Abstract
Non-toxicity, biodegradability and non-carcinogenicity of the natural pigments, dyes and colorants make them an attractive source for human use. Bacterial pigments are colored metabolites secreted by bacteria under stress. The industrial uses of bacterial pigments have increased many folds because of several advantages over the synthetic pigments. Among natural resources, bacterial pigments are mostly preferred because of simple culturing and pigment extraction techniques, scaling up and being time economical. Generally, the bacterial pigments are safe for human use and therefore have a wide range of applications in pharmaceutical, textile, cosmetics and food industries. Therapeutic nature of the bacterial pigments is revealed because of their antimicrobial, anticancer, cytotoxic and remarkable antioxidant properties. Owing to the importance of bacterial pigments it was considered important to produce a comprehensive review of literature on the therapeutic and industrial potential of bacterial pigments. Extensive literature has been reviewed on the biomedical application of bacterial pigments while further opportunities and future challenges have been discussed.
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References
Aberoumand A (2011) A review article on edible pigments properties and sources as natural biocolorants in foodstuff and food industry. World J Dairy Food Sci 6(1):71–78
Ahmad WA, Ahmad WYW, Zakaria ZA, Yusof NZ (2012) Application of bacterial pigments as colorant. In: Application of bacterial pigments as colorant. Springer, pp 57–74
Alihosseini F, Ju KS, Lango J, Hammock BD, Sun G (2008) Antibacterial colorants: characterization of prodiginines and their applications on textile materials. Biotechnol Prog 24(3):742–747
Andrighetti-Fröhner CR, Antonio RV, Creczynski-Pasa TB, Barardi CRM, Simões CMO (2003) Cytotoxicity and potential antiviral evaluation of violacein produced by Chromobacterium violaceum. Memórias do Instituto Oswaldo Cruz 98(6):843–848
Arun N, Singh D (2013) Differential response of Dunaliella salina and Dunaliella tertiolecta isolated from brines of Sambhar Salt Lake of Rajasthan (India) to salinities: a study on growth, pigment and glycerol synthesis. J Mar Biol Assoc India 55(1):65–70
August P, Grossman T, Minor C, Draper M, MacNeil I, Pemberton J, Call K, Holt D, Osburne M (2000) Sequence analysis and functional characterization of the violacein biosynthetic pathway from Chromobacterium violaceum. J Mol Microbiol Biotechnol 2(4):513–519
Asker D, Ohta Y (2002) Production of canthaxanthin by Haloferax alexandrinus under non-aseptic conditions and a simple, rapid method for its extraction. Appl Microbiol Biotechnol 58(6):743–750
Banerjee D, Chatterjee S, Banerjee U, Guha AK, Ray L (2011) Green Pigment from Bacillus cereus M116 (MTCC 5521): production parameters and antibacterial activity. Appl Biochem Biotechnol 164(6):767–779
Bohlke K, Spiegelman D, Trichopoulou A, Katsouyanni K, Trichopoulos D (1999) Vitamins A, C and E and the risk of breast cancer: results from a case-control study in Greece. Br J Cancer 79(1):23
Boo H-O, Hwang S-J, Bae C-S, Park S-H, Song W-S (2011) Antioxidant activity according to each kind of natural plant pigments. Korean J Plant Resour 24(1):105–112
