Abstract
Synthetic colors have been widely used in various industries including food, textile, cosmetic and pharmaceuticals. However toxicity problems caused by synthetic pigments have triggered intense research in natural colors and dyes. Among the natural Sources, pigment producing microorganisms hold a promising potential to meet present day challenges. Furthermore natural colors not only improve the marketability of the product but also add extra features like anti oxidant, anti cancer properties etc. In this review, we present various sources of microbial pigments and to explore their biological and clinical properties like antimicrobial, antioxidant, anticancer and anti inflammatory. The study also emphasizes upon key parameters to improve the bioactivity and production of microbial pigments for their commercial use in pharmacological and medical fields.
Similar content being viewed by others
References
Agarwal SK, Singh SS, Verma S, Kumar S (2000) Antifungal activity of anthraquinone derivatives from Rheum emodi. J Ethnopharmacol 72(1):43–46
Andersen DO, Weber ND, Wood SG, Hughes BG, Murray BK, North JA (1991) In vitro virucidal activity of selected anthraquinones and anthraquinone derivatives. Antivir Res 16(2):185–196
Andrighetti-Frohner CR, Antonio RV, Creczynski-Pasa TB, Barandi CRM, Simo˜es CMO (2003) Cytotoxicity and potential antiviral evaluation of violacein produced by Chromobacterium violaceum. Mem Inst Oswaldo Cruz 98:834–848
Antonisamy P, Ignacimuthu S (2010) Immunomodulatory, analgesic and antipyretic effects of violacein isolated from chromobacterium violaceum. Phytomedicine 17:300–304
Araújo HWCD, Fukushima K, Takaki GMC (2010) Prodigiosin production by Serratia marcescens UCP 1549 using renewable-resources as a Low cost substrate. Molecules 15:6931–6940
Arias JI, Aller MA, Arias J (2007) Cancer cell; using inflammation to invade the host. Mol Cancer 6:29–39
Baron SS, Rowe JJ (1981) Antibiotic action of pyocyanin. Antimicrob Agents Chemother 20:814–820
Blanc PJ, Loret MO, Santerre AL, Pareilleux A, Prome D, Prome JC, Laussac JP, Goma G (1994) Pigments of Monascus. J Food Sci 59:862–865
Cerdá-Olmedo E (2001) Phycomyces and the biology of light and color. FEMS Microbiol Rev 25:503–512
Chew BP, Park JS, Wong MW, Wong TS (1998) A comparison of the anticancer activities of dietary beta-carotene, canthaxanthin and astaxanthin in mice in vivo. Anticancer Res 19(3A):1849–1853
Cho YJ, Hwang HJ, Kim SW, Song CH, Yun JW (2002) Effect of carbon source and aeration rate on broth rheology and fungal morphology during red pigment production by Paecilomyces sinclairii in a batch bioreactor. J Biotechnol 95:13–23
Clauditz A, Resch A, Wieland KP, Peschel A, Götz F (2006) Staphyloxanthin plays a role in the fitness of Staphylococcus aureus and its ability to cope with oxidative stress. Infect Immun 74(8):4950–4953
Clydesdale FM (1993) Color as a factor in food choice. Crit Rev Food Sci Nutr 33(1):83–101
Cooney JJ, Marks HW, Smith AM (1966) Isolation and identification of canthaxanthin from Micrococcus roseus. J Bacteriol 92:342–345
Costa FTM, Justo GZ, Dura’n N, Nogueira PA, Lopes SCP: The use of violacein in its free and encapsulated form in polymeric systems against malaria. Brazilian Patent PIBr 2005, 056399–0
Cude WN, Mooney J, Tavanaei AA, Hadden MK, Frank AM, Gulvik CA, May AL, Buchan A (2012) Production of the antimicrobial secondary metabolite indigoidine contributes to competitive surface colonization by the marine roseobacter Phaeobacter sp. strain Y4I. Appl Environ Microbiol 78(14):4771–4780
De Azevedo MBM, Melo PS, Almeida ABA, Souza-Brito ARM, Haun M, Dura’n N (2000) Antiulcerogenic activity of violacein/beta-cyclodextrin inclusion complexes and violacein. Proc Int Sym Controlled Release Bioact Mater 27:508–509
Deorukhkar AA, Chander R, Ghosh SB, Sainis KB (2007) Identification of a red-pigmented bacterium producing a potent anti-tumor N-alkylated prodigiosin as Serratia marcescens. Res Microbiol 158(5):399–404
