International Journal of Microbial Resource Technology ©2012 INPRESSCO. All Rights Reserved. Available at http://ijmrt.inpressco.com
ISSN 2278 – 3822
Review Article
Microbial Pigments: A review Kamla Malik*, Jayanti Tokkas1 and Sneh Goyal Department of Microbiology Department of Biochemistry College of Basic Sciences & Humanities CCS HAU, Hisar-125004, Haryana, India 1
*E-mail:
[email protected]:
[email protected]
Accepted 4 Nov. 2012, Available online 1 Dec. 2012, Vol.1, No. 4 (Dec. 2012)
Abstract In last few decades, there has been an increasing trend towards replacement of synthetic colorants with natural pigments because of the strong consumer demand for more natural products. Natural pigments and synthetic dyes have been extensively used in various fields of everyday life such as food production, textile industries, paper production, agricultural practices and researches, water science and technology. Natural pigments not only have the capacity to increase the marketability of products, they also display advantageous biological activities as antioxidants and anticancer agents. On the other hand, synthetic pigments cause considerably environmental pollution and adverse toxicological side effects. It is therefore, essential to explore various natural sources of food grade colorants and their use potentials. Use of microbial pigments in processed food is an area of promise with large economic potential. However, microbial pigments offer challenges due to high cost, lower stability and variation in shades due to changes in pH. Keywords: Microorganism, pigment, food, colour, natural
1. Introduction Color of a food substance is important to indicate its freshness and safety that are also indices of good aesthetic and sensorial values. In the recent years, coloring of food with pigments produced from natural sources is of worldwide interest and is gaining importance. These pigments are looked upon for their safe use as a natural food dye in replacement of synthetic ones because of undesirable market. A well textured food, rich in nutrients and flavor, can not be eaten unless it has the right color. The demand for natural source of such compounds is increasing day by day because of the awareness of positive health benefits out of natural compounds. It is therefore, essential to explore various natural sources of food grade colorants and their potentials. Though many natural colors are available, microbial colorants play a significant role as food coloring agent, because of its production and easy down streaming process. Industrial production of natural food colorants by microbial fermentation has several advantages such
as cheaper production, easier extraction, higher yields through strain improvement, no lack of raw materials and no seasonal variations. Pigments are compounds with characteristics of importance to many industries. In the food industry they are used as additives, color intensifiers, antioxidants, etc. Pigments come in a wide variety of colors, some of which are watersoluble (Tibor, 2007). Microorganisms are the most powerful creatures in existence and determine the life and death on this planet. Microorganisms are associated with all the foods that we eat and are responsible for the formation of certain food products by the process of fermentation and can also be used as a source of food in the form of single cell proteins and food supplements in the form of pigments, amino acids, vitamins, organic acids, and enzymes. In this way the pigments from microbial sources are a good alternative. Microorganisms are known to produce a variety of pigments; therefore they are promising source of food colorants (Aberoumand, 2011 and
361
Malik et al.
Ahmad, 2012). Most of the bacteria and fungi are widely studied for their potential as a source of food colorants. Natural pigments possess anticancer activity, contain pro-vitamin A and have some desirable properties like stability to light, heat and pH (Joshi et al., 2003). Thus, the food industry has become increasingly interested in the use of microbial technology to produce colors for use in foods. It can also help to overcome the growing public concern over the adverse health effects of addition of synthetic colors in food products. Furthermore, natural colorants will not only be beneficial to the health of human beings, but it will be a boon for the preservation of biodiversity as harmful chemicals released into the environment while producing synthetic colorants could be stopped. These natural colorants are used in baby foods, breakfast cereals, pastas, sauces, processed cheese, fruit drinks, vitamin-enriched milk products, and some energy drinks. Thus, natural colors in addition to being environment friendly, can also serve the dual need for visually appealing colors and probiotic health benefits in food products (Nagpal et al., 2011). In this review, we have summarized the current understanding of microbial pigments and their potential application in the industries.
International J. Microbial Resource Technol. ISSN 2278 – 3822
Heamatococcus pluvialis. Astaxanthin production using Agrobacterium aurantiacum has been investigated to a lesser extent as compared to Xanthophyllomyces dendrorhous (Golubev, 1995). A fungus strain Penicillium oxalicum with the properties to produce a red colorant can be applied in food and cosmetic industries (Sardaryan et al., 2004). 3. Classification of pigments
1.
2. 2. Pigment produced by Microorganisms Some of the most important natural pigments are cartenoids, flavonoids, tetrapirroles and some xantophylls as astaxanthin. The pigment most commonly used in industries is beta-carotene which is obtained from some microalgae and cyanobacteria. Astaxanthin obtained from phaffia rohodozoa and Haematococcus pluviais, is a red pigment of great commercial value and is used in feed, pharmaceutical and aquaculture industries. Micro-organisms which have the ability to produce pigments in high yields include species of Monascus, Paecilomyces, Serratia, Cordyceps, Streptomyces and yellow-red and blue compounds produced by Penicillium herquei and Penicillium atrovenetum, Rhodotorula, Sarcina, Cryptococcus, Monascus purpureus, Phaffia rhodozyma, Bacillus sp., Achromobacter, Yarrowia and Phaffia also produce a large number of pigments (Table 1). Monascus species, fungi which produce monascus pigments, have long been used in production of traditional East Asian foods such as red rice wine and red bean curd (Mohankumari et al., 2009). Natural astaxanthin from microorganisms is mainly supplied by the red basidiomycetous yeast Xanthophyllomyces dendrorhous and the green algae
3.
