Hostname: page-component-78c5997874-v9fdk Total loading time: 0 Render date: 2024-11-10T14:51:44.868Z Has data issue: false hasContentIssue false
  • English
  • Français

Red yeast (Phaffia rhodozyma) as a source of Astaxanthin and its impacts on productive performance and physiological responses of poultry

Published online by Cambridge University Press:  23 May 2019

H.A.M. ELWAN ,
S.S. ELNESR ,
Y. ABDALLAH ,
A. HAMDY  and
A.H. EL-BOGDADY
H.A.M. ELWAN*
Affiliation:
Animal and Poultry Production Department, Faculty of Agriculture, Minia University, 61519, El-Minya, Egypt
S.S. ELNESR
Affiliation:
Poultry Production Department, Faculty of Agriculture, Fayoum University, 63514, Fayoum, Egypt
Y. ABDALLAH
Affiliation:
Plant Pathology Department, Minia University, 61519, El-Minya, Egypt
A. HAMDY
Affiliation:
Animal and Poultry Production Department, Faculty of Agriculture, Minia University, 61519, El-Minya, Egypt
A.H. EL-BOGDADY
Affiliation:
Animal and Poultry Production Department, Faculty of Agriculture, Minia University, 61519, El-Minya, Egypt
*
Corresponding author: hamadaelwan83@mu.edu.eg
Get access

Abstract

The red yeast Phaffia rhodozyma is considered as a useful source of astaxanthin (ASX) which is a carotenoid pigment widely used in the feed industry. Poultry cannot synthesise carotenoids, so they must obtain these pigments from diet supplementation with sources such as red yeast, as a source of ASX. Astaxanthin has health benefits including the protection against oxidative damage in cells, enhancement of the immune response and protection against diseases by scavenging oxygen free radicals. It has activities approximately 10 times stronger than that of other carotenoids and 100 times greater than α-tocopherol against reactive oxygen species. In recent years, Phaffia rhodozyma has become an important microorganism for its use in both the pharmaceutical industries and food. Dietary Phaffia rhodozyma addition at the level of 10 and 20 mg/kg in broiler diets positively increased weight gain by 4.12 and 6.41% respectively. The inclusion of ASX rich red yeast (100 mg/kg) in broiler diets for 14 days improved T-cell proliferation and IgG production by 111.1 and 34.6% respectively. However, the optimum level or feeding duration of dietary ASX rich red yeast addition for enhancing poultry productive, physiological and immunological responses has not been determined.

Keywords

astaxanthinred yeastperformancephysiologyimmunitypoultry
Type
Review
Information
World's Poultry Science Journal , Volume 75 , Issue 2 , June 2019 , pp. 273 - 284
Copyright
Copyright © World's Poultry Science Association 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

ABD EL-HAFEZ SOLIMAN, A.M., ELWAN, A.H.M., HADDAD, S.A. and ABD EL-RAHMAN, A.A. (2018) Biochemical, immunological and histopathological alterations in quail fed on Xanthophyllomyces dendrohous. Assiut Journal of Agricultural Sciences 1: 118-132. 10.21608/ajas.2018.8197.Google Scholar
AKIBA, Y., SATO, K., TAKAHASHI, K., MATSUSHITA, H., KOMIYAMA, H., TSUNEKAWA, H. and NAGAO, H. (2001) Meat colour modification in broiler chickens by feeding yeast Phaffia rhodozyma containing high concentrations of astaxanthin. Journal of Applied Poultry Research 10: 154-161.Google Scholar