Campas C, Dalmau M, Montaner B, Barragan M, Bellosillo B, Colomer D, Pons G, Pérez-Tomás R, Gil J (2003) Prodigiosin induces apoptosis of B and T cells from B-cell chronic lymphocytic leukemia. Leukemia 17(4):746–750
Carte BK (1996) Biomedical potential of marine natural products. Bioscience 46(4):271–286
Carreira A, Ferreira L, Loureiro V (2001a) Production of brown tyrosine pigments by the yeast Yarrowia lipolytica. J App Microbiol 90(3):372–379
Carreira A, Ferreira LM, Loureiro Vl (2001b) Brown pigments produced by Yarrowia lipolytica result from extracellular accumulation of homogentisic acid. Appl Environ Microbiol 67(8):3463–3468
Chandi GK, Gill BS (2011) Production and characterization of microbial carotenoids as an alternative to synthetic colors: a review. Int J Food Prop 14(3):503–513
Chávez R, Fierro F, García-Rico RO, Laich F (2011) Mold-fermented foods: Penicillium spp. as ripening agents in the elaboration of cheese and meat products. In: Mycofactories. Bentham Science Publishers Ltd.,
Chen M-T, Tseng Y-Y Efficacy of antimicrobial substances from Monascus metabolites on preservation of meat. In: 35. International Congress of Meat Science and Technology, Copenhagen (Denmark), 20–25 Aug 1989, 1989. SFI
Choi SY, Yoon K-h, Lee JI, Mitchell RJ (2015) Violacein: properties and production of a versatile bacterial pigment. BioMed research international 2015
Cragg GM, Newman DJ (1999) Discovery and development of antineoplastic agents from natural sources. Cancer Invest 17(2):153–163
Cserháti T (2006) Liquid chromatography of natural pigments and synthetic dyes, vol 71. Elsevier,
De Carvalho DD, Fabio TM, Costa, Duran N, Duran M (2006) Cytotoxic activity of violacein in human colon cancer cells. Toxicol in Vitro 20(8):1514–1521
Davoli P, Weber RW (2002) Carotenoid pigments from the red mirror yeast. Sporobolomyces roseus. Mycologist 16(3):102–108
Demain AL (1980) Microbial production of primary metabolites. Naturwissenschaften 67(12):582–587
Duerre JA, Buckley PJ (1965) Pigment production from tryptophan by an Achromobacter species. J Bacteriol 90(6):1686–1691
Dufossé L (2006) Microbial production of food grade pigments. Food Technology and Biotechnology 44(3):313–323
Duran M, Ponezi AN, Faljoni-Alario A, Teixeira MF, Justo GZ, Duran N (2012) Potential applications of violacein: a microbial pigment. Med Chem Res 21(7):1524–1532
S.editors B (2009) Microbial pigments. Biotechnology for agro-industrial residues, 8. Dodrdrecht. Springer
El-Banna AAE-R, El-Razek AMA, El-Mahdy AR (2012) Isolation, identification and screening of carotenoid-producing strains of Rhodotorula glutinis. Food Nutr Sci 3(05):627
Fenical W (1997) New pharmaceuticals from marine organisms. Trends Biotechnol 15(9):339–341
Ferreira CV, Bos CL, Versteeg HH, Justo GZ, Durán N, Peppelenbosch MP (2004) Molecular mechanism of violacein-mediated human leukemia cell death. Blood 104(5):1459–1464
Frandsen RJ, Nielsen NJ, Maolanon N, Sørensen JC, Olsson S, Nielsen J, Giese H (2006) The biosynthetic pathway for aurofusarin in Fusarium graminearum reveals a close link between the naphthoquinones and naphthopyrones. Mol Microbiol 61(4):1069–1080
Galaup P, Sutthiwong N, Leclercq-Perlat MN, Valla A, Caro Y, Fouillaud M, Guérard F, Dufossé L (2015) First isolation of Brevibacterium sp. pigments in the rind of an industrial red-smear-ripened soft cheese. Int J Dairy Technol 68(1):144–147
Gerber NN (1975) Prodigiosin-like pigments. CRC. Crit Rev Microbiol 3(4):469–485