Di Mascio P, Kaiser S, Sies H (1989) Lycopene as the most efficient biological carotenoid singlet oxygen quencher. Arch Biochem Biophys 274(2):532–538
Duffose L (2006) Microbial production of food grade pigments, food grade pigments. Food Technol Biotechnol 44(3):313–321
Dufossé L (2009) Microbial and microalgal carotenoids as colourants and supplements. In Carotenoids Birkhäuser Basel 83–98
Dura’n N, Justo GZ, Melo PS, De Azevedo MBM, Souza-Brito ARM, Almeida ABA, Haun M (2003) Evaluation of the antiulcerogenic activity of violacein and its modulation by the inclusion complexation with beta-cyclodextrin. Can J Physiol Pharmacol 81:387–396
Duran M, Ponezi AN, Faljoni-Alario A, Teixeira MF, Justo GJ, Duran N (2012) Potential applications of violacein: a microbial pigment. Med Chem Res 21(7):1524–1532
Farrow B, Sugiyama Y, Chen A, Uffort E, Nealon W, Mark BE (2004) Inflammatory mechanisms contributing to pancreatic cancer development. Ann Surg 239(6):763–769
Feher D, Barlow RS, Lorenzo PS, Hemscheidt T (2008) A 2-substituted prodiginine, 2-(p-hydroxybenzyl)prodigiosin, from Pseudoalteromonas rubra. J Nat Prod 71(11):1970–1972
Ferreira CV, Bos CL, Versteeq HH, Justo GZ, Duran N, Peppelenbosch MP (2004) Molecular mechanism of violacein-mediated human leukemia cell death. Blood 104(5):1459–1464
Florencio JA, Soccol CR, Furlanetto LF, Bonfim TMB, Krieger N, Baron M, Fontana JD (1998) A factorial approach for a sugarcane juice-based low cost culture medium: increasing the astaxanthin production by the red yeast Phaffia rhodozyma. Bioprocess Eng 19:161–164
Flores-Cotera LB, Sanchez S (2001) Copper but not iron limitation increases astaxanthin production by Phaffia rhodozyma in a chemically defined medium. Biotechnol Lett 23:793–797
Fuhrman B, Elis A, Aviram M (1997) Hypocholesterolemic effect of lycopene and β-carotene is related to suppression of cholesterol synthesis and augmentation of LDL receptor activity in macrophages. Biochem Biophys Res Commun 233(3):658–662
George YL, Nizet V (2009) Color me bad: microbial pigments as virulence factors. Trends Microbiol 17(9):406–413
Gerber NN (1975) A new prodiginine (prodigiosin like) pigment from Streptomyces. Antimalarial Act Several Prodiginines J Antibiot 28:194–199
Giovannucci E, Rimm EB, Liu Y, Stampfer MJ, Willett WC (2002) A prospective study of tomato products, lycopene, and prostate cancer risk. J Natl Cancer Inst 94(5):391–398
Grossart HP, Thorwest M, Plitzko I, Brinkhoff T, Simon M, Zeeck A (2009) Production of a blue pigment (glaukothalin) by marine rheinheimera spp. Int J Microbiol 2009:701735
Guerin M, Huntley ME, Olaizola M (2003) Haematococcus astaxanthin: applications for human health and nutrition. Trends Biotechnol 21(5):210–216
Hammond RK, White DC (1970) Inhibition of carotenoid hydroxylation in Staphylococcus aureus by mixed-function oxidase inhibitors. J Bacteriol 103:607–610
Han SB, Park SH, Jeon YJ, Kim YK, Kim HM, Yang KH (2001) Prodigiosin blocks T cell activation by inhibiting interleukin - 2Rα expression and delays progression of autoimmune diabetes and collagen induced arthritis. J Pharm Exp Ther 299:415–425
Hayashi M, Matsui M (2000) Genotoxicity evaluation datasheet of food additives by the MHW (1980–1998). Environ Mutagen Res 22:27–44
Hong MY, Seeram NP, Zhang Y, Heber D (2008) Anticancer effects of Chinese red yeast rice versus monacolin K alone on colon cancer cells. J Nutr Biochem 19(7):448–458
Hsu LC, Hsu YW, Liang YH, Kuo YH, Pan TM (2011) Anti-tumor and anti-inflammatory properties of ankaflavin and monaphilone A from Monascus purpureus NTU 568. J Agri Food Chem 59(4):1124–1130
Iacobucci GA, Sweeney LG (1981) Process for enhancing the sunlight stability of rubrolone. US patent 4:285,985
Ishidate MJ, Sofuni T (1984) Primary mutagenicity screening of food additives currentlyused in Japan. Food Chem Toxicol 22(8):623–636
Jacobson G, Wasileski J (1994) Production of food colorants by fermentation. In Bioprocess Production of Flavor, Fragrance, and Color Ingredients. Ed. A. Gabelman, John Wiley and Sons Inc 205–237.