AMBATI, R.R., PHANG, S.M., RAVI, S. and ASWATHANARAYANA, R.G. (2014) Astaxanthin: sources, extraction, stability, biological activities and its commercial applications - a review. Marine Drugs 12 (1): 128-152, https://doi.org/10.3390/md12010128.Google Scholar
AN, G.H., SONG, J.Y., CHANG, K.S., LEE, B.D., CHAE, H.S. and JANG, B.G. (2004) Pigmentation and delayed oxidation of broiler chickens by the red carotenoid, astaxanthin, from chemical synthesis and the yeast, Xanthophyllomyces dendrorhous. Asian-Australian Journal of Animal Science 17: 1309-1314.Google Scholar
ANDREWES, G.A.G., PHAFF, H.J. and STARR, M.P. (1976) Carotenoids of Phaffia rhodozyma a red-pigmented fermenting yeast. Phytochemistry 15: 1003-1007.Google Scholar
AYDIN, D. and AYDIN, R. (2012) The effects of dietary yeast extract containing mannan oligosaccharide and β-glucans on body performance, feed efficiency and carcass characteristics in Japanese quail. Journal of Animal Science Advanced 2: 184-187.Google Scholar
BARREDO, J.L., GARCÍA-ESTRADA, C., KOSALKOVA, K. and CARLOS, B. (2017) Biosynthesis of Astaxanthin as a Main Carotenoid in the Heterobasidiomycetous Yeast Xanthophyllomyces dendrorhous. Journal of Fungi 3 (3): 44; doi:10.3390/jof3030044.Google Scholar
BENDICH, A.E. and OLSON, J.A. (1989) Biological actions of carotenoids. The FASEB Journal 3 (8): 1927-1932.Google Scholar
BENNEDSEN, M., WANG, X., WILLÉN, R., WADSTRÖM, T. and ANDERSEN, L.P. (1999) Treatment of H. pylori infected mice with antioxidant astaxanthin reduces gastric inflammation, bacterial load and modulates cytokine release by splenocytes. Immunology Letters 70: 185-189.Google Scholar
BJERKENG, B., PEISKER, M.K., SCHWARTZENBERG, V., YTRESTØYL, T. and ÅSGÅRD, T. (2007) Digestibility and muscle retention of astaxanthin in Atlantic salmon, Salmo salar, fed diets with the red yeast Phaffia rhodozyma in comparison with synthetic formulated astaxanthin. Aquaculture 269: 476-489.Google Scholar
BOUSSIBA, S. (2000) Carotenogenesis in the green alga Haematococcus pluvialis: cellular physiology and stress response. Physiologia Plantarum 108 (2): 111-117.Google Scholar
BUBRICK, P. (1991) Production of astaxanthin from Haematococcus. Bioresource Technology 38 (2): 237-239.Google Scholar
CAO, J. and WANG, W. (2014) Effects of astaxanthin and esterified glucomannan on hematological and serum parameters, and liver pathological changes in broilers fed aflatoxin-B1-contaminated feed. Animal Science Journal 85: 150-157.Google Scholar
CHENG, Y.H., SHEN, T.F., PANG, V.F. and CHEN, B.J. (2001) Effect of aflatoxin and carotenoids on growth performance and immune response in mule ducklings. Comparative Biochemistry and Physiology - Part C: Toxicology 128: 19-26.Google Scholar
CHEW, B.P., WONG, M.W., PARK, J.S. and WONG, T.S. (1999) Dietary beta-carotene and astaxanthin but not canthaxanthin stimulate splenocyte function in mice. Anticancer Research 19: 5223-5227.Google Scholar
COMHAIRE, F.H. and MAHMOUD, A. (2003) The role of food supplements in the treatment of the infertile man. Reproductive Biomedicine Online 7 (4): 385-391.Google Scholar
CONTRERAS, G., BARAHONA, S., SEPÚLVEDA, D., BAEZA, M., CIFUENTES, V. and ALCAÍNO, J. (2015) Identification and analysis of metabolite production with biotechnological potential in Phaffia rhodozyma isolates. World Journal of Microbiology and Biotechnology 31 (3): 517-526.Google Scholar