Gerber NN, Gauthier M (1979) New prodigiosin-like pigment from Alteromonas rubra. Appl Environ Microbiol 37(6):1176–1179
Gupte M, Kulkarni P, Ganguli B (2002) Antifungal antibiotics. Appl Microbiol Biotechnol 58(1):46
Guyomarc’h F, Binet A, Dufossé L (2000) Production of carotenoids by Brevibacterium linens: variation among strains, kinetic aspects and HPLC profiles. J Ind Microbiol Biotechnol 24(1):64–70
Hendry GAF, Houghton J (1996) Natural food colorants. Springer Science & Business Media
Herz S, Weber RW, Anke H, Mucci A, Davoli P (2007) Intermediates in the oxidative pathway from torulene to torularhodin in the red yeasts Cystofilobasidium infirmominiatum and C. capitatum (Heterobasidiomycetes, Fungi). Phytochem 68(20):2503–2511
Hobson DKWD (1998) Green colorants. J Soc Dyers Colour 114:42–44
Houbraken J, Frisvad JC, Seifert K, Overy DP, Tuthill D, Valdez J, Samson R (2012) New penicillin-producing Penicillium species and an overview of section Chrysogena. Persoonia: Molecular Phylogeny and Evolution of Fungi 29:78
Howarth S, Dedman M (1964) Pigmentation Variants of Pseudomonas aeruginosa. J Bacteriol 88(2):273–278
Huang P (1964) Recombination and complementation of albino mutants in Neurospora. Genet 49(3):453
Ichiyama S, Shimokata K, Tsukamura M (1989) Carotenoid pigments of genus Rhodococcus. Microbiol Immunol 33(6):503–508
Johnson EA (2003) Phaffia rhodozyma: colorful odyssey. Int Microbiol 6(3):169–174
Johnson EA, Villa TG, Lewis MJ, Phaff HJ (1978) Simple method for the isolation of astaxanthin from the basidiomycetous yeast Phaffia rhodozyma. Appl Environ Microbiol 35(6):1155–1159
Joshi V, Attri D, Bala A, Bhushan S (2003) Microbial pigments. Indian J Biotechnol 2(362):9
Katsube N, Iwashita K, Tsushida T, Yamaki K, Kobori M (2003) Induction of apoptosis in cancer cells by bilberry (Vaccinium myrtillus) and the anthocyanins. J Agric Food Chem 51(1):68–75
Kawauchi K, Shibutani K, Yagisawa H, Kamata H, Nakatsuji S, Anzai H, Yokoyama Y, Ikegami Y, Moriyama Y, Hirata H (1997) A Possible Immunosuppressant, Cycloprodigiosin Hydrochloride, Obtained from Pseudoalteromonas denitrificans. Biochem Biophys Res Commun 237(3):543–547
Khaneja R, Perez-Fons L, Fakhry S, Baccigalupi L, Steiger S, To E, Sandmann G, Dong T, Ricca E, Fraser P (2010) Carotenoids found in Bacillus. J Applied Microbiol 108(6):1889–1902
Kim H-S, Hayashi M, Shibata Y, Wataya Y, Mitamura T, Horii T, Kawauchi K, Hirata H, Tsuboi S, Moriyama Y (1999) Cycloprodigiosin hydrochloride obtained from Pseudoalteromonas denitrificans is a potent antimalarial agent. Biol Pharm Bull 22(5):532–534
Kim H, Han S, Lee C, Lee K, Park S, Kim Y (2003) Use of prodigiosin for treating diabetes mellitus. Google Patents
Kim C, Jung H, Kim JH, Shin CS (2006) Effect of monascus pigment derivatives on the electrophoretic mobility of bacteria, and the cell adsorption and antibacterial activities of pigments. Colloids Surf B 47(2):153–159
Kim D, Lee J, Park Y, Kim J, Jeong H, Oh TK, Kim B, Lee C (2007) Biosynthesis of antibiotic prodiginines in the marine bacterium Hahella chejuensis KCTC 2396. J Appl Microbiol 102(4):937–944
Kim HW, Kim JB, Cho SM, Chung MN, Lee YM, Chu SM, Che JH, Kim SN, Kim SY, Cho YS (2012) Anthocyanin changes in the Korean purple-fleshed sweet potato, Shinzami, as affected by steaming and baking. Food Chem 130(4):966–972
