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Microbial Pigments

  • Júlio C. De CarvalhoEmail author
  • Lígia C. Cardoso
  • Vanessa Ghiggi
  • Adenise Lorenci Woiciechowski
  • Luciana Porto de Souza Vandenberghe
  • Carlos Ricardo Soccol
Chapter

Abstract

Color is a visual way of communication and rather very important one in foods, drugs, and cosmetics for creating or maintaining their acceptability or appeal. However, not all products are colored, or evenly so, and color additives are to be used in these products. Synthetic colors are being substituted by natural color additives, which have a market estimated in US$ 600 million and steadily growing at around 2 % annually. Natural colors are usually easier to metabolize than their synthetic counterparts and in several cases even have beneficial metabolic activity, as in carotenoid pigments. As a natural source, microbial pigments are suitable for mass production, when compared with vegetal or animal extracts. At the other side, these color additives are inherently less stable than synthetic ones, a problem that explains the limited palette of commercial microbial color additives. This chapter discusses the biological function of biopigments and presents the most important cases of commercial microbial pigments such as β-carotene, riboflavin, astaxanthin, phycocyanin, chlorophyllins, and Monascus pigments and the challenges and opportunities of its production using agro-industrial wastes. Finally, it discusses new product development, from microorganism selection to product formulation and trends in biopigment production.

Keywords

Color Additive Mixotrophic Culture Riboflavin Production Rhodotorula Glutinis Monascus Pigment 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Abe K, Hattori H, Hirano M (2007) Accumulation and antioxidant activity of secondary carotenoids in the aerial microalga Coelastrella striolata var multistriata. Food Chem 100:656–661CrossRefGoogle Scholar
  2. Aberoumand A (2011) A review article on edible pigments properties and sources as natural biocolorants in foodstuff and food industries. World J Dairy Food Sci 6:71–78Google Scholar
  3. Babitha S, Soccol CR, Pandey A (2006) Jackfruit seed – a novel substrate for the production of Monascus pigments through solid-state fermentation. Food Technol Biotechnol 44:465–471Google Scholar
  4. BBC Research (2010) Carotenoids global market folder. http://www.bbcresearch.com. Accessed 13 Oct 2012
  5. Ben DR, Ghenim N, Trabelsi L, Yahia A, Challouf R, Ghozzi K, Ammar J, Omrane H, Ben OH (2010) Modeling growth and photosynthetic response in Arthrospira platensis as function of light intensity and glucose concentration using factorial design. J Appl Phycol 22:745–752CrossRefGoogle Scholar
  6. Boussiba S, Fan L, Vonshak A (1992) Enhancement and determination of astaxanthin accumulation in green alga Haematococcus pluvialis. Methods Enzymol 213:386–391CrossRefGoogle Scholar
  7. Buzzini P, Martini A (1999) Production of carotenoids by strains of Rhodotorula glutinis cultured in raw materials of agro-industrial origin. Bioresour Technol 71:41–44CrossRefGoogle Scholar
  8. Carvalho JC, Oishi BO, Pandey A, Soccol CR (2005) Biopigments from Monascus: strains selection, citrinin production and color stability. Braz Arch Biol Technol 48:885–894CrossRefGoogle Scholar
  9. Carvalho JC, Pandey A, Oishi BO, Brand D, Rodriguez-Leon JA, Soccol CR (2006) Relation between growth, respirometric analysis and biopigments production from Monascus by solid-state fermentation. Biochem Eng J 29:262–269CrossRefGoogle Scholar