Joshi V, Attri D, Bala A, Bhushan S (2003) Microbial Pigments. Indian J Biotechnol 2:362–369
Kang JS, Cho SA, Han SB, Lee K, Kim HM (2011) Scytonemin inhibits lipopolysaccharide-induced production of nitric oxide, tumor necrosis factor-α and interleukin-1β by blocking NF-{kappa}B/Rel signaling in macrophages. J Immunol 186:112.13
Kavitha R, Aiswarya S, Ratnawali MG (2010) Anticancer activity of red pigment from Serratia marcescens in human cervix carcinoma. Int J ChemTech Res 2(1):784–787
Keith S, Kaye MD, Donald Kaye MD (2000) Multidrug-resistant pathogens: mechanisms of resistance and epidemiology. Curr Infect Disease Rep 2(5):391–398
Kim HS, Hayashi M, Shibata Y (1999) Cycloprodigiosin hydrochloride obtained from Pseudoalteromonas denitrificans is a potent antimalarial agent. Biol Pharm Bull 22(5):532–534
Kobayashi M, Kakizono T, Nagai S (1993) Enhanced carotenoid biosynthesis by oxidative stress in acetate induced cyst cells of a green unicellular alga, Haematococcus pluvialis. Appl Environ Microbiol 59:867–873
Konzen M, De Marco D, Cordova CA, Vieira TO, Antônio RV, Creczynski-Pasa TB (2006) Antioxidant properties of violacein: possible relation on its biological function. Bioorg Med Chem 14(24):8307–8313
Kumar S (2007) Antimalarial drugs inhibiting hemozoin (beta-hematin) formation: a mechanistic update. Life Sci 80:813–828
Kurjogi MM, Sanakal RD, Kaliwal BB (2010) Antibiotic susceptibility and antioxidant activity of Staphylococcus aureus pigment staphyloxanthin on carbon tetrachloride (ccl4) induced stress in swiss albino mice. Int J Biot Appl 2(2):33–40
Lampila LE, Wallen SE, Bullerman LB (1985) A review of factors affecting biosynthesis of carotenoids by the order Mucorales. Mycopathologia 90:65–80
Liu GY, Essex A, Buchanan JT, Datta V, Hoffman HM, Bastian JF, Fierer J, Nizet V (2005a) Staphylococcus aureus golden pigment impairs neutrophil killing and promotes virulence through its antioxidant activity. J Exp Med 202(2):209–215
Liu R, Cui CB, Duan L, Gu QQ, Zhu WM (2005b) Potentin Vitro anticancer activity of metacycloprodigiosin and undecylprodigiosin from a sponge-derived actinomycete Sac-charopolyspora sp. nov. Archives Pharm Res 28(12):1341–1344
Lo HM, Chen CL, Yang CM, Wu PH, Tsou CJ, Chiang KW, Wu WB (2013) The carotenoid lutein enhances matrix metalloproteinase-9 production and phagocytosis through intracellular ROS generation and ERK1/2, p38 MAPK, and RARβ activation in murine macrophages. J Leukoc Biol 93(5):723–35
Lopes SCP, Blanco YC, Justo GZ, Nogueira PA, Rodrigues FLS, Goelnitz U, Wunderlich G, Facchini G, Brocchi M, Dura’n N, Costa FTM (2009) Violacein extracted from Chromobacterium violaceum inhibits Plasmodium growth in vitro and in vivo. Antimicrob Agents Chemother 53:2149–2152
Lorquin J, Molouba F, Dreyfus BL (1997) Identification of the carotenoid pigment canthaxanthin from photosynthetic Bradyrhizobium strains. Appl Environ Microbiol 63:1151–1154
Mathews-Roth MM (1982) Antitumor activity of β-carotene, canthaxanthin and phytoene. Oncology 39(1):33–37
Matula TI, Downie RH (1984) Genetic toxicity of erythrosine in yeast. Mutat Res 138(2–3):153–156
Matz C, Deines P, Boenigk J, Arndt H, Eberl L, Kjelleberg S, Jurgens K (2004) Impact of violacein producing bacteria on survival and feeding of bacteriovorans nanoflagellates. Appl Environ Microbiol 70:1593–1599
McGregor DB, Brown A (1988) Responses of the L5178Y tk+/tk- mouse lymphoma cell forward mutation assay: III. 72 coded chemicals. Environ Mol Mutagen 12(1):85–154
