The Possible Mechanisms Involved in Citrinin Elimination by Cryptococcus podzolicus Y3 and the Effects of Extrinsic Factors on the Degradation of Citrinin

Xiaoyun  Zhang; Zhen  Lin; Maurice Tibiru Apaliya; Xiangyu  Gu; Xiangfeng  Zheng; Lina  Zhao; Mandour Haydar  Abdelhai; Hongyin  Zhang; Weicheng  Hu

doi:10.4014/jmb.1707.07051

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Research article

Food Microbiology and Biotechnology (FMB) | Food Biotechnology

The Possible Mechanisms Involved in Citrinin Elimination by Cryptococcus podzolicus Y3 and the Effects of Extrinsic Factors on the Degradation of Citrinin

Xiaoyun Zhang ¹, Zhen Lin ¹, Maurice Tibiru Apaliya ¹, Xiangyu Gu ², Xiangfeng Zheng ¹, Lina Zhao ¹, Mandour Haydar Abdelhai ¹, Hongyin Zhang ^1* and Weicheng Hu ³

¹School of Food and Biological Engineering, Jiangsu University, Zhenjiang 212013, P.R. China, ²School of Grain Science and Technology, Jiangsu University of Science and Technology, Zhenjiang 212003, P.R. China, ³Jiangsu Collaborative Innovation Center of Regional Modern Agriculture & Environmental Protection/Jiangsu Key Laboratory for Eco-Agricultural Biotechnology Around Hongze Lake, Huaiyin Normal University, Huai’an 223300, P.R. China

Received: July 21, 2017; Accepted: September 21, 2017

J. Microbiol. Biotechnol. 2017; 27(12): 2119-2128

Published December 28, 2017 https://doi.org/10.4014/jmb.1707.07051

Abstract

Citrinin (CIT) is a toxic secondary metabolite produced by fungi belonging to the Penicillium, Aspergillus, and Monascus spp. This toxin has been detected in many agricultural products. In this study, a strain Y3 with the ability to eliminate CIT was screened and identified as Cryptococcus podzolicus, based on the sequence analysis of the internal transcribed spacer region. Neither uptake of CIT by cells nor adsorption by cell wall was involved in CIT elimination by Cryptococcus podzolicus Y3. The extracellular metabolites of Cryptococcus podzolicus Y3 stimulated by CIT or not showed no degradation for CIT. It indicated that CIT elimination was attributed to the degradation of intracellular enzyme(s). The degradation of CIT by C. podzolicus Y3 was dependent on the type of media, yeast concentration, temperature, pH, and initial concentration of CIT. Most of the CIT was degraded by C. podzolicus Y3 in NYDB medium at 42 h but not in PDB medium. The degradation rate of CIT was the highest (94%) when the concentration of C. podzolicus Y3 was 1 × 108 cells/ml. The quantity of CIT degradation was highest at 28°C, and there was no degradation observed at 35°C. The study also showed that acidic condition (pH 4.0) was the most favorable for CIT degradation by C. podzolicus Y3. The degradation rate of CIT increased to 98% as the concentration of CIT was increased to 20 μg/ml. The toxicity of CIT degradation product(s) toward HEK293 was much lower than that of CIT.