4.
Pigments are classified as either organic/inorganic or natural/synthetic. Biological pigments can be classified based on structural affinities and natural occurrence. Some examples of naturally occurring pigments are: Riboflavin is a yellow water-soluble vitamin produced by many micro-organisms. Traditional chemical synthesis of riboflavin is now being replaced by commercially competitive biotechnological processes using ascomycetes Ashbya gossypii, filamentous fungi Candida famata, or bacterium Bacillus subtilis (Stahmann et al., 2000). It is used in baby foods, breakfast cereals, pastas, sauces, processed cheese, fruit drinks, vitamin-enriched milk products, and some energy drinks. Beta-carotene: Phycomyces and Mucor circinelloides (wild type) are a potential source of beta-carotene. The European Union Committee considers that betacarotene produced by fermentation of Blakeslea trispora is equivalent to the chemically synthesized material used as food colorant and is therefore acceptable for use as a coloring agent in foodstuffs (European Commission, 2000). Canthaxanthin is produced as the major carotenoid pigment by orange- and dark pink-pigmented bacteriochlorophyll-containing Bradyrhizobium (photosynthetic) strains isolated from stem nodules of Aeschynomene species and Halobacterium spp. Canthaxanthins are potent antioxidants and inhibit the oxidation of lipids in liposomes. Carotenoids are yellow to orange-red pigments that are ubiquitous in nature. A number of microorganisms produce this pigment such as Serratia and Streptomyces. Carotenoids are effective antioxidants and are widely used as food colorants. Majority of microbes reported produce carotenoids belonging to Myxococcus (Browning et al., 2003), Streptomyces (Takano et al., 2005), Mycobacterium, Agrobacterium (Yokoyama et al., 1994) and Sulfolobus (Kull and Pfander, 1997).
362
International Journal of Microbial Resource Technology ©2012 INPRESSCO. All Rights Reserved. Available at http://ijmrt.inpressco.com
ISSN 2278 – 3822
Table 1. List of pigment producing microorganisms. Microorganism(s) Bacteria Agrobacterium aurantiacum Paracoccus carotinifaciens Bradyrhizobium sp. Flavobacterium sp., Paracoccus zeaxanthinifaciens Achromobacter Bacillus Brevibacterium sp. Corynebacterium michigannise Corynebacterium insidiosum Rugamonas rubra , Streptoverticillium rubrireticuli,Vibrio gaogenes, Alteromonas rubra Rhodococcus maris Xanthophyllomyces dendrorhous Haloferax alexandrinus Staphylococcus aureus Chromobacterium violaceum Serratia marcescens, Serratia rubidaea, Pseudomonas aeruginosa Xanthomonas oryzae Janthinobacterium lividum
Pigments/Molecule
Colour/appearance
Astaxanthin Astaxanthin Canthaxanthin Zeaxanthin
Indigoidine Prodigiosin
Pink-red Pink-red Dark- red yellow Creamy Brown Orange yellow Greyish to creamish Blue Red
Astaxanthin Canthaxanthin Staphyloxanthin Zeaxanthin Violacein Prodigiosin Pyocyanin Xanthomonadin Violacein
Bluish- red Pink -red Dark Red Golden Yellow Purple Red Blue-green Yellow Purple
Algae Dunaliella salina Chlorococcum Hematococcus
β-carotene Lutein Canthaxanthin
Red
Fungi Aspergillus sp. Aspergillus galucus Blakeslea trispora Helminthosporium catenarium Helminthosporium avenae Penicilllum cyclopium Penicilllum nalgeovensis Fusarium sporotrichioides Haematococcus Pluvialis Monascus sp. Monascus purpureus Monascus roseus Monascus sp. Penicillium oxalicum Blakeslea trispora Cordyceps unilateralis Ashbya gossypi Mucor circinelloides, Neurospora crassa and Phycomyces blakesleeanus Penicillium purpurogenum , Paecilomyces sinclairii Pacilomyces farinosus
Lycopene Astaxanthin Monascorubramin Rubropunctatin Monascin Ankaflavin Canthaxanthin Ankaflavin Anthraquinone Lycopene Naphtoquinone Riboflavin β-carotene
Orange-red Dark -red Cream Red Bronze Orange Yellow Red Red Red Orange Red-yellow Orange-Pink Yellow Red Red Deep blood-red Yellow Yellow-orange
Anthraquinone
Red Red
Astaxanthin Torularhodin -
Red Melanin black Pink-red Orange-red Brown
Prodigiosin Rubrolone
Red Red
β -carotene
Yeast Cryptococus sp. Saccharomyces neoformans var. nigricans Phaffia rhodozyma Rhodotorula sp. Rhodotorula glutinis Yarrowia lipolytica
Actinomycetes Streptoverticillium rubrireticuli Streptomyces echinoruber
363
Malik et al.
