Investigating Ochratoxin-A Biodegradation, Detoxification, and Antibiotic Resistance Ability of Brevundimonas naejangsanensis

Mohammed  Al-Nussairawi

doi:10.55544/sjmars.3.4.11

Authors

Mohammed Al-Nussairawi Department of Clinical and Laboratory Sciences, College of Pharmacy, University of Misan, Misan, IRAQ https://orcid.org/0000-0001-8819-5356

DOI:

https://doi.org/10.55544/sjmars.3.4.11

Keywords:

OTA, biodegradation, detoxification, antibiotic, resistance

Abstract

Ochratoxin A (OTA) is a nephrotoxic and genotoxic mycotoxin produced by Aspergillus and Penicillium species. It threatens animal and human health by contaminating feed and food commodities. Biodegradation is the most widely utilized method for detoxifying this mycotoxin. Brevundimonas naejangsanensis was reported to biodegrade 60 % of OTA at 4 mg/l during the first day, 85% on the second day, and almost 99-100 % at the end of the third day when using 10 ppm of OTA. The capacity of B. naejangsanensis was examined to break down OTA at 28 and 30 °C in LB medium at concentrations of 4 ppm and 10 ppm. Under these circumstances, B. naejangsanensis was able to degrade almost 100% of OTA starting at a concentration of 10 (g/ml). B. naejangsanensis eliminated an average of 0.1008 and 0.05455 (g/ml/h) of OTA from a medium having an initial concentration of 4 (g/ml) at 28 and 30 °C, respectively. At both incubation temperatures, Ochratoxin A was halted significantly by B. naejangsanensis at both log phase and after finishing the log phase of cell development. According to the results, OTA was decomposed by B. naejangsanensis to ochratoxin of lower toxicity. At the same time a strain of microorganism was being tested for its antimicrobial potential, with tests demonstrating that such resistance might be achieved. The antibiotic susceptibility of a B. naejangsanensis strain isolated from soil samples was evaluated against a range of unrelated antibiotic drug classes. A. calcoaceticus was resistant to most of the antibiotics. Through the use of several methods, including high-performance liquid chromatography (HPLC), the toxin's breakdown was tracked.

References

Stark, A.A., 1980. Mutagenicity and Carcinogenicity of Mycotoxins: DNA Binding as a Possible Mode of Action. Annu. Rev. Microbiol. 34, 235–262. https://doi.org/10.1146/annurev.mi.34.100180.001315

Malir, F., Ostry, V., Grosse, Y., Roubal, T., Skarkova, J., Ruprich, J., 2006. Monitoring the mycotoxins in food and their biomarkers in the Czech Republic. Mol. Nutr. Food Res. 50, 513–518. https://doi.org/10.1002/mnfr.200500175

Wild, C.P., Gong, Y.Y., 2009. Mycotoxins and human disease: A largely ignored global health issue. Carcinogenesis 31, 71–82. https://doi.org/10.1093/carcin/bgp264

Krifaton, C., Kukolya, J., Szoboszlay, S., Cserháti, M., Szucs, Á., Kriszt, B., 2010. Adaptation of bacterial biotests for monitoring mycotoxins. WIT Trans. Ecol. Environ. 132, 143–153. https://doi.org/10.2495/ETOX100141

Kensler, T.W., Roebuck, B.D., Wogan, G.N., Groopman, J.D., 2011. Aflatoxin: A 50-year Odyssey of mechanistic and translational toxicology. Toxicol. Sci. 120, 28–48. https://doi.org/10.1093/toxsci/kfq283

Zimmerli, B., Dick, R., 1995. Determination of ochratoxin A at the ppt level in human blood, serum, milk and some foodstuffs by high-performance liquid chromatography with enhanced fluorescence detection and immunoaffinity column cleanup: methodology and Swiss data. J. Chromatogr. B Biomed. Sci. Appl. 666, 85–99. https://doi.org/https://doi.org/10.1016/0378-4347(94)00569-Q

Vega, F.E., Chaves, F., Gianfagna, T.J., Posada, F., Peterson, S.W., 2006. Penicillium species endophytic in coffee plants and ochratoxin A production. Mycologia 98, 31–42.

Bragulat, M.R., Martínez, E., Castellá, G., Cabañes, F.J., 2008. Ochratoxin A and citrinin producing species of the genus Penicillium from feedstuffs. Int. J. Food Microbiol. 126, 43–48. https://doi.org/10.1016/j.ijfoodmicro.2008.04.034

Duarte, S.C., Lino, C.M., Pena, A., 2012. Food safety implications of ochratoxin A in animal-derived food products. Vet. J. 192, 286–292. https://doi.org/10.1016/j.tvjl.2011.11.002

Kőszegi, T., Poór, M., 2016. Ochratoxin a: Molecular interactions, mechanisms of toxicity and prevention at the molecular level. Toxins (Basel). 8, 1–25. https://doi.org/10.3390/toxins8040111

