Microorganisms and microalgae as sources of pigments for food use: a scientific oddity or an industrial reality?

Pigments producing microorganisms and microalgae are quite common in Nature. However, there is a long way from the Petri dish to the market place. Five productions, using Monascus, Penicillium, Dunaliella, Haematococcus and Porphyridium, are discussed. Some companies invested a lot of money as any combination of new source and/or new pigment drives a lot of experimental work, process optimization, toxicological studies and regulatory issues. Time will tell whether investments were cost-effective. Future trends involve combinatorial engineering and production of niche pigments not found in plants.

[1]  R. Watson,et al.  Beta‐Carotene Stimulates Human Leukocytes to Secrete a Novel Cytokine , 1989, Journal of leukocyte biology.

[2]  D. Albanes,et al.  Effects of supplemental beta-carotene, cigarette smoking, and alcohol consumption on serum carotenoids in the Alpha-Tocopherol, Beta-Carotene Cancer Prevention Study. , 1997, The American journal of clinical nutrition.

[3]  T. Rees,et al.  Algal and cyanobacterial biotechnology , 1989 .

[4]  O. Halevy,et al.  Inhibition of arachidonic acid oxidation by β-carotene, retinol and α-tocopherol , 1987 .

[5]  D M Snodderly,et al.  Evidence for protection against age-related macular degeneration by carotenoids and antioxidant vitamins. , 1995, The American journal of clinical nutrition.

[6]  M. Borowitzka,et al.  Culture of the astaxanthin-producing green algaHaematococcus pluvialis 1. Effects of nutrients on growth and cell type , 1991, Journal of Applied Phycology.

[7]  K. Yeum,et al.  Carotenoid bioavailability and bioconversion. , 2003, Annual review of nutrition.

[8]  H. Iizuka,et al.  Production of Extracellular Pigment by a Mutant of Monascus kaoliang sp. nov , 1982, Applied and environmental microbiology.

[9]  M. Pike,et al.  Diet and colon cancer in Los Angeles County, California , 1992, Cancer Causes & Control.

[10]  H. Wong,et al.  Pigmentation and Antibacterial Activity of Fast Neutron- and X-Ray-induced Strains of Monascus purpureus Went. , 1977, Plant physiology.

[11]  G. Goma,et al.  A new process for red pigment production by submerged culture of Monascus purpureus , 1997 .

[12]  F. Guyomarc'h,et al.  Production of carotenoids by Brevibacterium linens: variation among strains, kinetic aspects and HPLC profiles , 2000, Journal of Industrial Microbiology and Biotechnology.

[13]  M. Johns,et al.  Effect of pH and nitrogen source on pigment production by Monascus purpureus , 2004, Applied Microbiology and Biotechnology.

[14]  F. Rancan,et al.  Singlet oxygen quenching by dietary carotenoids in a model membrane environment. , 2003, Archives of biochemistry and biophysics.

[15]  Gokare A. Ravishankar,et al.  Influence of stress on astaxanthin production in Haematococcus pluvialis grown under different culture conditions , 2002 .

[16]  A. Hara,et al.  Suppression of azoxymethane-induced rat colon carcinogenesis by dietary administration of naturally occurring xanthophylls astaxanthin and canthaxanthin during the postinitiation phase. , 1995, Carcinogenesis.

[17]  G. Goma,et al.  Pigments of Monascus , 1994 .

[18]  J. Frisvad,et al.  Exploring fungal biodiversity for the production of water-soluble pigments as potential natural food colorants. , 2005, Current opinion in biotechnology.

[19]  A. Zamir,et al.  Photoinduction of Massive beta-Carotene Accumulation by the Alga Dunaliella bardawil: Kinetics and Dependence on Gene Activation. , 1990, Plant physiology.

[20]  C. Schmidt-Dannert,et al.  Identification of a carotenoid oxygenase synthesizing acyclic xanthophylls: combinatorial biosynthesis and directed evolution. , 2005, Chemistry & biology.

[21]  A. Ben‐Amotz,et al.  ACCUMULATION OF β‐CAROTENE IN HALOTOLERANT ALGE: PURIFICATION AND CHARACTERIZATION OF β‐CAROTENE‐RICH GLOBULES FROM DUNALIELLA BARDAWIL (CHLOROPHYCEAE) 1 , 1982 .

[22]  O. Torrissen,et al.  Growth and survival of Atlantic salmon, Salmo salar L. fed different dietary levels of astaxanthin. Juveniles , 1996 .

[23]  M. Mathews-Roth.  Antitumor Activity of β-Carotene, Canthaxanthin and Phytoene , 1982 .

[24]  T. Storebakken.  Krill as a potential feed source for salmonids , 1988 .

