Sempele KT, Lappin-Scott HM (eds) Society for General Microbiology Symposium 65. Micro-organisms and earth systems: advances in geobiology. Cambridge University Press, Cambridge, pp 247–272CrossRefGoogle Scholar
  80. Raven JA, Beardall J, Larkum AWD, Sanchez-Baracaldo P (2013) Interaction of photosynthesis with genome size and function. Phil Trans Roy Soc London B 368:2012–2264CrossRefGoogle Scholar
  81. Read BA, Kegel J, Klute MJ, Kuo A et al (2013) Pan genome of the phytoplankter Emiliania underpins its global distribution. Nature 499:209–213CrossRefPubMedGoogle Scholar
  82. Remacle C, Baurain D, Cardoll P, Matgane RF (2001) Mutants of Chlamydomonas reinhardtii deficient in mitochondrial complex I: characterization of two mutations affecting the nfI coding sequence. Genetics 156:1051–1060Google Scholar
  83. Schaum CE, Collins S (2014) Plasticity predicts evolution in a marine alga. Proc Roy Soc B 281:20141486. doi: 10.1098/rspb.2014.1486 CrossRefGoogle Scholar
  84. Schmidt S, Raven JA, Paungfoo-Lonhienne C (2013) The mixotrophic nature of photosynthetic plants. Funct Plant Biol 40:425–438CrossRefGoogle Scholar
  85. Shiheoka S, Onishi T, Maeda K, Nakano Y, Kitaoka S (1986) Occurrence of thiamin pyrophosphate-dependent 2-oxoglutarate decarboxylase in mitochondria of Euglena gracilis. FEBS Lett 195:43–47CrossRefGoogle Scholar
  86. Slamovitz CH, Okmaoto N, Burri J, James JR, Keeling PJ (2011) A bacterial proteorhodopsin in marine eukaryotes. Nat Commun 2:183. doi: 10.1038/ncomms1188 CrossRefGoogle Scholar
  87. Vanlerberghe GC, Schuller KA, Smith RG, Fell R, Plaxton WC, Turpin DH (1990) Relationship between NH4 + assimilation rate and in vivo phosphoenolpyruvate carboxylase activity. Regulation of anaplerotic carbon flow in the green alga Selenastrum minutum. Plant Physiol 94:284–290CrossRefPubMedPubMedCentralGoogle Scholar
  88. Vázquez-Avecedo M, Cardol P, CanpEstrada A, Lapaille M, Remacle C, Gonmzález-Halphen D (2006) The mitochondrial ATP synthase of chlorophycean algae contains eight subunits of unknown origin involved in the formation of an atypical stalk-structure and in the dimerization of the complex. J Bioenerg Biomembr 38:271–282CrossRefGoogle Scholar
  89. Wagner H, Jakob T, Wilhelm C (2006) Balancing the energy flow from captured light to biomass under fluctuating light conditions. New Phytol 169:95–108CrossRefPubMedGoogle Scholar
  90. Wikström M, Hummer G (2012) Stoichiometry of proton translocation by respiratory complex I and its mechanistic implications. Proc Natl Acad Sci U S A 109:4431–4436CrossRefPubMedPubMedCentralGoogle Scholar
  91. Xue X, Gauthier DA, Turpin DH, Weger HG (1996) Interactions between photosynthesis and respiration in the green alga Chlamydomonas reinhardtii. Characterisation of light-enhanced dark respiration. Plant Physiol 112:1005–1014PubMedPubMedCentralGoogle Scholar
  92. Zhang S, Bryant DA (2011) The tricarboxylic acid cycle of cyanobacteria. Science 334:1551–1663CrossRefPubMedGoogle Scholar

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© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Division of Plant BiologyUniversity of Dundee at the James Hutton InstituteInvergowrieUK
  2. 2.Plant Functional Biology and Climate Change ClusterUniversity of Technology SydneyUltimoAustralia
  3. 3.School of Biological SciencesMonash UniversityClaytonAustralia

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