  10. Carvalho JC, Oishi BO, Woiciechowski AL, Pandey A, Soccol CR (2007) Effect of substrates on the production of Monascus biopigments by solid-substrate fermentation and pigment extraction using different solvents. Ind J Biotechnol 6:194–199Google Scholar
  11. Chaiklahan R, Chirasuwan N, Bunnag B (2012) Stability of phycocyanin extracted from Spirulina sp: influence of temperature, pH and preservatives. Process Biochem 47:659–664CrossRefGoogle Scholar
  12. Cheirsilp B, Torpee S (2012) Enhanced growth and lipid production of microalgae under mixotrophic culture condition: effect of light intensity, glucose concentration and fed-batch cultivation. Bioresour Technol 110:510–516CrossRefGoogle Scholar
  13. Chen F, Zhang Y, Guo S (1996) Growth and phycocyanin formation of Spirulina platensis in photoheterotrophic culture. Biotechnol Lett 18:603–608CrossRefGoogle Scholar
  14. Chen F, Zhang Y (1997) High cell density mixotrophic culture of Spirulina platensis on glucose for phycocyanin production using a fed-batch system. Enzyme Microb Technol 20:221–224CrossRefGoogle Scholar
  15. Das A, Yoon SH, Lee SH, Kim JY, Oh DK, Kim SW (2007) An update on microbial carotenoid production: application of recent metabolic engineering tools. Appl Microbiol Biotechnol 77:505–512CrossRefGoogle Scholar
  16. Del Campo JA, Moreno J, Rodrıguez H, Vargas MA, Rivas J, Guerrero MJ (2000) Carotenoid content of chlorophycean microalgae: factors determining lutein accumulation in Muriellopsis sp (Chlorophyta). J Biotechnol 76:51–59CrossRefGoogle Scholar
  17. Dufossé L (2006) Microbial production of food grade pigments. Food Technol Biotechnol 44:313–321Google Scholar
  18. Durán D, Teixeira MFS, Conti R, Esposito E (2002) Ecological-friendly pigments from fungi. Crit Rev Food Sci Nutr 42:53–66CrossRefGoogle Scholar
  19. Elliot AM (1934) Morphology and life history of Haematococcus pluvialis. Archiv Protistenk 82:250–272Google Scholar
  20. Dominguez-Espinosa RM, Webb C (2003) Submerged fermentation in wheat substrates for production of Monascus pigments. World J Microbiol Biotechnol 19:329–336CrossRefGoogle Scholar
  21. FDA (2012) Color additives inventories. http://www.fda.gov. Accessed 13 Oct 2012
  22. FAO (2012) Yearbook of fishery statistics. http://www.fao.org/fishery/statistics/programme/publications/all/en. Accessed 15 Nov 2012
  23. Garcıa-Malea MC, Brindley C, Del Río E, Acien FG, Fernandez JM, Molina E (2005) Modeling of growth and accumulation of carotenoids in Haematococcus pluvialis as a function of irradiance and nutrients supply. Biochem Eng J 26:107–114CrossRefGoogle Scholar
  24. Giri AV, Anandkumar N, Muthukumaran G, Pennathur G (2004) A novel medium for the enhanced cell growth and production of prodigiosin from Serratia marcescens isolated from soil. BMC Microbiol 4:11. Available at http://www.biomedcentral.com/content/pdf/1471-2180-4-11.pdf. Accessed 15 Nov 2012
  25. Graverholt OS, Eriksen NT (2007) Heterotrophic high-cell-density fed-batch and continuous-flow cultures of Galdieria sulphuraria and production of phycocyanin. Appl Microbiol Biotechnol 77:69–75CrossRefGoogle Scholar
  26. Gulani C, Bhattacharya S, Das A (2012) Assessment of process parameters influencing the enhanced production of prodigiosin from Serratia marcescens and evaluation of its antimicrobial, antioxidant and dyeing potentials. Maln J Microbiol 8:116–122Google Scholar
  27. Harker M, Tsavalos A, Young AJ (1996) Factors responsible for astaxanthin formation in the chlorophyte Haematococcus pluvialis. Bioresour Technol 55:207–217CrossRefGoogle Scholar