Mekhael R, Yousif SY (2009) The role of red pigment produced by Serratia marcescens as antibacterial and plasmid curing agent. J Duhok Univ 12(1):268–274
Melvin MS, Tomlinson JT, Saluta GR, Kucera GL, Lindquist N, Manderville RA (2000) Double-strand DNA cleavage by copper prodigiosin. J Am Chem Soc 122(26):6333–6334
Montaner B, Navarro S, Pique M, Vilaseca M, Martinell M, Giralt E, Gil J, Perez-Thomas R (2000) Prodigiosin from the supernatant of serratia marcescens induce apoptosis in haematopoietic cancer cell lines. Br J Pharmacol 131(3):585–593
Nakamura Y, Asada C, Sawada T (2003) Production of antibacterial violet pigment by psychrotropic bacterium RT102 strain. Biotechnol Bioprocess Eng 8:37–40
Nelson WG, De AMM, De TLW, Isaacs WB (2004) The role of inflammation in the pathogenesis of prostate cancer. J Urol 172:S6–11
Nematollahi A, Aminimoghadamfarouj N, Wiart C (2012) Reviews on 1, 4-naphthoquinones from Diospyros L. J Asian Nat Prod Res 14(1):80–88
Pandey R, Chander R, Sainis KB (2007) Prodigiosins; A novel family of immunosuppressants with anticancer activity. Ind J Biochem Biophy 44:295–302
Patel KC, Patel MA, Chauhan K, Anto H, Trivedi U (2007) Production of an antioxidant naphthaquinone pigmant by comamonas testosteroni during growth on naphthalene. J Scientific Indus Res 66:605–610
Patterson RM, Butler JS (1982) Tartrazine-induced chromosomal aberrations in mammalian cells. Food Chem Toxicol 20(4):461–465
Powers HJ (2003) Riboflavin (vitamin B-2) and health. Am J Clin Nutr 77(6):1352–1360
Prathumpai W, Phimmakong K, Srikitikulchai P, Wongsa P (2006) Kinetic study of naphthoquinone and key metabolite production of C. unilateralis BCC1869. Thai J Biotechnol 7(2):39–43
Price PJ, Suk WA (1978) In vitro and in vivo indications of the carcinogenicity and toxicity of food dyes. Int J Cancer 21:361–367
Rajagopal L, Sundari CS, Balasubramanian D, Sonti RV (1997) The bacterial pigment Xanthomonadin offers protection against photodamage. FEBS Lett 415:125–128
Ramirez I, Nunez ML, Valdivia R (2000) Increased astaxanthin production by a Phaffia rhodozyma mutant grown on date juice from Yucca fillifera. J Ind Microbiol Biotechnol 24:187–190
Rayburn ER, Ezell SJ, Zhang R (2009) Anti-inflammatory agents for cancer therapy. Mol Cell Pharmacol 1(1):29–43
Reyes FG, Valim MF, Vercesi AE (1996) Effect of organic synthetic food colours on mitochondrial respiration. Food Addit Contam 13(1):5–11
Rosa-Fraile M (2006) Granadaene: proposed structure of the group B Streptococcus polyenic pigment. Appl Environ Microbiol 72:6367–6370
Sakaki H, Nakanishi T, Satonaka KY, Miki W, Fujita T, Komemushi S (2000) Properties of a high-torularhodin mutant of Rhodotorula glutinis cultivated under oxidative stress. J Biosci Bioeng 89:203–205
Sasaki YF, Kawaguchi S (2002) The comet assay with 8 mouse organs: results with 39 currently used food additives. Mutat Res 519:103–119
Schüep W, Blount JF, Williams TH, Stempel A (1978) Production of a novel red pigment, rubrolone, by Streptomyces echinoruber Sp. Nov II Chem Struct Elucidation J Antibiot 31(12):1226–1232
Shirata A, Tsukamoto T, Yasui H, KatoH HS, Kojima A (1997) Production of bluish-purple pigments by Janthinobacterium lividum isolated from the raw silk and dyeing with them. Nippon Sanshigaku Zasshi 66:377–385