Kodach LL, Bos CL, Durán N, Peppelenbosch MP, Ferreira CV, Hardwick JC (2005) Violacein synergistically increases 5-fluorouracil cytotoxicity, induces apoptosis and inhibits Akt-mediated signal transduction in human colorectal cancer cells. Carcinog 27(3):508–516
Kodach LL, Bos CL, Durán N, Peppelenbosch MP, Ferreira CV, Hardwick JC (2006) Violacein synergistically increases 5-fluorouracil cytotoxicity, induces apoptosis and inhibits Akt-mediated signal transduction in human colorectal cancer cells. Carcinogenesis 27(3):508–516
Koes RE, Quattrocchio F, Mol JN (1994) The flavonoid biosynthetic pathway in plants: function and evolution. BioEssays 16(2):123–132
Kong J-M, Chia L-S, Goh N-K, Chia T-F, Brouillard R (2003) Analysis and biological activities of anthocyanins. Phytochemistry 64(5):923–933
Konuray G, Erginkaya Z (2015) Antimicrobial and antioxidant properties of pigments synthesized from microorganisms. The Battle Against Microbial Pathogens: Basic Science, Technological Advances and Educational Programs (A Méndez-Vilas, Ed) FORMATEX:27-33
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
Korkina L (2007) Phenylpropanoids as naturally occurring antioxidants: from plant defense to human health. Cell Mol Biol 53(1):15–25
Krishnamurthy K, Siva R, Senthil T (2002) Natural dye-yielding plants of Shervaroy Hills of Eastern Ghats. In: Proceedings of National Seminar on the Conservation of the Eastern Ghats, Environment Protection Training and Research Institute, Hyderabad, pp 24–26
Lazzè MC, Savio M, Pizzala R, Cazzalini O, Perucca P, Scovassi AI, Stivala LA, Bianchi L (2004) Anthocyanins induce cell cycle perturbations and apoptosis in different human cell lines. Carcinogenesis 25(8):1427–1433
Lazaro J, Nitcheu J, Predicala RZ, Mangalindan GC, Nesslany F, Marzin D, Concepcion GP, Diquet B (2002) Heptyl prodigiosin, a bacterial metabolite, is antimalarial in vivo and non-mutagenic in vitro. J Nat Toxins 11(4):367–377
Leon LL, Machado GM, de Carvalho Paes LE, Grimaldi G (1990) Antigenic differences of Leishmania amazonensis isolates causing diffuse cutaneous leishmaniasis. Trans R Soc Trop Med Hyg 84(5):678–680
Leon LL, Machado G, Barral A, Carvalho-Paes LEd, Grimaldi Júnior G (1992) Antigenic differences among Leishmania amazonensis isolates and their relationship with distinct clinical forms of the disease. Memórias do Instituto Oswaldo Cruz 87(2):229–234
Leon L, Miranda C, De Souza A, Durán N (2001) Antileishmanial activity of the violacein extracted from Chromobacterium violaceum. J Antimicrob Chemother 48(3):449–450
Li JW-H, Vederas JC (2009) Drug discovery and natural products: end of an era or an endless frontier? Science 325(5937):161–165
Lichstein HC, Van De Sand VF (1946) The antibiotic activity of violacein, prodigiosin, and phthiocol. J Bacteriol 52(1):145
Lin J, Yan XJ, Zheng L, Ma HH, Chen HM (2005) Cytotoxicity and apoptosis induction of some selected marine bacteria metabolites. J Appl Microbiol 99(6):1373–1382
Lowe SW, Lin AW (2000) Apoptosis in cancer. Carcinogenesis 21(3):485–495
Malik K, Tokkas J, Goyal S (2012) Microbial pigments: a review. Int J Microbial Res Technol 1(4):361–365
Mapari SA, Nielsen KF, Larsen TO, Frisvad JC, Meyer AS, Thrane U (2005) Exploring fungal biodiversity for the production of water-soluble pigments as potential natural food colorants. Curr Opin Biotechnol 16(2):231–238