  28. Hirschberg J et al (1999) Carotenoid-producing bacterial species and process for production of carotenoids using same. United States Patent 5,935,808Google Scholar
  29. Hoffmann JP (1998) Wastewater treatment with suspended and non-suspended algae. J Phycol 34:757–763CrossRefGoogle Scholar
  30. Hong ME, Choi SP, Park YI, Kim YK, Chang WS, Kim BW, Sim SJ (2012) Astaxanthin production by a highly photosensitive Haematococcus mutant. Process Biochem, 47:1972–1979. http://dx.doi.org/10.1016/j.procbio.2012.07.007
  31. Ip PF, Wong KH, Chen F (2004) Enhanced production of astaxanthin by the green microalga Chlorella zofingiensis in mixotrophic culture. Process Biochem 39:1761–1766CrossRefGoogle Scholar
  32. Ip PF, Chen F (2005) Production of astaxanthin by the green microalga Chlorella zofingiensis in the dark. Process Biochem 40:733–738CrossRefGoogle Scholar
  33. Kang DK, An JY, Park TH, Sim SJ (2006) Astaxanthin biosynthesis from simultaneous N and P uptake by the green alga Haematococcus pluvialis in primary-treated wastewater. Biochem Eng J 31:234–238CrossRefGoogle Scholar
  34. Khodaiyan F, Razavi SH, Mousavi SM (2008) Optimization of canthaxanthin production by Dietzia natronolimnaea HS-1 from cheese whey using statistical experimental methods. Biochem Eng J 40:415–422CrossRefGoogle Scholar
  35. Kim SJ, Lee HK, Lee YK, Yim JH (2008) Mutant selection of Hahella chejuensis KCTC 2396 and statistical optimization of medium components for prodigiosin yield-up. J Microbiol 46:183–188CrossRefGoogle Scholar
  36. Kleinegris DMM, Janssen M, Brandenburg WA, Wijffels RH (2011) Continuous production of carotenoids from Dunaliella salina. Enzyme Microb Technol 48:253–259CrossRefGoogle Scholar
  37. Kobayashi M, Kakizono T, Nishio S, Nagai S (1992) Effects of light intensity, light quality and illumination cycle on astaxanthin formation in the green alga Haematococcus pluvialis. J Ferment Bioeng 74:61–63CrossRefGoogle Scholar
  38. Kuo FS, Chien YH, Chen CJ (2012) Effects of light sources on growth and carotenoid content of photosynthetic bacteria Rhodopseudomonas palustris. Bioresour Technol 113:315–318CrossRefGoogle Scholar
  39. Kwon SK, Park YK, Kim JF (2010) Genome-wide screening and identification of factors affecting the biosynthesis of prodigiosin by Hahella chejuensis, using Escherichia coli as a surrogate host. Appl Environ Microbiol 76:1661–1668CrossRefGoogle Scholar
  40. Lim SH, Choi JS, Park EY (2001) Microbial production of riboflavin using riboflavin overproducers, Ashbya gossypii, Bacillus subtilis, and Candida famata: an overview. Biotechnol Bioprocess Eng 6:75–88CrossRefGoogle Scholar
  41. Lin CF, Iizuka H (1982) Production of extracellular pigment by a mutant of Monascus kaoliang sp nov. Appl Environ Microbiol 43(3):671–676Google Scholar
  42. Margalith PZ (1999) Production of ketocarotenoids by microalgae. Appl Microbiol Biotechnol 51:431–438CrossRefGoogle Scholar
  43. Marova I, Carnecka M, Halienova A, Certik M, Dvorakova T, Haronikova A (2012) Use of several waste substrates for carotenoid-rich yeast biomass production. J Environ Manag 95:338–342CrossRefGoogle Scholar
  44. Meléndez-Martínez AJ, Britton G, Vicario IM, Heredia FJ (2007) Relationship between the colour and the chemical structure of carotenoid pigments. Food Chem 101:1145–1150CrossRefGoogle Scholar
  45. Merck (2006) The Merck index. Merck &Co, Whitehouse Station, NJGoogle Scholar
  46. Margalith PZ (1992) Pigment microbiology. Chapman & Hall, CambridgeGoogle Scholar