FASSETT, R.G. and COOMBES, J.S. (2011) Astaxanthin: a potential therapeutic agent in cardiovascular disease. Marine Drugs 9 (3): 447-465.Google Scholar
GAO, J., ZHANG, H.J., YU, S.H., WU, S.G., YOON, I., QUIGLEY, J. and QI, G.H. (2008) Effects of yeast culture in broiler diets on performance and immunomodulatory functions. Poultry Science 87 (7): 1377-1384.Google Scholar
GOODWIN, T.W. (1980) Biogeochemistry of Carotenoids, in: The biochemistry of the carotenoids, pp. 346-349 (Springer, Dordrecht).Google Scholar
GOODWIN, T.W. (1986) Metabolism, nutrition, and function of carotenoids. Annual Review of Nutrition 6 (1): 273-297.Google Scholar
HAINES, D.D., VARGA, B., BAK, I., JUHASZ, B., MAHMOUD, F.F., KALANTARI, H. and TOSAKI, A. (2011) Summative interaction between astaxanthin, Ginkgo biloba extract (EGb761) and vitamin C in suppression of respiratory inflammation: a comparison with ibuprofen. Phytotherapy Research 25 (1): 128-136.Google Scholar
HIGUERA-CIAPARA, I., FELIX-VALENZUELA, L. and GOYCOOLEA, F.M. (2006) Astaxanthin: a review of its chemistry and applications. Critical Reviews in Food Science and Nutrition 46 (2): 185-196.Google Scholar
HU, Z., ZHENG, Y., WANG, Z. and SHEN, Y. (2007) Production of astaxanthin by Xanthophyllomyces dendrorhous ZJUT46 with Fed-Batch Fermentation in 2.0 M^ 3 Fermentor. Food Technology and Biotechnology 45 (2): 209.Google Scholar
HUSSEIN, G., SANKAWA, U., GOTO, H., MATSUMOTO, K. and WATANABE, H. (2006) Astaxanthin, a carotenoid with potential in human health and nutrition. Journal of Natural Products 69: 443-449.Google Scholar
IKEUCHI, M., KOYAMA, T., TAKAHASHI, J. and YAZAWA, K. (2006) Effects of astaxanthin supplementation on exercise-induced fatigue in mice. Biological and Pharmaceutical Bulletin 29 (10): 2106-2110.Google Scholar
IKEUCHI, M., KOYAMA, T., TAKAHASHI, J. and YAZAWA, N. (2007) Effects of astaxanthin in obese mice fed a high-fat diet. Bioscience, Biotechnology, and Biochemistry 71 (4): 893-899.Google Scholar
IWAMOTO, T., HOSODA, K., HIRANO, R., KURATA, H., MATSUMOTO, A., MIKI, W. and KONDO, K. (2000) Inhibition of low-density lipoprotein oxidation by astaxanthin. Journal of Atherosclerosis and Thrombosis 7 (4): 216-222.Google Scholar
JEONG, J.S. and KIM, I.H. (2014) Effect of astaxanthin produced by Phaffia rhodozyma on growth performance, meat quality, and fecal noxious gas emission in broilers. Poultry Science 93: 3138-3144 http://dx.doi.org/ 10.3382/ps.2013-03847.Google Scholar
JOHNSON, E.A. and SCHROEDER, W.A. (1995) Microbial carotenoids. In: Fiechter A (ed) Advanced Biochemical Engendering Biotechnology 53: 119-178.Google Scholar
JOHNSON, E.A. and AN, G.H. (1991) Astaxanthin from microbial sources. Critical Reviews in Biotechnology 11 (4): 297-326.Google Scholar
JOHNSON, E.A. and LEWIS, M.J. (1979) Astaxanthin formation by the yeast Phaffia rhodozyma. Microbiology 115 (1): 173-183.Google Scholar
JOHNSON, E.A., VILLA, T.G. and LEWIS, M.J. (1980) Phaffia rhodozyma as an astaxanthin source in salmonid diets. Aquaculture 20 (2): 123-134.Google Scholar
JOHNSON, E.A., YANG, H., GELDIAY-TUNCER, B., HALL, W.T., SCHREIHER, D. and HO, K. (2010) Process for in vivo production of astaxanthin and Phaffia rhodozyma yeast of enhanced astaxanthin content. US Patent No. US 7723066.Google Scholar
