Anaerobic degradation of microcystin-LR by an indigenous bacterial Enterobacter sp. YF3

References

• Botha, N., M. M. Gehringer, T. G. Downing, M. van de Venter, and E. G. Shephard. 2004. The role of microcystin-LR in the induction of apoptosis and oxidative stress in CaCo2 cells. Toxicon 43:85–92. doi:10.1016/j.toxicon.2003.10.025.
   PubMed Web of Science ®Google Scholar
• Bourne, D. G., G. J. Jones, R. L. Blakeley, A. Jones, A. P. Negri, and P. Riddles. 1996. Enzymatic pathway for the bacterial degradation of the cyanobacterial cyclic peptide toxin microcystin LR. Appl. Environ. Microbiol. 62:4086–94.
   PubMed Web of Science ®Google Scholar
• Cao, L., F. Huang, I. Y. Massey, C. Wen, S. Zheng, S. Xu, and F. Yang. 2019a. Effects of microcystin-LR on the microstructure and inflammation-related factors of jejunum in mice. Toxins (Basel) 11. doi:10.3390/toxins11090482.
   Web of Science ®Google Scholar
• Cao, L., I. Y. Massey, H. Feng, and F. Yang. 2019b. A review of cardiovascular toxicity of microcystins. Toxins (Basel) 11. doi:10.3390/toxins11090507.
   Web of Science ®Google Scholar
• Carmichael, W. W. 1992. Cyanobacteria secondary metabolites–The cyanotoxins. J. Appl. Bacteriol. 72:445–59. doi:10.1111/j.1365-2672.1992.tb01858.x.
   PubMedGoogle Scholar
• Carmichael, W. W., S. M. Azevedo, J. S. An, R. J. Molica, E. M. Jochimsen, S. Lau, K. L. Rinehart, G. R. Shaw, and G. K. Eaglesham. 2001. Human fatalities from cyanobacteria: Chemical and biological evidence for cyanotoxins. Environ. Health Perspect. 109:663–68. doi:10.1289/ehp.01109663.
   PubMed Web of Science ®Google Scholar
• Chen, X. G., X. Yang, L. L. Yang, B. D. Xiao, X. Q. Wu, J. T. Wang, and H. G. Wan. 2010. An effective pathway for the removal of microcystin LR via anoxic biodegradation in lake sediments. Water Res. 44:1884–92. doi:10.1016/j.watres.2009.11.025.
   PubMed Web of Science ®Google Scholar
• Chorus, I., I. R. Falconer, and H. J. Salas. 2000. Health risks caused by freshwater cyanobacteria in recreational waters. J. Toxicol. Environ. Health B 3:323–47. doi:10.1080/109374000436364.
   PubMed Web of Science ®Google Scholar
• Drobac, D., N. Tokodi, J. Lujic, Z. Marinovic, G. Subakov-Simic, T. Dulic, T. Vazic, S. Nybom, J. Meriluoto, G. A. Codd, et al. 2016. Cyanobacteria and cyanotoxins in fishponds and their effects on fish tissue. Harmful Algae 55:296. doi:10.1016/j.hal.2016.03.018.
   PubMed Web of Science ®Google Scholar
• Falconer, I. R. 2005. Is there a human health hazard from microcystins in the drinking water supply? Acta Hydrochim. Hydrobiol. 33:64–71. doi:10.1002/(ISSN)1521-401X.
   Google Scholar
• Gupta, N., S. C. Pant, R. Vijayaraghavan, and P. V. Rao. 2003. Comparative toxicity evaluation of cyanobacterial cyclic peptide toxin microcystin variants (LR, RR, YR) in mice. Toxicology 188:285–96. doi:10.1016/S0300-483X(03)00112-4.
   PubMed Web of Science ®Google Scholar
• Harada, K., S. Imanishi, H. Kato, M. Mizuno, E. Ito, and K. Tsuji. 2004. Isolation of Adda from microcystin-LR by microbial degradation. Toxicon 44:107–09. doi:10.1016/j.toxicon.2004.04.003.
   PubMed Web of Science ®Google Scholar
• Ho, L., D. Hoefel, C. P. Saint, and G. Newcombe. 2007. Isolation and identification of a novel microcystin-degrading bacterium from a biological sand filter. Water Res. 41:4685–95. doi:10.1016/j.watres.2007.06.057.