  47. Mendes AS, Carvalho JE, Duarte MCT, Durán N, Bruns RE (2001) Factorial design and response surface optimization of crude violacein for Chromobacterium violaceum production. Biotechnol Lett 23:1963–1969CrossRefGoogle Scholar
  48. Miki W (1991) Biological functions and activities of animal carotenoids. Pure Appl Chem 63:141–146CrossRefGoogle Scholar
  49. Mishraa SK, Shrivastava R, Mauryaa RR, Patidara SK, Haldarb S, Mishraa S (2012) Effect of light quality on the C-phycoerythrin production in marine cyanobacteria Pseudanabaena sp isolated from Gujarat coast, India. Protein Expr Purif 81:5–10CrossRefGoogle Scholar
  50. Nelis HJ, De Leenheer AP (1989) Microbial production of carotenoids other than β-carotene. In: Vandamme J (ed) Biotechnology of vitamins, pigments and growth factors. Elsevier, EssexGoogle Scholar
  51. Nassau K (2003) The physics and chemistry of color: the 15 mechanisms. In: Shevell SK (ed) The science of color. Elsevier, New York, NYGoogle Scholar
  52. Orosa M, Franqueira D, Cid A, Abalde J (2001) Carotenoid accumulation in Haematococcus pluvialis in mixotrophic growth. Biotechnol Lett 23:373–378CrossRefGoogle Scholar
  53. Papaioannou EH, Liakopoulou-Kyriakides M (2010) Substrate contribution on carotenoids production in Blakeslea trispora cultivations. Food Bioprod Process 8:305–311CrossRefGoogle Scholar
  54. Perez-Fons L, Steiger S, Khaneja R, Bramley PM, Cutting SM, Sandmann G, Fraser PD (2011) Identification and the developmental formation of carotenoid pigments in the yellow/orange Bacillus spore-formers. Biochim Biophys Acta 1811:177–185CrossRefGoogle Scholar
  55. Puttananjaiah MKH, Dhale MA, Govindaswamy V (2011) Non-toxic effect of Monascus purpureus extract on lactic acid bacteria suggested their application in fermented foods. Food Nutri Sci 2:837–843CrossRefGoogle Scholar
  56. Rangel-Yagui CO, Danesi EDG, Carvalho JCM, Sato S (2004) Chlorophyll production from Spirulina platensis: cultivation with urea addition by fed-batch process. Bioresour Technol 92:133–141CrossRefGoogle Scholar
  57. Razavi SH, Marc I (2006) Effect of temperature and pH on the growth kinetics and carotenoid production by Sporobolomyces ruberrimus H110 using technical glycerol as carbon source. Iran Chem Chem Eng 25:59–64Google Scholar
  58. SAG (2012) List of media recipes. http://www.uni-goettingen.de/en/184982.html. Accessed 13 Oct 2012Google Scholar
  59. Shen H, Kuo CC, Chou J, Delvolve A, Jackson SN, Post J, Woods AS, Hoffer BJ, Wang Y, Harvey BK (2009) Astaxanthin reduces ischemic brain injury in adult rats. FASEB J 23(6): 1958–1968Google Scholar
  60. Soccol CR, Sydney EB, de Carvalho JC, Dalmas Neto CJ, Coraucci Neto D, Assmann R, Thomaz-Soccol V (2012) Microalgae use in integrated processes for simultaneous carbon fixation, aqueous agroindustrial residues treatment and production of value-added biomolecules. Annals of the 5th Conference on Industrial Bioprocesses, IFIB, October 7–10, 2012, TaipeiGoogle Scholar
  61. Sommer TR, Pottsa WT, Morrisy NM (1991) Utilization of microalgal astaxanthin by rainbow trout (Oncorhynchus mykiss). Aquaculture 94:79–88CrossRefGoogle Scholar
  62. Soni SK (2007) Microbes: a source of energy for the 21st century. New India Publishing Agency, New DelhiGoogle Scholar
  63. Tagua VG, Medina HR, Martín-Dominguez R, Eslava AP, Corrochano LM, Cerdá-Olmedo E, Idnurm A (2012) A gene for carotene cleavage required for pheromone biosynthesis and carotene regulation in the fungus Phycomyces blakesleeanus. Fungal Genet Biol 49:398–404CrossRefGoogle Scholar