JYONOUCHI, H., SUN, S., TOMITA, Y. and GROSS, M.D. (1995) Astaxanthin, a carotenoid without vitamin A activity, augments antibody responses in cultures including T-helper cell clones and suboptimal doses of antigen. Journal of Nutrition 125: 2483-2492.Google Scholar
LEE, S.J., BAI, S.K., LEE, K.S., NAMKOONG, S., NA, K.S., HAN, J.A., YIM, S.V., CHANG, K., KWON, Y.G., LEE, S.K. and KIM, Y.M. (2003) Astaxanthin inhibits nitric oxide production and inflammatory gene expression by suppressing I (kappa) B kinase-dependent NF-kappaB activation. Molecules and Cells 31: 97-105.Google Scholar
LEITE, M.F., DE LIMA, A.M., KANG, S.J.S., DOS SANTOS, M.T.B.R. and OTTON, R. (2014) Effect of astaxanthin and fish oil on enzymatic antioxidant system and α-amylase activity of salivary glands from rats. Brazilian Journal of Oral Sciences 13 (1): 58-63.Google Scholar
LIBKIND, D., MOLINÉ, M., DE GARCÍA, V., FONTENLA, S. and VAN BROOCK, M. (2008) Characterization of a novel South American population of the astaxanthin producing yeast Xanthophyllomyces dendrorhous (Phaffia rhodozyma). Journal of Industrial Microbiology & Biotechnology 35 (3): 151-158.Google Scholar
LIU, B., GE, X., HE, Y., XIE, J., XU, P., HE, Y. and CHEN, R. (2010) Effects of anthraquinones extracted from Rheum officinale Bail on the growth, non-specific immune response of Macrobrachium rosenbergii. Aquaculture 310 (1): 13-19.Google Scholar
LIU, Y.S. and WU, J.Y. (2006) Use of n-hexadecane as an oxygen vector to improve Phaffia rhodozyma growth and carotenoid production in shake-flask cultures. Journal of Applied Microbiology 101 (5): 1033-1038.Google Scholar
LU, Y.P., LIU, S.Y., SUN, H., WU, X.M., LI, J.J. and ZHU, L. (2010) Neuroprotective effect of astaxanthin on H2O2-induced neurotoxicity in vitro and on focal cerebral ischemia in vivo. Brain Research 1360: 40-48.Google Scholar
LYONS, N.M. and O'BRIEN, N.M. (2002) Modulatory effects of an algal extract containing astaxanthin on UVA-irradiated cells in culture. Journal of Dermatological Science 30: 73-84.Google Scholar
MAGNUSON, A.D., SUN, T., YIN, R., LIU, G., TOLBA, S., SHINDE, S. and LEI, X.G. (2018) Supplemental microalgal astaxanthin produced coordinated changes in intrinsic antioxidant systems of layer hens exposed to heat stress. Algal Research 33: 84-90. doi:10.1016/j.algal.2018.04.031.Google Scholar
MIKI, W. (1993) Recent progress in the research of biological activities, in: MIKI, W. (Ed.) Carotenoids in Marine Organisms 94, Chapter 7 (Koseisya Koseikaku: Tokyo).Google Scholar
MILLER, M.W., YONEYAMA, M. and SONEDA, M. (1976) Phaffia, a new yeast genus in the Deuteromycotina (Blastomycetes). International Journal of Systematic Bacteriology 26: 286-291.Google Scholar
MONTANTI, J., NGHIEM, N.P. and JOHNSTON, D.B. (2011) Production of astaxanthin from cellulosic biomass sugars by mutants of the yeast Phaffia rhodozyma. Applied Biochemistry and Biotechnology, 164 (5): 655-665.Google Scholar
MORALES-LÓPEZ, R., AUCLAIR, E., GARCIA, F., ESTEVE-GARCIA, E. and BRUFAU, J. (2009) Use of yeast cell walls; β-1, 3/1, 6-glucans; and mannoproteins in broiler chicken diets. Poultry Science 88 (3): 601-607.Google Scholar