   PubMed Web of Science ®Google Scholar
• Holst, T., N. O. G. Jorgensen, C. Jorgensen, and A. Johansen. 2003. Degradation of microcystin in sediments at oxic and anoxic, denitrifying conditions. Water Res. 37:4748–60. doi:10.1016/S0043-1354(03)00413-5.
   PubMed Web of Science ®Google Scholar
• Howard, M. D. A., C. Nagoda, R. M. Kudela, K. Hayashi, A. Tatters, D. A. Caron, L. Busse, J. Brown, M. Sutula, and E. D. Stein. 2017. Microcystin prevalence throughout lentic waterbodies in Coastal Southern California. Toxins 9. doi:10.3390/toxins9070231.
   Web of Science ®Google Scholar
• Huisman, J., G. A. Codd, H. W. Paerl, B. W. Ibelings, J. M. H. Verspagen, and P. M. Visser. 2018. Cyanobacterial blooms. Nat. Rev. Microbiol. 16:471–83. doi:10.1038/s41579-018-0040-1.
   PubMed Web of Science ®Google Scholar
• Hunter, P. D., A. N. Tyler, D. J. Gilvear, and N. J. Willby. 2009. Using remote sensing to aid the assessment of human health risks from blooms of potentially toxic cyanobacteria. Environ. Sci. Technol. 43:2627–33. doi:10.1021/es802977u.
   PubMed Web of Science ®Google Scholar
• IARC Working Group on the Evaluation of Carcinogenic Risks to. 2010. IARC monographs on the evaluation of carcinogenic risks to humans. Ingested nitrate and nitrite, and cyanobacterial peptide toxins. IARC Monogr. Eval. Carcinogen Risks Human 94: 1–412.
   Google Scholar
• Jones, G. J., D. G. Bourne, R. L. Blakeley, and H. Doelle. 1994. Degradation of the cyanobacterial hepatotoxin microcystin by aquatic bacteria. Nat. Toxins 2:228–35. doi:10.1002/(ISSN)1056-9014.
   PubMedGoogle Scholar
• Li, J. M., R. H. Li, and J. Li. 2017. Current research scenario for microcystins biodegradation - A review on fundamental knowledge, application prospects and challenges. Sci. Total Environ. 595:615–32. doi:10.1016/j.scitotenv.2017.03.285.
   PubMed Web of Science ®Google Scholar
• Li, J. M., K. Shimizu, M. K. Sakharkar, M. Utsumi, Z. Y. Zhang, and N. Sugiura. 2011. Comparative study for the effects of variable nutrient conditions on the biodegradation of microcystin-LR and concurrent dynamics in microcystin-degrading gene abundance. Bioresour. Technol. 102:9509–17. doi:10.1016/j.biortech.2011.07.112.
   PubMed Web of Science ®Google Scholar
• Lyra, C., S. Suomalainen, M. Gugger, C. Vezie, P. Sundman, L. Paulin, and K. Sivonen. 2001. Molecular characterization of planktic cyanobacteria of Anabaena, Aphanizomenon, Microcystis and Planktothrix genera. Int. J. Syst. Evol. Microbiol. 51:513–26. doi:10.1099/00207713-51-2-513.
   PubMed Web of Science ®Google Scholar
• Ma, G. X., H. Y. Pei, W. R. Hu, X. C. Xu, C. X. Ma, and X. Q. Li. 2014. The removal of cyanobacteria and their metabolites through anoxic biodegradation in drinking water sludge. Bioresour. Technol. 165:191–98. doi:10.1016/j.biortech.2014.03.068.
   PubMed Web of Science ®Google Scholar
• Ma, G. X., H. Y. Pei, W. R. Hu, X. C. Xu, C. X. Ma, and R. T. Pei. 2016. Effects of glucose on microcystin-LR removal and the bacterial community composition through anoxic biodegradation in drinking water sludge. Environ. Technol. 37:64–73. doi:10.1080/09593330.2015.1063705.
   PubMed Web of Science ®Google Scholar
• MacKintosh, C., K. A. Beattie, S. Klumpp, P. Cohen, and G. A. Codd. 1990. Cyanobacterial microcystin-LR is a potent and specific inhibitor of protein phosphatases 1 and 2A from both mammals and higher plants. FEBS Lett. 264:187–92. doi:10.1016/0014-5793(90)80245-E.
