Abstract
Microcystin-LR (MC-LR) and microcystin-RR (MC-RR) are the two most common microcystins (MCs) present in fresh water posing a direct threat to public health because of their hepatotoxicity. A novel MC-degrading bacterium designated MC-LTH1 capable of degrading MC-LR and -RR was isolated, and the degradation rates and mechanisms of MC-LR and -RR for this bacterium were investigated. The bacterium was identified as Bordetella sp. and shown to possess a homologous mlrA gene responsible for degrading MCs. To the best of our knowledge, this is the first report of mlrA gene detection in Bordetella species. MC-LR and -RR were completely degraded separately at rates of 0.31 mg/(L h) and 0.17 mg/(L h). However, the degradation rates of MC-LR and -RR decreased surprisingly to 0.27 mg/(L h) and 0.12 mg/(L h), respectively, when both of them were simultaneously present. Degradation products were identified by high performance liquid chromatography coupled with time-of-flight mass spectrometry. Adda (m/z 332.2215, C20H29NO3) commonly known as a final product of MC degradation by isolated bacteria was detected as an intermediate in this study. Linearized MC-LR (m/z 1013.5638, C49H76N10O13), linearized MC-RR (m/z 1056.4970, C49H77N13O13), and tetrapeptide (m/z 615.3394, C32H46N4O8) were also detected as intermediates. These results indicate that the bacterial strain MC-LTH1 is quite efficient for the detoxification of MC-LR and MC-RR, and possesses significant bioremediation potential.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Alamri SA (2012) Biodegradation of microcystin-RR by Bacillus flexus isolated from a Saudi freshwater lake. Saudi J Biol Sci 19(4):435–440. doi:10.1016/j.sjbs.2012.06.006
Bourne DG, Jones GJ, Blakeley RL, Jones A, Negri AP, Riddles P (1996) Enzymatic pathway for the bacterial degradation of the cyanobacterial cyclic peptide toxin microcystin LR. Appl Environ Microbiol 62(11):4086–4094
Bourne DG, Riddles P, Jones GJ, Smith W, Blakeley RL (2001) Characterisation of a gene cluster involved in bacterial degradation of the cyanobacterial toxin microcystin LR. Environ Toxicol 16(6):523–534. doi:10.1002/tox.10013
Bourne DG, Blakeley RL, Riddles P, Jones GJ (2006) Biodegradation of the cyanobacterial toxin microcystin LR in natural water and biologically active slow sand filters. Water Res 40(6):1294–1302. doi:10.1016/j.watres.2006.01.022
Chen W, Song LR, Peng L, Wan N, Zhang XM, Gan NQ (2008) Reduction in microcystin concentrations in large and shallow lakes: water and sediment-interface contributions. Water Res 42(3):763–773. doi:10.1016/j.watres.2007.08.007
Chen J, Hu LB, Zhou W, Yan SH, Yang JD, Xue YF, Shi ZQ (2010) Degradation of microcystin-LR and RR by a Stenotrophomonas sp. strain EMS isolated from Lake Taihu, China. Int J Mol Sci 11(3):896–911. doi:10.3390/ijms11030896
Chen P, Zhu LY, Fang SH, Wang CY, Shan GQ (2012) Photocatalytic degradation efficiency and mechanism of microcystin-RR by mesoporous Bi2WO6 under near ultraviolet light. Environ Sci Technol 46(4):2345–2351. doi:10.1021/es2036338
Codd GA, Bell SG, Kaya K, Ward CJ, Beattie KA, Metcalf JS (1999) Cyanobacterial toxins, exposure routes and human health. Eur J Phycol 34(4):405–415. doi:10.1017/s0967026299002255
Gagala I, Mankiewicz-Boczek J (2012) The natural degradation of microcystins (cyanobacterial hepatotoxins) in fresh water—the future of modern treatment systems and water quality improvement. Pol J Environ Stud 21(5):1125–1139
Harada K, Imanishi S, Kato H, Mizuno M, Ito E, Tsuji K (2004) Isolation of Adda from microcystin-LR by microbial degradation. Toxicon 44(1):107–109. doi:10.1016/toxicon.2004.04.003
Ho L, Hoefel D, Saint CP, Newcombe G (2007) Isolation and identification of a novel microcystin-degrading bacterium from a biological sand filter. Water Res 41(20):4685–4695. doi:10.1016/j.watres.2007.06.057
Hu LB, Yang JD, Zhou W, Yin YF, Chen J, Shi ZQ (2009) Isolation of a Methylobacillus sp. that degrades microcystin toxins associated with cyanobacteria. N Biotechnol 26(3–4):205–211. doi:10.1016/j.nbt.2009.09.001
Imanishi S, Kato H, Mizuno M, Tsuji K, Harada K (2005) Bacterial degradation of microcystins and nodularin. Chem Res Toxicol 18(3):591–598. doi:10.1021/tx049677g
Ito E, Takai A, Kondo F, Masui H, Imanishi S, Harada K (2002) Comparison of protein phosphatase inhibitory activity and apparent toxicity of microcystins and related compounds. Toxicon 40(7):1017–1025. doi:10.1016/S0041-0101(02)00099-5
Jones GJ, Bourne DG, Blakeley RL, Doelle H (1994) Degradation of the cyanobacterial hepatotoxin microcystin by aquatic bacteria. Nat Toxins 2(4):228–235. doi:10.1002/nt.2620020412