5.
6.
7.
8.
Prodigiosin is a multipurpose red pigment, produced by various microorganisms such as Serratia marcescens, Vibrio psychoerythrus, Rugamonas rubra, actinomycetes, such as Streptoverticillium rubrireticuli and other eubacteria (Khanafari et al., 2006). It is known to have antibacterial, anti-malarial, antineoplastic and antibiotic activity. Phycocyanin is a blue pigment, produced by cyanobacteria which contain chlorophyll a. The blue colorant is known by the name spirulina (blue green alga), which is also the name of a dietary supplement rich in proteins and consists of dried cyanobacteria. Violacein is a versatile pigment from a bacterium Chromobacterium violaceum that exhibits several biological activities. It has gained increasing importance in industrial markets, such as in medicine, cosmetics, food and textiles. Astaxanthin (3, 3’-dihydroxy-b, b-carotene-4, 4’dione) is a orange- red pigment and produced by microorganisms such as red basidiomycetous yeast Xanthophyllomyces dendrorhous (Golubev, 1995), green algae Heamatococcus pluvialis, Agrobacterium aurantiacum and Xanthophyllomyces dendrorhous.
International J. Microbial Resource Technol. ISSN 2278 – 3822
4.
5.
6.
7.
8.
9.
4. Challenges and scope 10. Thus there is an urgent need for alternative colorants that are natural, cost effective and easily degradable and without production of recalcitrant intermediates when they enter the ecosystem. There is an increasing interest involving microorganisms as a possible alternate source of colorants used in food industry. In this direction, biotechnology may play a crucial role for large fermentation of natural biocolorants.
11.
References 12. 1.
2.
3.
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, W.A., Ahmad, W.Y.W., Zakaria Z.A. and Yusof, N.Z. (2012). Application of Bacterial Pigments as Colorant. Springer Briefs in Molecular Science, pp 57-74. Browning, D.F., Whitworth, D.E. and Hodgson, D.A. (2003). Light induced carotenogenesis in Myxococcus xanthus: Functional characterization of the ECF sigma factor CarQ and antisigma factor CarR. Mol. Microbiol., 48: 237–251.
13.
European Commission (2000). Opinion of the Scientific Committee on Food on betacarotene from Blakeslea trispora (SCF/CS/ADD/COL) pp 158. Golubev, W.I. (1995). Perfect state of Rhodomyces dendrorhous (Phaffia rhodozyma). Yeast, 11: 101-110. Joshi, V.K., Attri, D., Bala, A. and Bhushan, S. (2003). Microbial Pigments. Indian J. Biotech., 2: 362-369. Khanafari, A., Assadi, M.M. and Fakhr, F.A. (2006). Review of prodigiosin, pigmentation in Serratia marcescens. J. Biol. Sci., 6: 1-13. Kull, D.R. and Pfander, H. (1997). Isolation and structure elucidation of carotenoid glycosides from the thermoacidophilic archaea Sulfolobus shibatae. J. Nat. Prod., 60:371–374. Mohankumari, H.P., Naidu, A., Vishwanatha, S., Narasimhamurthy, K. and Vijayalakshmi, G. (2009). Safety evaluation of Monascus purpureus red mould rice in albino rats. Food Chem. Toxicol., 47: 17391746. Nagpal, N., Munjal, N. and Chatterjee, S. (2011). Microbial Pigments with Health Benefits - A Mini Review. Trends Biosci, 4: 157-160. Sardaryan, H., Zihlova, R., Strnad, Z. and Cermakoya, C. (2004). Arpink Red– Meet a new natural red food colorant of microbial origin. In: Pigments in Food, More than Colours. L. Dufossé (ed) Université de Bretagne Occidentale, Quimper France, pp 207-208. Stahmann, K.P., Revuelta, J.L. and Seulberger, H. (2000). Three biotechnical processes using Ashbya gossypii, Candida famata, or Bacillus subtilis compete with chemical riboflavin production. Appl. Microbiol. Biotech., 53: 509–516. Takano, H., Obitsu, S., Beppu, T. and Ueda, K. (2005). Light-induced carotenogenesis in Streptomyces coelicolor A3 (2): Identification of an extracytoplasmic function sigma factor that directs photodependent transcription of the carotenoid biosynthesis gene cluster. J. Bacteriol., 187: 1825–1832.
364
Malik et al.
14. Tibor, C. (2007). Liquid Chromatography of Natural pigments and synthetic dyes. J. Chromatography Library, 71: 11-19.
International J. Microbial Resource Technol. ISSN 2278 – 3822
15. Yokoyama, A.H., Izumida, I., and Miki, W. (1994). Production of astaxanthin and 4ketozeaxanthin by the marine bacterium Agrobacterium aurantiacum. Biosci Biotechnol. Biochem., 58: 1842–1844.
365