Keywords

Citrinin, Cryptococcus podzolicus, degradation, extrinsic factor

References

Li Y, Zhou YC, Yang MH, Ou-Yang Z. 2012. Natural occurrence of citrinin in widely consumed traditional Chinese food red yeast rice, medicinal plants and their related products. Food Chem. 132: 1040-1045.
Magro M, Moritz DE, Bonaiuto E, Baratella D, Terzo M, Jakubec P, et al. 2016. Citrinin mycotoxin recognition and removal by naked magnetic nanoparticles. Food Chem. 203:505-512.
European Food Safety Authority. 2012. Scientific opinion on the risks for public and animal health related to the presence of citrinin in food and feed. EFSA J. 10: 2605.
Phillips RD, Hayes AW, Berndt WO, Williams W. 1980. Effects of citrinin on renal function and structure. Toxicology 16: 123-127.
Gupta M, Sasmal D, Bandyopadhyay S, Bagchi G, Chatterjee T, Dey S. 1983. Hematological changes produced in mice by ochratoxin A and citrinin. Toxicology 26: 55-62.
Pascual-Ahuir A, Vanacloig-Pedros E, Proft M. 2014. Toxicity mechanisms of the food contaminant citrinin: application of a quantitative yeast model. Nutrients 6: 2077-2087.
Ribeiro SM, Chagas GM, Campello AP, Kluppel ML. 1997. Mechanism of citrinin-induced dysfunction of mitochondria. 5. Effect on the homeostasis of the reactive oxygen species. Cell Biochem. Funct. 15: 203-209.
Da Lozzo EJ, Mangrich AS, Rocha ME, De Oliveira MB, Carnieri EG. 2002. Effects of citrinin on iron-redox cycle. Cell Biochem. Funct. 20: 19-29.
Da Lozzo EJ, Oliveira MB, Carnieri EG. 1998. Citrinininduced mitochondrial permeability transition. J. Biochem. Mol. Toxicol. 12: 291-297.
CAST. 2003. Mycotoxin: Risks in Plant, Animal, and Human Systems. Council of Agricultural Science and Technology, Task Force Report No. 139. CAST, Ames, IA.
Xu BJ, Jia XQ, Gu LJ, Sung CK. 2006. Review on the qualitative and quantitative analysis of the mycotoxin citrinin. Food Control 17: 271-285.
Blaszkewicz M, Munõz K, Degen GH. 2013. Methods for analysis of citrinin in human blood and urine. Arch. Toxicol. 87: 1087-1094.
Kononenko GP, Burkin AA. 2008. A survey on the occurrence of citrinin in feeds and their ingredients in Russia. Mycotoxin Res. 24: 3-6.
Aziz NH, Moussa LAA. 2002. Influence of gamma-radiation on mycotoxin producing moulds and mycotoxins in fruits. Food Control 13: 281-288.
Tokuşoğlu Ö, Alpas H, Bozoğlu F. 2010. High hydrostatic pressure effects on mold flora, citrinin mycotoxin, hydroxytyrosol, oleuropein phenolics and antioxidant activity of black table olives. Innov. Food Sci. Emerg. 11: 250-258.
Var I, Kabak B, Erginkaya Z. 2008. Reduction in ochratoxin A levels in white wine, following treatment with activated carbon and sodium bentonite. Food Control 19: 592-598.
Bellí N, Marín S, Sanchis V, Ramos AJ. 2006. Impact of fungicides on Aspergillus carbonarius growth and ochratoxin A production on synthetic grapelike medium and on grapes. Food Addit. Contam. 23: 1021-1029.
Cao J, Zhang HY, Yang QY, Ren R. 2013. Efficacy of Pichia caribbica in controlling blue mold rot and patulin degradation in apples. Int. J. Food Microbiol. 162: 167-173.
Ponsone ML, Chiotta ML, Combina M, Dalcero A, Chulze S. 2011. Biocontrol as a strategy to reduce the impact of ochratoxin A and Aspergillus section Nigri in grapes. Int. J. Food Microbiol. 151: 70-77.
Zhang HY, Apaliya MT, Mahunu GK, Chen LL, Li WH. 2016. Control of ochratoxin A-producing fungi in grape berry by microbial antagonists: a review. Trends Food Sci. Technol. 51: 88-97.
Péteri Z, Téren J, Vágvölgyi C, Varga J. 2007. Ochratoxin degradation and adsorption caused by astaxanthin-producing yeasts. Food Microbiol. 24: 205-210.
Mahunu GK, Zhang HY, Y ang QY, Li CL, Zheng XF. 2 016. Biological control of patulin by antagonistic yeast: a case study and possible model. Crit. Rev. Microbiol. 42: 643-655.
Grazioli B, Fumi MD, Silva A. 2006. The role of processing on ochratoxin A content in Italian must and wine: a study on naturally contaminated grapes. Int. J. Food Microbiol. 111: S93-S96.
Wilson CL, Wisniewski ME. (Eds.). 1994. Biological Control of Postharvest Diseases: Theory and Practice. CRC Press, Boca Raton.
Piotrowsk M. 2012. Adsorption of ochratoxin A by Saccharomyces cerevisiae living and non-living cells. Acta Aliment. 41: 1-7.
Yang QY, Wang JJ, Zhang HY, Li CL, Zhang XY. 2016. Ochratoxin A is degraded by Yarrowia lipolytica and generates non-toxic degradation products. World Mycotoxin J. 9: 269-278.
Abd-Allah EE, Ezzat SM. 2005. Natural occurrence of citrinin in rice grains and its biocontrol by Trichoderma hamatum. Phytoparasitica 33: 73-84.
Chen YH, Sheu SC, Mau JL, Hsieh PC. 2010. Isolation and characterization of a strain of Klebsiella pneumoniae with citrinin-degrading activity. World J. Microbiol. Biotechnol. 27: 487-493.
Kanpiengjai A, Mahawan R, Lumyong S, Khanongnuch C. 2015. A soil bacterium Rhizobium borbori and its potential for citrinin-degrading application. Ann. Microbiol. 66: 807-816.
Guillamón JM, Sabaté J, Barrio E, Cano J, Querol A. 1998. Rapid identification of wine yeast species based on RFLP analysis of the ribosomal internal transcribed spacer (ITS) region. Arch. Microbiol. 169: 387-392.
Shen T, Wang GH, You L, Zhang L, Ren HW, Hu WC, et al. 2017. Polysaccharide from wheat bran induces cytokine expression via the Toll-like receptor 4-mediated p38 MAPK signaling pathway and prevents cyclophosphamide-induced immunosuppressionin mice. Food Nutr. Res. 61: 1344523.
Azizi IG, Gorgi M, Rouhi S, Azimi M, Shakib P, Shahbazi B, et al. 2014. Citrinin reduction in wheat flour by using “Yeast Saccharomyces Cerevisiae”. Iran. J. Public Health 43: 241-241.
Patharajan S, Reddy KRN, Karthikeyan V, Spadaro D, Lore A, Gullino ML, et al. 2011. Potential of yeast antagonists on in vitro biodegradation of ochratoxin A. Food Control 22: 290-296.
Petruzzi L, Bevilacqua A, Baiano A, Beneduce L, Corbo MR, Sinigaglia M. 2014. Study of Saccharomyces cerevisiae W13 as a functional starter for the removal of ochratoxin A. Food Control 35: 373-377.
Ianiri G, Idnurm A, Wright SAI, Durán-Patrón R, Mannina L, Ferracane R, et al. 2013. Searching for genes responsible for patulin degradation in a biocontrol yeast provides insight into the basis for resistance to this mycotoxin. Appl. Environ. Microbiol. 79: 3101-3115.
Sumbu ZL, Thonart P, Bechet J . 1983. Action of patulin on a yeast. Appl. Environ. Microbiol. 45: 110-115.
Afsah-Hejri L, Jinap S, Mirhosseini H. 2012. Ochratoxin A quantification: newly developed HPLC conditions. Food Control 23: 113-119.
Gil-Serna J, Patino B, Cortes L, Gonzalez-Jaen MT, Vazquez C. 2011. Mechanisms involved in reduction of ochratoxin A produced by Aspergillus westerdijkiae using Debaryomyces hansenii CYC 1244. Int. J. Food Microbiol. 151: 113-118.