  64. Tanaka T et al (2011) Microorganism and method for producing carotenoid using it. United States Patent 8,030,022Google Scholar
  65. Tchobanoglous G, Burton FL, Stensel HD (2003) Wastewater engineering: treatment, disposal and reuse/Metcalf & Eddy Inc. McGraw-Hill, New York, NYGoogle Scholar
  66. Tinoi J, Rakariyatham N, Deming RL (2005) Simplex optimization of carotenoid production by Rhodotorula glutinis using hydrolyzed mung bean waste flour as substrate. Process Biochem 40:2551–2557CrossRefGoogle Scholar
  67. Tooley AJ, Cai YA, Glazer AN (2001) Biosynthesis of a fluorescent cyanobacterial C-phycocyanin holo-α subunit in a heterologous host. Proc Natl Acad Sci 98:10560–10565CrossRefGoogle Scholar
  68. Silva MC (2004) Alterações na biossíntese de carotenoids em leveduras induzidas por agentes químicos. Thesis, University of CampinasGoogle Scholar
  69. Vaquero I, Ruiz-Domínguez C, Márquez M, Vílchez C (2012) Cu-mediated biomass productivity enhancement and lutein enrichment of the novel microalga Coccomyxa onubensis. Process Biochem 47:694–700CrossRefGoogle Scholar
  70. Varzakakou M, Roukas T, Kotzekidou P (2010) Effect of the ratio of (+) and (-) mating type of Blakeslea trispora on carotene production from cheese whey in submerged fermentation. World J Microbiol Biotechnol 26:2151–2156CrossRefGoogle Scholar
  71. Vignolini S, Rudall PJ, Rowland AR, Moyroud E, Faden RB, Baumberg JJ, Glover BJ, Steiner Y (2012) Pointillist structural color in Pollia fruit. Proc Natl Acad Sci 109:15712–15715CrossRefGoogle Scholar
  72. Vílchez C, Forján E, Cuaresma M, Bédmar F, Garbayo I, Veja JM (2011) Marine carotenoids: biological functions and commercial applications. Mar Drugs 9:319–333CrossRefGoogle Scholar
  73. Walter A, de Carvalho JC, Thomaz-Soccol V, Faria ABB, Ghiggi V, Soccol CR (2011) Study of phycocyanin production from Spirulina platensis under different light spectra. Braz Arch Biol Technol 54:675–682CrossRefGoogle Scholar
  74. Wang F, Jiang JG, Chen Q (2007) Progress on molecular breeding and metabolic engineering of biosynthesis pathways of C30, C35, C40, C45, C50 carotenoids. Biotechnol Adv 25:211–222CrossRefGoogle Scholar
  75. Williamson NR, Fineran PC, Leeper FJ, Salmond GP (2006) The biosynthesis and regulation of bacterial prodiginines. Nat Rev Microbiol 4:887–899CrossRefGoogle Scholar
  76. Yan SG, Zhu LP, Su HN, Zhang XY, Chen XL, Zhou BC, Zhang YZ (2011) Single-step chromatography for simultaneous purification f C-phycocyanin and allophycocyanin with high purity and recovery from Spirulina (Arthrospira) platensis. J Appl Phycol 23:1–6CrossRefGoogle Scholar
  77. Yang XF, Xie ML, Liu Y (2003) Metabolic uncouplers reduce excess sludge production in an activated sludge process. Process Biochem 38:1373–1377CrossRefGoogle Scholar
  78. Yang J, Tan H, Yang R, Sun X, Zhai H, Li K (2011) Astaxanthin production by Phaffia rhodozyma fermentation of cassava residues substrate. Agricult Eng Int 13:1–6Google Scholar
  79. Yarnell A (2012) Bringing blue to a plate near you. Chem Eng News 37:30–31Google Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Júlio C. De Carvalho
    • 1
    Email author
  • Lígia C. Cardoso
    • 2
  • Vanessa Ghiggi
    • 1
  • Adenise Lorenci Woiciechowski
    • 1
  • Luciana Porto de Souza Vandenberghe
    • 1
  • Carlos Ricardo Soccol
    • 1
  1. 1.Department of Biotechnology and Bioprocess EngineeringFederal University of Paraná—UFPRCuritibaBrazil
  2. 2.Positivo UniversityCuritibaBrazil

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