[25]  L. Kolonel,et al.  Vegetable and fruit consumption in relation to prostate cancer risk in Hawaii: a reevaluation of the effect of dietary beta-carotene. , 1991, American journal of epidemiology.

[26]  M. Maudet,et al.  Vitamin A status and metabolism of cutaneous polyamines in the hairless mouse after UV irradiation: action of beta-carotene and astaxanthin. , 1995, International journal for vitamin and nutrition research. Internationale Zeitschrift fur Vitamin- und Ernahrungsforschung. Journal international de vitaminologie et de nutrition.

[27]  J. François,et al.  Biosynthetic Pathway of Citrinin in the Filamentous Fungus Monascus ruber as Revealed by 13C Nuclear Magnetic Resonance , 1999, Applied and Environmental Microbiology.

[28]  R. Good,et al.  Studies of immunomodulating actions of carotenoids. I. Effects of beta-carotene and astaxanthin on murine lymphocyte functions and cell surface marker expression in in vitro culture system. , 1991, Nutrition and cancer.

[29]  G Goma,et al.  Characterization of monascidin A from Monascus as citrinin. , 1995, International journal of food microbiology.

[30]  G. Goma,et al.  Production and food applications of the red pigments of Monascus ruber , 1993 .

[31]  Shiro Nagai,et al.  Astaxanthin production by a green alga, Haematococcus pluvialis accompanied with morphological changes in acetate media , 1991 .

[32]  A. Glazer,et al.  Subunit structure and chromophore composition of rhodophytan phycoerythrins. Porphyridium cruentum B-phycoerythrin and b-phycoerythrin. , 1977, The Journal of biological chemistry.

[33]  W. Miki,et al.  Biological functions and activities of animal carotenoids , 1991 .

[34]  R. Willson,et al.  Stimulation of microsomal lipid peroxidation by iron and cysteine. Characterization and the role of free radicals. , 1983, The Biochemical journal.

[35]  K. F. Finney,et al.  Use of algae dunaliella as a protein supplement in bread , 1984 .

[36]  J. Freudenheim,et al.  Nutritional epidemiology of postmenopausal breast cancer in western New York. , 1991, American journal of epidemiology.

[37]  S. Weitzman,et al.  Phagocytes as carcinogens: malignant transformation produced by human neutrophils. , 1985, Science.

[38]  G. An,et al.  Isolation of Phaffia rhodozyma Mutants with Increased Astaxanthin Content , 1989, Applied and environmental microbiology.

[39]  P. Sabuquillo,et al.  Biocontrol of Fusarium and Verticillium Wilt of Tomato by Penicillium oxalicum under Greenhouse and Field Conditions , 2003 .

[40]  J. Weststrate,et al.  Amount of fat in the diet affects bioavailability of lutein esters but not of α-carotene, β-carotene, and vitamin E in humans , 2000 .

[41]  G. Goma,et al.  Medium-Chain Fatty Acids Affect Citrinin Production in the Filamentous Fungus Monascus ruber , 2000, Applied and Environmental Microbiology.

[42]  A. Abramovici,et al.  The safety evaluation of Dunaliella bardawil as a potential food supplement. , 1989, Food and chemical toxicology : an international journal published for the British Industrial Biological Research Association.

[43]  A. Otero,et al.  Two-stage cultures for the production of astaxanthin from Haematococcus pluvialis. , 2001, Journal of biotechnology.

[44]  T. Sommer,et al.  Utilization of microalgal astaxanthin by rainbow trout (Oncorhynchus mykiss) , 1991 .

[45]  J. Schwartz,et al.  Beta carotene is associated with the regression of hamster buccal pouch carcinoma and the induction of tumor necrosis factor in macrophages. , 1986, Biochemical and biophysical research communications.

[46]  L. Dufossé,et al.  Assessment of the coloring strength of brevibacterium linens strains: spectrocolorimetry versus total carotenoid extraction/quantification. , 2001, Journal of dairy science.

[47]  M. Banerjee,et al.  Beta-carotene inhibition of 7,12-dimethylbenz[a]anthracene-induced transformation of murine mammary cells in vitro. , 1984, Carcinogenesis.

[48]  Goma,et al.  Improvement of red pigment/citrinin production ratio as a function of environmental conditions by monascus ruber , 1999, Biotechnology and bioengineering.

[49]  Z. Cohen,et al.  Chemicals from Microalgae , 1999 .

[50]  R. Watson,et al.  Effects of Retinoids on Human Lymphocyte Functions in vitro , 1985, Human toxicology.

[51]  K. Prasad,et al.  Beta-carotene induces morphological differentiation and decreases adenylate cyclase activity in melanoma cells in culture. , 1990, Journal of the American College of Nutrition.