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Article

Research article

J. Microbiol. Biotechnol. 2017; 27(12): 2119-2128

Published online December 28, 2017 https://doi.org/10.4014/jmb.1707.07051

The Possible Mechanisms Involved in Citrinin Elimination by Cryptococcus podzolicus Y3 and the Effects of Extrinsic Factors on the Degradation of Citrinin

Xiaoyun Zhang ¹, Zhen Lin ¹, Maurice Tibiru Apaliya ¹, Xiangyu Gu ², Xiangfeng Zheng ¹, Lina Zhao ¹, Mandour Haydar Abdelhai ¹, Hongyin Zhang ^1* and Weicheng Hu ³

¹School of Food and Biological Engineering, Jiangsu University, Zhenjiang 212013, P.R. China, ²School of Grain Science and Technology, Jiangsu University of Science and Technology, Zhenjiang 212003, P.R. China, ³Jiangsu Collaborative Innovation Center of Regional Modern Agriculture & Environmental Protection/Jiangsu Key Laboratory for Eco-Agricultural Biotechnology Around Hongze Lake, Huaiyin Normal University, Huai’an 223300, P.R. China

Received: July 21, 2017; Accepted: September 21, 2017

Abstract

Citrinin (CIT) is a toxic secondary metabolite produced by fungi belonging to the Penicillium,
Aspergillus, and Monascus spp. This toxin has been detected in many agricultural products. In
this study, a strain Y3 with the ability to eliminate CIT was screened and identified as
Cryptococcus podzolicus, based on the sequence analysis of the internal transcribed spacer
region. Neither uptake of CIT by cells nor adsorption by cell wall was involved in CIT
elimination by Cryptococcus podzolicus Y3. The extracellular metabolites of Cryptococcus
podzolicus Y3 stimulated by CIT or not showed no degradation for CIT. It indicated that CIT
elimination was attributed to the degradation of intracellular enzyme(s). The degradation of
CIT by C. podzolicus Y3 was dependent on the type of media, yeast concentration, temperature,
pH, and initial concentration of CIT. Most of the CIT was degraded by C. podzolicus Y3 in
NYDB medium at 42 h but not in PDB medium. The degradation rate of CIT was the highest
(94%) when the concentration of C. podzolicus Y3 was 1 × 108 cells/ml. The quantity of CIT
degradation was highest at 28°C, and there was no degradation observed at 35°C. The study
also showed that acidic condition (pH 4.0) was the most favorable for CIT degradation by
C. podzolicus Y3. The degradation rate of CIT increased to 98% as the concentration of CIT was
increased to 20 μg/ml. The toxicity of CIT degradation product(s) toward HEK293 was much
lower than that of CIT.