Mapari SA, Meyer AS, Thrane U, Frisvad JC (2009) Identification of potentially safe promising fungal cell factories for the production of polyketide natural food colorants using chemotaxonomic rationale. Microb Cell Fact 8(1):24
Martin S, Giannone G, Andriantsitohaina R, Carmen Martinez M (2003) Delphinidin, an active compound of red wine, inhibits endothelial cell apoptosis via nitric oxide pathway and regulation of calcium homeostasis. Br J Pharmacol 139(6):1095–1102
Matz C, Deines P, Boenigk J, Arndt H, Eberl L, Kjelleberg S, Jürgens K (2004) Impact of violacein-producing bacteria on survival and feeding of bacterivorous nanoflagellates. Appl Environ Microbiol 70(3):1593–1599
McConkey DJ, Zhivotovsky B, Orrenius S (1996) Apoptosis—molecular mechanisms and biomedical implications. Mol Aspects Med 17(1):1517396771–315376569110
Mellouli L, Ameur-Mehdi RB, Sioud S, Salem M, Bejar S (2003) Isolation, purification and partial characterization of antibacterial activities produced by a newly isolated Streptomyces sp. US24 strain. Res Microbiol 154(5):345–352
Miller M, Yoneyama M, Soneda M (1976) Phaffia, a new yeast genus in the Deuteromycotina (Blastomycetes). Int J Syst Evol Microbiol 26(2):286–291
Mohana DC, Thippeswamy S, Abhishek RU (2013) Antioxidant, antibacterial, and ultraviolet-protective properties of carotenoids isolated from Micrococcus spp. Radiation Prot Environ 36(4):168
Mukherjee G, Singh SK (2011) Purification and characterization of a new red pigment from Monascus purpureus in submerged fermentation. Process Biochem 46(1):188–192
Nagpal N, Munjal N, Chatterjee S (2011) Microbial pigments with health benefits-A mini review. Trends Biosci 4(2):157–160
Nakamura Y, Sawada T, Morita Y, Tamiya E (2002) Isolation of a psychrotrophic bacterium from the organic residue of a water tank keeping rainbow trout and antibacterial effect of violet pigment produced from the strain. Biochem Eng J 12(1):79–86
Nuijen B, Bouma M, Manada C, Jimeno J, Schellens JH, Bult A, Beijnen J (2000) Pharmaceutical development of anticancer agents derived from marine sources. Anticancer Drugs 11(10):793–811
Palanichamy V, Hundet A, Mitra B, Reddy N (2011) Optimization of cultivation parameters for growth and pigment production by Streptomyces spp. isolated from marine sediment and rhizosphere soil. Int J Plant Animal Env Sci 1(3):158–170
Pandey RC, Sainis Ramesh, Krishna B (2007) Prodigiosins: a novel family of immunosuppressants with anti-cancer activity. Indian J Biochem Biophys 44(5):295–302
Parajó J, Santos V, Vázquez M (1998) Optimization of carotenoid production by Phaffia rhodozyma cells grown on xylose. Process Biochem 33(2):181–187
PDS Melo, Maria SS, Vidal BDC, Haun M, Durán N (2000) Violacein cytotoxicity and induction of apoptosis in V79 cells. Vitro Cellular & Developmental Biology-Animal 36(8):539–543
Radjasa OK, Limantara L, Sabdono A (2009) Antibacterial activity of a pigment producing-bacterium associated with Halimeda sp. from eland-locked marine lake kakaban, Indonesia. J Coast Dev 12(2):100–104
Rashid M, Fakruddin M, Mazumdar RM, Kaniz F, Chowdhury M (2014) Anti-bacterial activity of pigments isolated from pigment-forming soil bacteria
Richard C (1992) Chromobacterium violaceum, opportunist pathogenic bacteria in tropical and subtropical regions. Bull Soc Pathol Exot (1990) 86(3):169–173