   PubMed Web of Science ®Google Scholar
• Massey, I. Y., X. Zhang, and F. Yang. 2018. Importance of bacterial biodegradation and detoxification processes of microcystins for environmental health. J. Toxicol. Environ. Health B 21:357–69. doi:10.1080/10937404.2018.1532701.
   PubMed Web of Science ®Google Scholar
• Miller, M. A., R. M. Kudela, A. Mekebri, D. Crane, S. C. Oates, M. T. Tinker, M. Staedler, W. A. Miller, S. Toy-Choutka, C. Dominik, et al. 2010. Evidence for a novel marine harmful algal bloom: Cyanotoxin (Microcystin) transfer from land to sea otters. PLoS ONE 5:e12576. doi:10.1371/journal.pone.0012576.
   PubMed Web of Science ®Google Scholar
• Preece, E. P., B. C. Moore, and F. J. Hardy. 2015. Transfer of microcystin from freshwater lakes to puget sound, WA and toxin accumulation in marine mussels (Mytilus trossulus). Ecotoxicol. Environ. Saf. 122:98–105. doi:10.1016/j.ecoenv.2015.07.013.
   PubMed Web of Science ®Google Scholar
• Rastogi, R. P., R. P. Sinha, and A. Incharoensakdi. 2014. The cyanotoxin-microcystins: Current overview. Rev. Environ. Sci. BioTechnol. 13:215–49. doi:10.1007/s11157-014-9334-6.
   Web of Science ®Google Scholar
• Semyalo, R., T. Rohrlack, C. Naggawa, and G. W. Nyakairu. 2010. Microcystin concentrations in Nile tilapia (Oreochromis niloticus) caught from Murchison Bay, Lake Victoria and Lake Mburo: Uganda. Hydrobiologia 638:235–44. doi:10.1007/s10750-009-0047-8.
   Web of Science ®Google Scholar
• Shimizu, K., H. Maseda, K. Okano, T. Kurashima, Y. Kawauchi, Q. Xue, M. Utsumi, Z. Zhang, and N. Sugiura. 2012. Enzymatic pathway for biodegrading microcystin LR in Sphingopyxis sp. C-1. J. Biosci. Bioeng. 114:630–34. doi:10.1016/j.jbiosc.2012.07.004.
   PubMed Web of Science ®Google Scholar
• Takenaka, S., and M. F. Watanabe. 1997. Microcystin LR degradation by Pseudomonas aeruginosa alkaline protease. Chemosphere 34:749–57. doi:10.1016/S0045-6535(97)00002-7.
   PubMed Web of Science ®Google Scholar
• Tamura, K., J. Dudley, M. Nei, and S. Kumar. 2007. MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24:1596–99. doi:10.1093/molbev/msm092.
   PubMed Web of Science ®Google Scholar
• Wang, J., C. Zhang, J. Zhu, J. Ding, Y. Chen, and X. Han. 2019. Blood-brain barrier disruption and inflammation reaction in mice after chronic exposure to Microcystin-LR. Sci. Total Environ. 689:662–78. doi:10.1016/j.scitotenv.2019.06.387.
   PubMed Web of Science ®Google Scholar
• Wei, J., X. Xie, F. Huang, L. Xiang, Y. Wang, T. Han, I. Y. Massey, G. Liang, P. Yuepu, and F. Yang. 2019. Simultaneous Microcystis algicidal and microcystin synthesis inhibition by a red pigment prodigiosin. Environ. Pollut. 113444. doi:10.1016/j.envpol.2019.113444.
   PubMedGoogle Scholar
• World Health Organization (WHO). 1998. Cyanobacterial toxins: Microcystin-LR guidelines for drinking water. quality. Geneva: World Health Organization.
   Google Scholar
• Yan, H., J. Wang, J. Chen, W. Wei, H. Wang, and H. Wang. 2012. Characterization of the first step involved in enzymatic pathway for microcystin-RR biodegraded by Sphingopyxis sp. USTB-05. Chemosphere 87:12–18. doi:10.1016/j.chemosphere.2011.11.030.