Keywords: Citrinin, Cryptococcus podzolicus, degradation, extrinsic factor

Abstract

References

Li Y, Zhou YC, Yang MH, Ou-Yang Z. 2012. Natural occurrence of citrinin in widely consumed traditional Chinese food red yeast rice, medicinal plants and their related products. Food Chem. 132: 1040-1045.
Magro M, Moritz DE, Bonaiuto E, Baratella D, Terzo M, Jakubec P, et al. 2016. Citrinin mycotoxin recognition and removal by naked magnetic nanoparticles. Food Chem. 203:505-512.
European Food Safety Authority. 2012. Scientific opinion on the risks for public and animal health related to the presence of citrinin in food and feed. EFSA J. 10: 2605.
Phillips RD, Hayes AW, Berndt WO, Williams W. 1980. Effects of citrinin on renal function and structure. Toxicology 16: 123-127.
Gupta M, Sasmal D, Bandyopadhyay S, Bagchi G, Chatterjee T, Dey S. 1983. Hematological changes produced in mice by ochratoxin A and citrinin. Toxicology 26: 55-62.
Pascual-Ahuir A, Vanacloig-Pedros E, Proft M. 2014. Toxicity mechanisms of the food contaminant citrinin: application of a quantitative yeast model. Nutrients 6: 2077-2087.
Ribeiro SM, Chagas GM, Campello AP, Kluppel ML. 1997. Mechanism of citrinin-induced dysfunction of mitochondria. 5. Effect on the homeostasis of the reactive oxygen species. Cell Biochem. Funct. 15: 203-209.
Da Lozzo EJ, Mangrich AS, Rocha ME, De Oliveira MB, Carnieri EG. 2002. Effects of citrinin on iron-redox cycle. Cell Biochem. Funct. 20: 19-29.
Da Lozzo EJ, Oliveira MB, Carnieri EG. 1998. Citrinininduced mitochondrial permeability transition. J. Biochem. Mol. Toxicol. 12: 291-297.
CAST. 2003. Mycotoxin: Risks in Plant, Animal, and Human Systems. Council of Agricultural Science and Technology, Task Force Report No. 139. CAST, Ames, IA.
Xu BJ, Jia XQ, Gu LJ, Sung CK. 2006. Review on the qualitative and quantitative analysis of the mycotoxin citrinin. Food Control 17: 271-285.
Blaszkewicz M, Munõz K, Degen GH. 2013. Methods for analysis of citrinin in human blood and urine. Arch. Toxicol. 87: 1087-1094.
Kononenko GP, Burkin AA. 2008. A survey on the occurrence of citrinin in feeds and their ingredients in Russia. Mycotoxin Res. 24: 3-6.
Aziz NH, Moussa LAA. 2002. Influence of gamma-radiation on mycotoxin producing moulds and mycotoxins in fruits. Food Control 13: 281-288.
Tokuşoğlu Ö, Alpas H, Bozoğlu F. 2010. High hydrostatic pressure effects on mold flora, citrinin mycotoxin, hydroxytyrosol, oleuropein phenolics and antioxidant activity of black table olives. Innov. Food Sci. Emerg. 11: 250-258.
Var I, Kabak B, Erginkaya Z. 2008. Reduction in ochratoxin A levels in white wine, following treatment with activated carbon and sodium bentonite. Food Control 19: 592-598.
Bellí N, Marín S, Sanchis V, Ramos AJ. 2006. Impact of fungicides on Aspergillus carbonarius growth and ochratoxin A production on synthetic grapelike medium and on grapes. Food Addit. Contam. 23: 1021-1029.
Cao J, Zhang HY, Yang QY, Ren R. 2013. Efficacy of Pichia caribbica in controlling blue mold rot and patulin degradation in apples. Int. J. Food Microbiol. 162: 167-173.
Ponsone ML, Chiotta ML, Combina M, Dalcero A, Chulze S. 2011. Biocontrol as a strategy to reduce the impact of ochratoxin A and Aspergillus section Nigri in grapes. Int. J. Food Microbiol. 151: 70-77.