MOUSA, S.M.M., SOLIMAN, M.M. and BAHAKAIM, A.S.A. (2014) Effect of Mannan Oligosaccharides and β-glucans on productive performance and some physiological and immunological parameters of growing Japanese quail chicks. Egyptian Poultry Science Journal 34: 433-451.Google Scholar
NAGUIB, Y.M. (2000) Antioxidant activities of astaxanthin and related carotenoids. Journal of Agricultural and Food Chemistry 48 (4): 1150-1154.Google Scholar
NAKANO, T., KANMURI, T., SATO, M. and TAKEUCHI, M. (1999) Effect of astaxanthin rich red yeast (Phaffia rhodozyma) on oxidative stress in rainbow trout. Biochimica et Biophysica Acta (BBA)-General Subjects 1426 (1): 119-125.Google Scholar
NAKANO, T., TOSA, M. and TAKEUCHI, M. (1995) Improvement of biochemical features in fish health by red yeast and synthetic astaxanthin. Journal of Agricultural and Food Chemistry 43 (6): 1570-1573.Google Scholar
OHH, MI-H., SEONGJIN, K., SOK, C. and KEW-MAHN, C. (2016) Effects of dietary supplementation with astaxanthin on histamine induced lesions in the gizzard and proventriculus of broiler chicks. Asian Australians Journal of Animal Science 29 (6): 872-878.Google Scholar
PERENLEI, G., HITOMI TOJO, T.O., MASATOSHI, K., MOTONI, K. and SHINOBU, F. (2014) Effect of dietary astaxanthin rich yeast, Phaffia rhodozyma, on meat quality of broiler chickens. Animal Science Journal 85: 895-903.Google Scholar
RUIZ-NÚÑEZ, B., SCHUITEMAKER, G.E., DIJCK-BROUWER, D.J. and MUSKIET, F.A. (2014) Kinetics of plasma and erythrocyte-astaxanthin in healthy subjects following a single and maintenance oral dose. Journal of Young Pharmacists 6 (1): 43.Google Scholar
SANDERSON, G.W. and JOLLY, S.O. (1994) The value of Phaffia yeast as a feed ingredient for salmonid fish. Aquaculture 124: 193-200.Google Scholar
SIMPSON, K.L. and CHICHESTER, C.O. (1981) Metabolism and nutritional significance of carotenoids. Annual review of nutrition 1 (1): 351-374.Google Scholar
STANLEY, V.G., GRAY, C., DALEY, M., KRUEGER, W.F. and SEFTON, A.E. (2004) An alternative to antibiotic-based drugs in feed for enhancing performance of broilers grown on Eimeria spp.-infected litter. Poultry Science 83: 39-44.Google Scholar
STOREBAKKEN, T., SØRENSEN, M., BJERKENG, B., HARRIS, J., MONAHAN, P. and HIU, S. (2004) Stability of astaxanthin from red yeast, Xanthophyllomyces dendrorhous, during feed processing: effects of enzymatic cell wall disruption and extrusion temperature. Aquaculture 231 (1): 489-500.Google Scholar
SUN, T., YIN, R., MAGNUSON, A.D., TOLBA, S.A., LIU, G. and LEI, X.G. (2018) Dose-dependent enrichments and improved redox status in tissues of broiler chicks under heat stress by dietary supplemental microalgal astaxanthin. Journal of Agricultural and Food Chemistry 66 (22): 5521-5530 doi:10.1021/acs.jafc.8b00860.Google Scholar
SUZUKI, Y., OHGAMI, K., SHIRATORI, K.J., ILIEVA, I., KOYAMA, Y., YAZAWA, K., YOSHIDA, K., KASE, S. and OHNO, S. (2006) Suppressive effects of astaxanthin against rat endotoxin-induced uveitis by inhibiting the NF-kappaB signaling pathway. Experimental Eye Research 82: 275-281.Google Scholar
TAKAHASHI, K., WATANABE, M., TAKIMOTO, T. and AKIBA, Y. (2004) Uptake and distribution of astaxanthin in several tissues and plasma lipoproteins in male broiler chickens fed yeast (Phaffia rhodozyma) with a high concentration of astaxanthin. British Poultry Science 45 (1): 133-138.Google Scholar