Stankovic N, Radulovic V, Petkovic M, Vuckovic I, Jadranin M, Vasiljevic B, Nikodinovic-Runic J (2012) Streptomyces sp. JS520 produces exceptionally high quantities of undecylprodigiosin with antibacterial, antioxidative, and UV-protective properties. Appl Microbial Biotechnol 96(5):1217–1231
Starr MP (1958) The blue pigment of Corynebacterium insidiosum. Arch Mikrobiol 30:325–334
Stevenson CS, Capper EA, Roshak AK (2002) Scytonemin— a marine natural product inhibitor of kinases key in hyperproliferative inflammatory diseases. Inflamm Res 51(2):112–114
Terao J (1989) Antioxidant activity of β-carotene-related carotenoids in solution. Lipids 24(7):659–661
Tsuji RF, Yamamoto M, Nakamura A, Kataoka T, Magae J, Nagai K, Yamasaki M (1990) Selective immunosuppression of prodigiosin 25-C and FK506 in the murine immune system. J Antibiot 43(10):1293–1301
Tuli HS, Sharma AK, Sandhu SS (2013) Pharmacological and Therapeutic potential of Cordyceps with special reference to Cordycepin. 3Biotech. DOI 10.1007/s13205-013-0121-9.
Unagul P, Wongsa P, Kittakoop P, Intamas S, Srikitikulchai P, Tanticharoen M (2005) Production of red pigments by the insect pathogenic fungus Cordyceps unilateralis. J Ind Microbiol Biotechnol 32:135–140
Ungureanu C, Ferdes M (2012) Evaluation of antioxidant and antimicrobial activities of torularhodin. Adv Sci Lett 18(1):50–53
Vasanthabharathi V, Lakshminarayanan R, Jayalakshmi S (2011) Melanin production from marine Streptomyces. Afr J Biotechnol 10(54):11224–11234
Venil CK, Lakshmanaperumalsamy P (2009) An insightful overview on microbial pigment, prodigiosin. Elect J Biol 5(3):49–61
Venil CK, Zakaria ZA, Ahmad WA (2013) Bacterial pigments and their applications. Process Biochem 48(7):1065–1079
Ventura Pinto A, Lisboa de Castro S (2009) The trypanocidal activity of naphthoquinones: a review. Molecules 14(11):4570–4590
Vinarov A, Robucheva Z, Sidorenko T, Dirina E (2003) Microbial biosynthesis and making of pigment melanin. Commun Agric Appl Biol Sci 68:325–326
Visalakchi S, Muthumary J (2010) Antimicrobial activity of the new endophytic Monodictys castaneae SVJM139 pigment and its optimization. Afr J Microbiol Res 3(9):550–556
Wagner-D¨obler I, Beil W, Lang S, Meiners M, Laatsch H (1996) Integrated approach to explore the potential of marine microorganisms for the production of bioactive metabolites. Adv Biochem Eng Biotechnol 74:207–238
Wang D, Dubois RN, Richmond A (2009) The role of chemokines in intestinal inflammation andcancer. Curr Opin Pharmacol 9:688–8
Wissgot U, Bortlik K (1996) Prospects for new food colorants. Trends Food Sci Technol 7:298–302
Wodicka VO (1996) Regulation of food: where have we been? Food Technol 50:106–109
Yamamoto C, Takemoto H, Kuno K, Yamamoto D, Tsubura A, Kamata K, Hirata H, Yamamoto A, Kano H, Seki T, Inoue K (1999) Cycloprodigiosin hydrochloride, a new H+/Cl − symporter, induces apoptosis in human and rat hepatocellular cancer cell lines in vitro and inhibits the growth of hepatocellular carcinoma xenografts in nude mice. Hepatol 30(4):894–902
Zheng Y, Xin Y, Shi X, Guo Y (2010) Anti-cancer effect of rubropunctatin against human gastric carcinoma cells BGC-823. Appl Microbiol Biotechnol 88(5):1169–1177
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Tuli, H.S., Chaudhary, P., Beniwal, V. et al. Microbial pigments as natural color sources: current trends and future perspectives. J Food Sci Technol 52, 4669–4678 (2015). https://doi.org/10.1007/s13197-014-1601-6
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13197-014-1601-6