[52]  D. Albanes,et al.  Effect of α-tocopherol and β-carotene supplementation on coronary heart disease during the 6-year post-trial follow-up in the ATBC study , 2004 .

[53]  S. Arad,et al.  Natural pigments from red microalgae for use in foods and cosmetics , 1992 .

[54]  M. Gross,et al.  Effect of carotenoids on in vitro immunoglobulin production by human peripheral blood mononuclear cells: astaxanthin, a carotenoid without vitamin A activity, enhances in vitro immunoglobulin production in response to a T-dependent stimulant and antigen. , 1995, Nutrition and cancer.

[55]  X. Cameleyre,et al.  HPLC fluorescence method for determination of citrinin in Monascus cultures , 2003 .

[56]  Toshiomi Yoshida,et al.  Production of monascus pigments by a solid-liquid state culture method , 1995 .

[57]  P. Di Mascio,et al.  Carotenoids, tocopherols and thiols as biological singlet molecular oxygen quenchers. , 1990, Biochemical Society transactions.

[58]  G. Choubert,et al.  Carotenoid pigments of the green alga Haematococcus pluvialis: assay on rainbow trout, Oncorhynchus mykiss, pigmentation in comparison with synthetic astaxanthin and canthaxanthin , 1993 .

[59]  N. Krinsky,et al.  Introduction: The colorful, fascinating world of the carotenoids: important physiologic modulators , 1995, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[60]  M. R. Laguna,et al.  Effects of Phaeodactylum tricornutum and Dunaliella tertiolecta Extracts on the Central Nervous System , 1990, Planta medica.

[61]  S. Agarwal,et al.  Tomato lycopene and its role in human health and chronic diseases. , 2000, CMAJ : Canadian Medical Association journal = journal de l'Association medicale canadienne.

[62]  L. S. Jahnke.  Massive carotenoid accumulation in Dunaliella bardawil induced by ultraviolet-A radiation , 1999 .

[63]  G. R. South,et al.  Introduction to phycology , 1987 .

[64]  M. Siess,et al.  Effects of canthaxanthin, astaxanthin, lycopene and lutein on liver xenobiotic-metabolizing enzymes in the rat. , 1996, Xenobiotica; the fate of foreign compounds in biological systems.

[65]  A. Hashem.  Purification and properties of a milk-clotting enzyme produced by Penicillium oxalicum. , 2000 .

[66]  J. Fraumeni,et al.  Risk factors for esophageal cancer in Shanghai, China. II. Role of diet and nutrients , 1994, International journal of cancer.

[67]  O. Torrissen,et al.  Growth and survival of Atlantic salmon, Salmo salar L., fed different dietary levels of astaxanthin. First-feeding fry , 1995 .

[68]  Goma,et al.  Kinetic analysis of red pigment and citrinin production by Monascus ruber as a function of organic acid accumulation. , 2000, Enzyme and microbial technology.

[69]  K. Utsumi,et al.  Inhibition of oxidative injury of biological membranes by astaxanthin. , 1990, Physiological chemistry and physics and medical NMR.

[70]  M. Kobayashi,et al.  Singlet oxygen quenching ability of astaxanthin esters from the green alga Haematococcus pluvialis , 1999, Biotechnology Letters.

[71]  C. la Vecchia,et al.  Selected micronutrient intake and the risk of gastric cancer. , 1994, Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology.

[72]  R T Lorenz,et al.  Commercial potential for Haematococcus microalgae as a natural source of astaxanthin. , 2000, Trends in biotechnology.

[73]  K. Higashi-Okai,et al.  Possible immunomodulating activities of carotenoids in in vitro cell culture experiments. , 1996, International journal of immunopharmacology.

[74]  N. J. Antia,et al.  Isolation of an unusually stable cis-isomer of alloxanthin from a bleached autolysed culture of Chroomonas salina grown photoheterotrophically on glycerol. Observations on cis-trans isomerization of alloxanthin. , 1974, The Journal of protozoology.

[75]  H. Volk,et al.  The influence of phagocytic stimuli on the expression of HLA‐DR antigens; role of reactive oxygen intermediates , 1986, European journal of immunology.

[76]  A. Cal,et al.  Drying of conidia of Penicillium oxalicum, a biological control agent against Fusarium wilt of tomato , 2003 .

[77]  V. O. Mora-Arellano,et al.  Free radicals and singlet oxygen scavengers: reaction of a peroxy-radical with beta-carotene, diphenyl furan and 1,4-diazobicyclo (2,2,2)-octane. , 1981, Biochemical and biophysical research communications.

[78]  M. P. V. Tieghem.  Monascus, Genre Nouveau De L'Ordre Des Ascomycétes , 1884 .