Li JM, Shimizu K, Sakharkar MK, Utsumi M, Zhang ZY, Sugiura N (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(20):9509–9517. doi:10.1016/j.biortech.2011.07.112
Li JM, Shimizu K, Maseda H, Lu ZJ, Utsumi M, Zhang ZY, Sugiura N (2012) Investigations into the biodegradation of microcystin-LR mediated by the biofilm in wintertime from a biological treatment facility in a drinking-water treatment plant. Bioresour Technol 106:27–35. doi:10.1016/j.biortech.2011.11.099
Liu YQ, Xie P, Zhang DW, Wen ZR (2008) Seasonal dynamics of microcystins with associated biotic and abiotic parameters in two bays of Lake Taihu, the third largest freshwater lake in China. Bull Environ Contam Toxicol 80(1):24–29. doi:10.1007/s00128-007-9293-5
MacKintosh C, Beattie KA, Klumpp S, Cohen P, Codd GA (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(2):187–192. doi:10.1016/0014-5793(90)80245-E
Manage PM, Edwards C, Singh BK, Lawton LA (2009) Isolation and identification of novel microcystin-degrading bacteria. Appl Environ Microbiol 75(21):6924–6928. doi:10.1128/aem.01928-09
Park HD, Sasaki Y, Maruyama T, Yanagisawa E, Hiraishi A, Kato K (2001) Degradation of the cyanobacterial hepatotoxin microcystin by a new bacterium isolated from a hypertrophic lake. Environ Toxicol 16(4):337–343. doi:10.1002/tox.1041
Saito T, Okano K, Park HD, Itayama T, Inamori Y, Neilan BA, Burns BP, Sugiura N (2003) Detection and sequencing of the microcystin LR-degrading gene, mlrA, from new bacteria isolated from Japanese. FEMS Microbiol Lett 229(2):271–276. doi:10.1016/s0378-1097(03)00847-4
Shimizu K, Maseda H, Okano K, Kurashima T, Kawauchi Y, Xue Q, Utsumi M, Zhang ZY, Sugiura N (2012) Enzymatic pathway for biodegrading microcystin LR in Sphingopyxis sp. C-1. J Biosci Bioeng 114(6):630–634. doi:10.1016/j.jbiosc.2012.07.004
Song L, Chen W, Peng L, Wan N, Gan N, Zhang X (2007) Distribution and bioaccumulation of microcystins in water columns: a systematic investigation into the environmental fate and the risks associated with microcystins in Meiliang Bay, Lake Taihu. Water Res 41(13):2853–2864. doi:10.1016/j.watres.2007.02.013
Takenaka S, Watanabe MF (1997) Microcystin LR degradation by Pseudomonas aeruginosa alkaline protease. Chemosphere 34(4):749–757. doi:10.1016/s0045-6535(97)00002-7
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28(10):2731–2739. doi:10.1093/molbev/msr121
Tsuji K, Asakawa M, Anzai Y, Sumino T, Harada K (2006) Degradation of microcystins using immobilized microorganism isolated in an eutrophic lake. Chemosphere 65(1):117–124. doi:10.1016/j.chemosphere.2006.02.018
Valeria AM, Ricardo EJ, Stephan P, Alberto WD (2006) Degradation of microcystin-RR by Sphingomonas sp. CBA4 isolated from San Roque reservoir (Cordoba—Argentina). Biodegradation 17(5):447–455. doi:10.1007/s10532-005-9015-9
Wang JF, Wu PF, Chen J, Yan H (2010) Biodegradation of microcystin-RR by a new isolated Sphingopyxis sp. USTB-05. Chin J Chem Eng 18(1):108–112. doi:10.1016/s1004-9541(08)60330-4
Wang SC, Geng ZZ, Wang Y, Tong ZH, Yu HQ (2012) Essential Roles of p53 and MAPK cascades in microcystin-LR-induced germline apoptosis in Caenorhabditis elegans. Environ Sci Technol 46(6):3442–3448. doi:10.1021/es203675y
Yan H, Wang JF, Chen J, Wei W, Wang HS, Wang H (2012) Characterization of the first step involved in enzymatic pathway for microcystin-RR biodegraded by Sphingopyxis sp. USTB-05. Chemosphere 87(1):12–18. doi:10.1016/j.chemosphere.2011.11.030
Yang H, Xie P, Xu J, Zheng L, Deng D, Zhou Q, Wu S (2006) Seasonal variation of microcystin concentration in Lake Chaohu, a shallow subtropical lake in the People’s Republic of China. Bull Environ Contam Toxicol 77(3):367–374. doi:10.1007/s00128-006-1075-y
Yang F, Wei HY, Li XQ, Li YH, Li XB, Yin LH, Pu YP (2013) Isolation and characterization of an algicidal bacterium indigenous to Lake Taihu with a red pigment able to lyse Microcystis aeruginosa. Biomed Environ Sci 26(2):148–154. doi:10.3967/0895-3988.2013.02.009
Acknowledgments
The authors are grateful to Michael Cunningham from the University of Maryland for help with language polishing, and Guangcan Zhu, Ran Yu, and Ying Zhan for help on HPLC–TOF-MS data analysis. This research was supported by the National Natural Science Foundation of China (30972440), the National Science and Technology Major Project (2012ZX07101-005), and the Jiangsu Province postgraduate Innovation Project (CX10B–087Z).
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Yang, F., Zhou, Y., Sun, R. et al. Biodegradation of microcystin-LR and-RR by a novel microcystin-degrading bacterium isolated from Lake Taihu. Biodegradation 25, 447–457 (2014). https://doi.org/10.1007/s10532-013-9673-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10532-013-9673-y