Scott, P.M., Kanhere, S.R., Lau, B.P.Y., Levvis, D.A., Hayward, S., Ryan, J.J., Kuiper‐Goodman, T., 1998. Survey of Canadian human blood plasma for ochratoxin A. Food Addit. Contam. 15, 555–562. https://doi.org/10.1080/02652039809374681

Vatinno, R., Aresta, A., Zambonin, C.G., Palmisano, F., 2007. Determination of ochratoxin A in human urine by solid-phase microextraction coupled with liquid chromatography-fluorescence detection. J. Pharm. Biomed. Anal. 44, 1014–1018. https://doi.org/10.1016/j.jpba.2007.04.008

Zain, M.E., 2011. Impact of mycotoxins on humans and animals. J. Saudi Chem. Soc. 15, 129–144. https://doi.org/10.1016/j.jscs.2010.06.006

IARC, 1993. Some naturally occurring substances: food items and constituents, heterocyclic aromatic amines and mycotoxins. IARC Monogr. Eval. Carcinog. Risk Chem. to Humans 56, 1–521. https://doi.org/10.1002/food.19940380335

Maaroufi, K., Pfohl-Leszkowicz, A., Achour, A., el May, M., Grosse, Y., Hammami, M., Ellouz, F., Creppy, E.E., Bacha, H., 1994. [Ochratoxin A genotoxicity, relation to renal tumors]. Arch. Inst. Pasteur Tunis 71, 21–31.

Žlender, V., Breljak, D., Ljubojević, M., Flajs, D., Balen, D., Brzica, H., Domijan, A.M., Peraica, M., Fuchs, R., Anzai, N., Sabolić, I., 2009. Low doses of ochratoxin A upregulate the protein expression of organic anion transporters Oat1, Oat2, Oat3 and Oat5 in rat kidney cortex. Toxicol. Appl. Pharmacol. 239, 284–296. https://doi.org/10.1016/j.taap.2009.06.008

Yang, Q., He, X., Li, X., Xu, W., Luo, Y., Yang, X., Wang, Y., Li, Y., Huang, K., 2014. DNA damage and S phase arrest induced by Ochratoxin A in human embryonic kidney cells (HEK 293). Mutat. Res. - Fundam. Mol. Mech. Mutagen. 765, 22–31.

Hennemeier, I., Humpf, H.U., Gekle, M., Schwerdt, G., 2014. Role of microRNA-29b in the ochratoxin A-induced enhanced collagen formation in human kidney cells. Toxicology 324, 116–122. https://doi.org/10.1016/j.tox.2014.07.012

Yang, X., Liu, S., Huang, C., Wang, H., Luo, Y., Xu, W., Huang, K., 2017. Ochratoxin A induced premature senescence in human renal proximal tubular cells. Toxicology 382, 75–83. https://doi.org/10.1016/j.tox.2017.03.009

EFSA 2010. Panel on Additives and Products or Substances used in Animal Feed (FEEDAP): Statement on the establishment of guidelines for the assessment of additives from the functional group ‘substances for reduction of the contamination of feed by mycotoxins.’ EFSA J. 8, 1693. https://doi.org/10.2903/j.efsa.2010.1693

Alberts, J.F., Engelbrecht, Y., Steyn, P.S., Holzapfel, W.H., van Zyl, W.H., 2006. Biological degradation of aflatoxin B1 by Rhodococcus erythropolis cultures. Int. J. Food Microbiol. 109, 121–126. https://doi.org/https://doi.org/10.1016/j.ijfoodmicro.2006.01.019

Teniola, O.D., Addo, P.A., Brost, I.M., Färber, P., Jany, K.-D., Alberts, J.F., van Zyl, W.H., Steyn, P.S., Holzapfel, W.H., 2005. Degradation of aflatoxin B1 by cell-free extracts of Rhodococcus erythropolis and Mycobacterium fluoranthenivorans sp. nov. DSM44556T. Int. J. Food Microbiol. 105, 111–117. https://doi.org/https://doi.org/10.1016/j.ijfoodmicro.2005.05.004

Krifaton, C., Kriszt, B., Szoboszlay, S., Cserháti, M., Szűcs, Á., Kukolya, J., 2011. Analysis of aflatoxin-B1-degrading microbes by use of a combined toxicity-profiling method. Mutat. Res. Toxicol. Environ. Mutagen. 726, 1–7. https://doi.org/10.1016/J.MRGENTOX.2011.07.011

Krifaton, C., Kriszt, B., Risa, A., Szoboszlay, S., Cserháti, M., Harkai, P., Eldridge, M., Wang, J., Kukolya, J., 2013. Application of a yeast estrogen reporter system for screening zearalenone degrading microbes. J. Hazard. Mater. 244–245, 429–435. https://doi.org/https://doi.org/10.1016/j.jhazmat.2012.11.063

Fuchs, S., Sontag, G., Stidl, R., Ehrlich, V., Kundi, M., Knasmüller, S., 2008. Detoxification of patulin and ochratoxin A, two abundant mycotoxins, by lactic acid bacteria. Food Chem. Toxicol. 46, 1398–1407. https://doi.org/10.1016/j.fct.2007.10.008