Sánchez C, Braña AF, Méndez C, Salas JA (2006) Reevaluation of the violacein biosynthetic pathway and its relationship to indolocarbazole biosynthesis. ChemBioChem 7(8):1231–1240
Saraiva VS, Marshall JC, Cools-Lartigue J, Burnier Jr MN (2004) Cytotoxic effects of violacein in human uveal melanoma cell lines. Melanoma Res 14(5):421–424
Schwartsmann G, Brondani A, Berlinck R, Jimeno J (2000) Marine organisms and other novel natural sources of new cancer drugs. Ann Oncol 11(3):235–243
Schwartsmann G, da Rocha AB, Berlinck RG, Jimeno J (2001) Marine organisms as a source of new anticancer agents. Lancet Oncol 2(4):221–225
Shirata A, Tsukamoto T, Yasui H, Hata T, Hayasaka S, Kojima A, Kato H (2000) Isolation of bacteria producing bluish-purple pigment and use for dyeing. JARQ (Japan)
Singh M, Kumar A, Singh R, Pandey KD (2017) Endophytic bacteria: a new source of bioactive compounds. 3. Biotech 7(5):315
Soliev AB, Hosokawa K, Enomoto K (2011) Bioactive pigments from marine bacteria: applications and physiological roles. Evidence-Based Complementary and Alternative Medicine 2011
Sowbhagya H, Chitra V (2010) Enzyme-assisted extraction of flavorings and colorants from plant materials. Crit Rev Food Sci Nutr 50(2):146–161
Suresh M, Renugadevi B, Brammavidhya S, Iyapparaj P, Anantharaman P (2015) Antibacterial activity of red pigment produced by halolactibacillus alkaliphilus MSRD1—an isolate from seaweed. Appl Biochem Biotechnol 176(1):185–195
Taylor MW, Radax R, Steger D, Wagner M (2007) Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol Mol Biol Rev 71(2):295–347
Umadevi K, Krishnaveni M (2013) Antibacterial activity of pigment produced from Micrococcus luteus KF532949. Int J Chem Anal Sci 4(3):149–152
Ungureanu C, Ferdes M (2012) Evaluation of antioxidant and antimicrobial activities of torularhodin. Adv Sci Lett 18(1):50–53
Venil CK, Lakshmanaperumalsamy P (2009) An insightful overview on microbial pigment, prodigiosin. Electron J Biol 5(3):49–61
Venil CK, Zakaria ZA, Ahmad WA (2013) Bacterial pigments and their applications. Process Biochem 48(7):1065–1079
Wang J, Mazza G (2002) Effects of anthocyanins and other phenolic compounds on the production of tumor necrosis factor α in LPS/IFN-γ-activated RAW 264.7 macrophages. J Agric Food Chem 50(15):4183–4189
Yadav S, Manjunatha K, Ramachandra B, Suchitra N, Prabha R (2014) Characterization of pigment producing rhodotorula from dairy environmental samples. Asian J Dairying & Foods Res 33(1):1–4
Yamamoto C, Takemoto H, Kuno K, Yamamoto D, Tsubura A, Kamata K, Hirata H, Yamamoto A, Kano H, Seki T (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
Youdim KA, McDonald J, Kalt W, Joseph JA (2002) Potential role of dietary flavonoids in reducing microvascular endothelium vulnerability to oxidative and inflammatory insults. J Nutr Biochem 13(5):282–288
Zhang H, Zhan J, Su K, Zhang Y (2006) A kind of potential food additive produced by Streptomyces coelicolor: characteristics of blue pigment and identification of a novel compound, λ-actinorhodin. Food Chem 95(2):186–192
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Numan, M., Bashir, S., Mumtaz, R. et al. Therapeutic applications of bacterial pigments: a review of current status and future opportunities. 3 Biotech 8, 207 (2018). https://doi.org/10.1007/s13205-018-1227-x
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DOI: https://doi.org/10.1007/s13205-018-1227-x