TAKAHASHI, K., TETSUYA, T.K. and AKIBA, Y. (2011) Effect of dietary supplementation of astaxanthin from Phaffia rhodozyma on lipopolysaccharide-induced early inflammatory responses in male broiler chickens (Gallus gallus) fed a corn-enriched diet. Animal Science Journal 82: 753-758.Google Scholar
TAKIMOTO, T., SATO, K., AKIBA, Y. and TAKAHASHI, K. (2006) Effect of astaxanthin from Phaffia rhodozyma on T-cell population and responsiveness to mitogen in splenic mononuclear cells of male broiler chicks. Journal Poultry Science 43: 41-48.Google Scholar
TAKIMOTO, T., TAKAHASHI, K. and AKIBA, Y. (2007) Effect of dietary supplementation of astaxanthin by Phaffia rhodozyma on lipid peroxidation, drug metabolism and some immunological variables in male broiler chicks fed on diets with or without oxidised fat. British Poultry Science 48 (1): 90-97, DOI: 10.1080/00071660601156453.Google Scholar
TAPINGKAE, W., YINDEE, P. and MOONMANEE, T. (2016) Effect of dietary red yeast (Sporidiobolus pararoseus) supplementation on small intestinal histomorphometry of laying hens. The Journal of Animal and Plant Sciences 26: 909-915.Google Scholar
TAPINGKAE, W., PANYACHAI, K., YACHAI, M. and DOAN, H.V. (2018) Effects of dietary red yeast (Sporidiobolus pararoseus) on production performance and egg quality of laying hens. Journal of Animal Physiology and Animal Nutrition 102 (1): e337-e344.Google Scholar
UCHIYAMA, K., NAITO, Y., HASEGAWA, G., NAKAMURA, N., TAKAHASHI, J. and YOSHIKAWA, T. (2002) Astaxanthin protects β-cells against glucose toxicity in diabetic db/db mice. Redox Report 7 (5): 290-293.Google Scholar
WANG, C., ARMSTRONG, D.W. and CHANG, C.D. (2008) Rapid baseline separation of enantiomers and a mesoform of alltransastaxanthin, 13cisastaxanthin, adonirubin, and adonixanthin in standards and commercial supplements. Journal of Chromatography, A 1194: 172177.Google Scholar
WANG, WJ. and YU, LJ. (2009) Effects of oxygen supply on the growth and carotenoids accumulation by Xanthophyllomyces dendrorhous. Zeitschrift für Naturforschung C 64c: 223-228.Google Scholar
WEBER, R.W.S., BECERRA, J., SILVA, M.J. and DAVOLI, P. (2008) An unusual Xanthophyllomyces strain from leaves of Eucalyptus globulus in Chile. Mycological Research 112: 861-867, doi: 10.1016/j.mycres.2007.11.019.Google Scholar
YAMANE, Y., HIGASHIDA, K., NAKASHIMADA, Y., KAKIZONO, T. and NISHIO, N. (1997) Influence of Oxygen and Glucose on Primary Metabolism and Astaxanthin Production by Phaffia rhodozyma in Batch and Fed-Batch Cultures: Kinetic and Stoichiometric Analysis. Applied and Environmental Microbiology 63 (11): 4471-4478.Google Scholar
YANG, Y., STERLING, J., STORICI, F., RESNICK, M.A. and GORDENIN, D.A. (2008) Hypermutability of damaged single-strand DNA formed at double-strand breaks and uncapped telomeres in yeast Saccharomyces cerevisiae. PLoS genetics 4 (11): e1000264.Google Scholar
ZHANG, J., LI, X., LENG, X., ZHANG, C., HAN, Z. and ZHANG, F. (2013) Effects of dietary astaxanthins on pigmentation of flesh and tissue antioxidation of rainbow trout (Oncorhynchus mykiss). Aquaculture International 21: 579-589.Google Scholar
ZHENG, Y.G., HU, Z.C., WANG, Z. and SHEN, Y.C. (2006) Large-scale production of astaxanthin by Xanthophyllomyces dendrorhous. Food and bioproducts processing 84 (2): 164-166.Google Scholar