Zhang HY, Apaliya MT, Mahunu GK, Chen LL, Li WH. 2016. Control of ochratoxin A-producing fungi in grape berry by microbial antagonists: a review. Trends Food Sci. Technol. 51: 88-97.
Péteri Z, Téren J, Vágvölgyi C, Varga J. 2007. Ochratoxin degradation and adsorption caused by astaxanthin-producing yeasts. Food Microbiol. 24: 205-210.
Mahunu GK, Zhang HY, Y ang QY, Li CL, Zheng XF. 2 016. Biological control of patulin by antagonistic yeast: a case study and possible model. Crit. Rev. Microbiol. 42: 643-655.
Grazioli B, Fumi MD, Silva A. 2006. The role of processing on ochratoxin A content in Italian must and wine: a study on naturally contaminated grapes. Int. J. Food Microbiol. 111: S93-S96.
Wilson CL, Wisniewski ME. (Eds.). 1994. Biological Control of Postharvest Diseases: Theory and Practice. CRC Press, Boca Raton.
Piotrowsk M. 2012. Adsorption of ochratoxin A by Saccharomyces cerevisiae living and non-living cells. Acta Aliment. 41: 1-7.
Yang QY, Wang JJ, Zhang HY, Li CL, Zhang XY. 2016. Ochratoxin A is degraded by Yarrowia lipolytica and generates non-toxic degradation products. World Mycotoxin J. 9: 269-278.
Abd-Allah EE, Ezzat SM. 2005. Natural occurrence of citrinin in rice grains and its biocontrol by Trichoderma hamatum. Phytoparasitica 33: 73-84.
Chen YH, Sheu SC, Mau JL, Hsieh PC. 2010. Isolation and characterization of a strain of Klebsiella pneumoniae with citrinin-degrading activity. World J. Microbiol. Biotechnol. 27: 487-493.
Kanpiengjai A, Mahawan R, Lumyong S, Khanongnuch C. 2015. A soil bacterium Rhizobium borbori and its potential for citrinin-degrading application. Ann. Microbiol. 66: 807-816.
Guillamón JM, Sabaté J, Barrio E, Cano J, Querol A. 1998. Rapid identification of wine yeast species based on RFLP analysis of the ribosomal internal transcribed spacer (ITS) region. Arch. Microbiol. 169: 387-392.
Shen T, Wang GH, You L, Zhang L, Ren HW, Hu WC, et al. 2017. Polysaccharide from wheat bran induces cytokine expression via the Toll-like receptor 4-mediated p38 MAPK signaling pathway and prevents cyclophosphamide-induced immunosuppressionin mice. Food Nutr. Res. 61: 1344523.
Azizi IG, Gorgi M, Rouhi S, Azimi M, Shakib P, Shahbazi B, et al. 2014. Citrinin reduction in wheat flour by using “Yeast Saccharomyces Cerevisiae”. Iran. J. Public Health 43: 241-241.
Patharajan S, Reddy KRN, Karthikeyan V, Spadaro D, Lore A, Gullino ML, et al. 2011. Potential of yeast antagonists on in vitro biodegradation of ochratoxin A. Food Control 22: 290-296.
Petruzzi L, Bevilacqua A, Baiano A, Beneduce L, Corbo MR, Sinigaglia M. 2014. Study of Saccharomyces cerevisiae W13 as a functional starter for the removal of ochratoxin A. Food Control 35: 373-377.
Ianiri G, Idnurm A, Wright SAI, Durán-Patrón R, Mannina L, Ferracane R, et al. 2013. Searching for genes responsible for patulin degradation in a biocontrol yeast provides insight into the basis for resistance to this mycotoxin. Appl. Environ. Microbiol. 79: 3101-3115.
Sumbu ZL, Thonart P, Bechet J . 1983. Action of patulin on a yeast. Appl. Environ. Microbiol. 45: 110-115.
Afsah-Hejri L, Jinap S, Mirhosseini H. 2012. Ochratoxin A quantification: newly developed HPLC conditions. Food Control 23: 113-119.
Gil-Serna J, Patino B, Cortes L, Gonzalez-Jaen MT, Vazquez C. 2011. Mechanisms involved in reduction of ochratoxin A produced by Aspergillus westerdijkiae using Debaryomyces hansenii CYC 1244. Int. J. Food Microbiol. 151: 113-118.