   PubMed Web of Science ®Google Scholar
• Yang, F., J. Guo, F. Huang, I. Y. Massey, R. Huang, Y. Li, C. Wen, P. Ding, W. Zeng, and G. Liang. 2018a. Removal of microcystin-LR by a novel native effective bacterial community designated as YFMCD4 isolated from Lake Taihu. Toxins (Basel) 10. doi:10.3390/toxins10090363.
   Web of Science ®Google Scholar
• Yang, F., F. Huang, H. Feng, J. Wei, S. Hu, B. Li, I. Y. Massey, F. Zhang, K. Cao, G. Liang, et al. 2019. A novel route for detoxification of potentially carcinogenic cyanotoxin microcystin-LR in a unique bacterium. Water Res. (in press).
   Web of Science ®Google Scholar
• Yang, F., I. Y. Massey, J. Guo, S. Yang, Y. Pu, W. Zeng, and H. Tan. 2018b. Microcystin-LR degradation utilizing a novel effective indigenous bacterial community YFMCD1 from Lake Taihu. J. Toxicol. Environ. Health Part A 81:184–93. doi:10.1080/15287394.2018.1423803.
   PubMed Web of Science ®Google Scholar
• Yang, F., Y. Zhou, R. Sun, H. Wei, Y. Li, L. Yin, and Y. Pu. 2014. Biodegradation of microcystin-LR and-RR by a novel microcystin-degrading bacterium isolated from Lake Taihu. Biodegradation 25:447–57. doi:10.1007/s10532-013-9673-y.
   PubMed Web of Science ®Google Scholar
• Zhang, X. J., C. Chen, J. Q. Ding, A. Hou, Y. Li, Z. B. Niu, X. Y. Su, Y. J. Xu, and E. A. Laws. 2010. The 2007 water crisis in Wuxi, China: Analysis of the origin. J. Hazard. Mater. 182:130–35. doi:10.1016/j.jhazmat.2010.06.006.
   PubMed Web of Science ®Google Scholar
• Zhao, Y. Y., L. Q. Xie, and Y. J. Yan. 2015. Microcystin-LR impairs zebrafish reproduction by affecting oogenesis and endocrine system. Chemosphere 120:115–22. doi:10.1016/j.chemosphere.2014.06.028.
   PubMed Web of Science ®Google Scholar
• Zheng, C. F., H. Zeng, H. Lin, J. Wang, X. B. Feng, Z. Q. Qiu, J. A. Chen, J. H. Luo, Y. Luo, Y. J. Huang, et al. 2017. Serum microcystin levels positively linked with risk of hepatocellular carcinoma: A case-control study in southwest China. Hepatology 66:1519–28. doi:10.1002/hep.29310.
   PubMed Web of Science ®Google Scholar
• Zhou, Y., Y. Chen, M. Yuan, Z. Xiang, and X. Han. 2013. In vivo study on the effects of microcystin-LR on the apoptosis, proliferation and differentiation of rat testicular spermatogenic cells of male rats injected i.p. with toxins. J. Toxicol. Sci. 38:661–70. doi:10.2131/jts.38.661.
   PubMed Web of Science ®Google Scholar
• Zhu, F. P., Z. L. Han, J. L. Duan, X. S. Shi, T. T. Wang, G. P. Sheng, S. G. Wang, and X. Z. Yuan. 2019. A novel pathway for the anaerobic biotransformation of microcystin-LR using enrichment cultures. Environ. Pollut. 247:1064–70. doi:10.1016/j.envpol.2019.02.013.
   PubMed Web of Science ®Google Scholar
• Zhu, X. Y., Y. T. Shen, X. G. Chen, Y. O. O. Hu, H. Y. Xiang, J. Tao, and Y. Ling. 2016. Biodegradation mechanism of microcystin-LR by a novel isolate of Rhizobium sp TH and the evolutionary origin of the mlrA gene. Int Biodeterior. Biodegrad. 115:17–25. doi:10.1016/j.ibiod.2016.07.011.
   Web of Science ®Google Scholar
• Zurawell, R. W., H. Chen, J. M. Burke, and E. E. Prepas. 2005. Hepatotoxic cyanobacteria: A review of the biological importance of microcystins in freshwater environments. J. Toxicol. Environ. Health B 8:1–37. doi:10.1080/10937400590889412.
   PubMed Web of Science ®Google Scholar