Beard, S.E., Capaldi, S.R., Gee, P., 1996. Stress responses to DNA damaging agents in the human colon carcinoma cell line, RKO. Mutat. Res. Toxicol. 371, 1–13. https://doi.org/10.1016/S0165-1218(96)90089-0

Petchkongkaew, A., Taillandier, P., Gasaluck, P., Lebrihi, A., 2008. Isolation of Bacillus spp. from Thai fermented soybean (Thua-nao): screening for aflatoxin B1 and ochratoxin A detoxification. J. Appl. Microbiol. 104, 1495–1502. https://doi.org/10.1111/j.1365-2672.2007.03700.x

Rodriguez, H., Reveron, I., Doria, F., Costantini, A., De Las Rivas, B., Muňoz, R., Garcia-Moruno, E., 2011. Degradation of Ochratoxin A by Brevibacterium Species. J. Agric. Food Chem. 59, 10755–10760. https://doi.org/10.1021/jf203061p

Ferenczi, S., Cserháti, M., Krifaton, C., Szoboszlay, S., Kukolya, J., Szoke, Z., Koszegi, B., Albert, M., Barna, T., Mézes, M., Kovács, K.J., Kriszt, B., 2014. A new ochratoxin a biodegradation strategy using cupriavidus basilensis Or16 strain. PLoS One 9. https://doi.org/10.1371/journal.pone.0109817

Abrunhosa, L., Inês, A., Rodrigues, A. I., Guimarães, A., Pereira, V. L., Parpot, P., et al. (2014). Biodegradation of Ochratoxin A by Pediococcus parvulus isolated from Douro wines. Int. J. Food Microbiol. 188, 45–52. doi: 10.1016/j.ijfoodmicro.2014.07.019

Chang, X., Wu, Z., Wu, S., Dai, Y., Sun, C., 2015. Degradation of ochratoxin A by Bacillus amyloliquefaciens ASAG1. Food Addit. Contam. - Part A Chem. Anal. Control. Expo. Risk Assess. 32, 564–571. https://doi.org/10.1080/19440049.2014.991948

De Bellis P, Tristezza M, Haidukowski M, Fanelli F, Sisto A, Mulè G, Grieco F. Biodegradation of Ochratoxin A by Bacterial Strains Isolated from Vineyard Soils. Toxins (Basel). 2015 Nov 27;7(12):5079-93. doi: 10.3390/toxins7124864. PMID: 26633497; PMCID: PMC4690114

Luz C, Ferrer J, Manes J, Meca G. Toxicity reduction of ochratoxin A by lactic acid bacteria. Food Chem Toxicol. 2018;112:60–66. doi: 10.1016/j.fct.2017.12.030.

Zhang, H.H., Wang, Y., Zhao, C., Wang, J., Zhang, X.L., 2017. Biodegradation of ochratoxin A by Alcaligenes faecalis isolated from soil. J. Appl. Microbiol. 123, 661–668.

Kowalska-Krochmal B, Dudek-Wicher R. The Minimum Inhibitory Concentration of Antibiotics: Methods, Interpretation, Clinical Relevance. Pathogens. 2021;10(2):165. doi: 10.3390/pathogens10020165

Kang, S.-J., Choi, N.-S., Choi, J.H., Lee, J.-S., Yoon, J.-H., and Song, J.J. "Brevundimonas naejangsanensis sp. nov., a proteolytic bacterium isolated from soil, and reclassification of Mycoplana bullata into the genus Brevundimonas as Brevundimonas bullata comb. nov." Int. J. Syst. Evol. Microbiol. (2009) 59:3155-3160

Moretti, A., Pascale, M., Logrieco, A.F., 2018. Mycotoxin risks under a climate change scenario in Europe. Trends Food Sci. Technol. https://doi.org/10.1016/j.tifs.2018.03.008

Capriotti, A.L., Caruso, G., Cavaliere, C., Foglia, P., Samperi, R., Lagana, A., 2012. Multiclass mycotoxin analysis in food, environmental and biological matrices with chromatography/mass spectrometry. Mass Spectrom. Rev. 31, 466–503. https://doi.org/10.1002/mas.20351

Piotrowska, M.Zakowska, Z., 2005. The elimination of ochratoxin A by lactic acid bacteria strains. Polish J. Microbiol. 54(4), 279–86. P.

Al-Nussairawi M, Risa A, Garai E, Varga E, Szabó I, Csenki-Bakos Z, Kriszt B, Cserháti M. Mycotoxin Biodegradation Ability of the Cupriavidus Genus. Curr Microbiol. 2020 Sep;77(9):2430-2440. doi: 10.1007/s00284-020-02063-7. Epub 2020 Jun 5. PMID: 32504322; PMCID: PMC7415022.

Al-Nussairawi M, Al-Tulaibawi NAJ, Aal-Aaboda M. Determination of Ochratoxin-A Detoxification and Antibiotic Resistance Potential of Acinetobacter calcoaceticus. J Pure Appl Microbiol. 2023;17(2):1017-1028. doi: 10.22207/JPAM.17.2.31