Biodegradation mechanism of microcystin-LR by a novel isolate of Rhizobium sp. TH and the evolutionary origin of the mlrA gene

International Biodeterioration and Biodegradation

Volumn 115, Issue , 2016, Pages 17-25

  Zhu, Xiaoyun ^a   Shen, Yitian ^a   Chen, Xiaoguo ^a   Hu, Yue O O ^b   Xiang, Huiyi ^a   Tao, Jia ^a   Ling, Yun ^a  

^a WUHAN UNIVERSITY OF TECHNOLOGY   (China)

^b ROYAL INSTITUTE OF TECHNOLOGY   (Sweden)

Author keywords

Degradation; Evolutionary origin; Mechanism; Microcystin; mlrA gene; Rhizobium

Indexed keywords

BACTERIA; DEGRADATION; ESCHERICHIA COLI; GENE EXPRESSION; GENE TRANSFER; GENES; MECHANISMS; RATE CONSTANTS; STRAIN; TOXIC MATERIALS;

ENVIRONMENTAL SAMPLE; EVOLUTIONARY ORIGIN; FIRST-ORDER RATE CONSTANTS; HETEROLOGOUS EXPRESSION; HORIZONTAL GENE TRANSFER; MICROCYSTINS; PHYLOGENETIC ANALYSIS; RHIZOBIUM;

BIODEGRADATION;

BIODEGRADATION; EUTROPHIC ENVIRONMENT; EVOLUTIONARY BIOLOGY; GENE; GENE TRANSFER; PHYLOGENETICS; REACTION KINETICS; RHIZOBACTERIUM; TOXIN;

ALPHAPROTEOBACTERIA; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; GAMMAPROTEOBACTERIA; PROTEOBACTERIA; RHIZOBIUM; RHIZOBIUM SP.; SPHINGOMONADALES;

EID: 84979710830     PISSN: 09648305     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ibiod.2016.07.011     Document Type: Article

References (42)

1. Bourne, D.G., Jones, G.J., Blakeley, R.L., Jones, A., Negri, A.P., Riddles, P., Enzymatic pathway for the bacterial degradation of the cyanobacterial cyclic peptide toxin microcystin LR. Appl. Environ. Microbiol. 62 (1996), 4086–4094.
2. Bourne, D.G., Riddles, P., Jones, G.J., Smith, W., Blakeley, R.L., Characterisation of a gene cluster involved in bacterial degradation of the cyanobacterial toxin microcystin LR. Environ. Toxicol. 16 (2001), 523–534, 10.1002/tox.10013.
3. Chen, J., Hu, L.B., Zhou, W., Yan, S.H., Yang, J.D., Xue, Y.F., Shi, Z.Q., Degradation of microcystin-LR and RR by a Stenotrophomonas sp. Strain EMS isolated from lake Taihu, China. Int. J. Mol. Sci. 11 (2010), 896–911, 10.3390/ijms11030896.
4. Chen, X., Yang, X., Yang, L., Xiao, B., Wu, X., Wang, J., Wan, H., An effective pathway for the removal of microcystin LR via anoxic biodegradation in lake sediments. Water Res. 44 (2010), 1884–1892, 10.1016/j.watres.2009.11.025.
5. Cousins, I.T., Bealing, D.J., James, H.A., Sutton, A., Biodegradation of microcystin-LR by indigenous mixed bacterial populations. Water Res. 30 (1996), 481–485, 10.1016/0043-1354(95)00189-1.
6. Dziga, D., Wasylewski, M., Szetela, A., Bochenska, O., Wladyka, B., Verification of the role of MlrC in microcystin biodegradation by studies using a heterologously expressed enzyme. Chem. Res. Toxicol. 25 (2012), 1192–1194, 10.1021/tx300174e.
7. Dziga, D., Wladyka, B., Zielińska, G., Meriluoto, J., Wasylewski, M., Heterologous expression and characterisation of microcystinase. Toxicon 59 (2012), 578–586, 10.1016/j.toxicon.2012.01.001.
8. Eleuterio, L., Batista, J.R., Biodegradation studies and sequencing of microcystin-LR degrading bacteria isolated from a drinking water biofilter and a fresh water lake. Toxicon 55 (2010), 1434–1442, 10.1016/j.toxicon.2010.02.020.
9. Giaramida, L., Manage, P.M., Edwards, C., Singh, B.K., Lawton, L.A., Bacterial communities' response to microcystins exposure and nutrient availability: linking degradation capacity to community structure. Int. Biodeterior. Biodegrad. 84 (2013), 111–117, 10.1016/j.ibiod.2012.05.036.
10. Hall, T., Hart, J., Croll, B., Gregory, R., Laboratory-scale investigations of algal toxin removal by water treatment. J. Chart. Inst. Water Environ. Manag. 14 (2000), 143–149, 10.1111/j.1747-6593.2000.tb00241.x.
11. Harada, K.-I., Imanishi, S., Kato, H., Mizuno, M., Ito, E., Tsuji, K., Isolation of Adda from microcystin-LR by microbial degradation. Toxicon 44 (2004), 107–109, 10.1016/j.toxicon.2004.04.003.
12. Ho, L., Hoefel, D., Saint, C.P., Newcombe, G., Isolation and identification of a novel microcystin-degrading bacterium from a biological sand filter. Water Res. 41 (2007), 4685–4695, 10.1016/j.watres.2007.06.057.
13. Ho, L., Sawade, E., Newcombe, G., Biological treatment options for cyanobacteria metabolite removal - a review. Water Res. 46 (2012), 1536–1548, 10.1016/j.watres.2011.11.018.
14. Ho, L., Tang, T., Monis, P.T., Hoefel, D., Biodegradation of multiple cyanobacterial metabolites in drinking water supplies. Chemosphere 87 (2012), 1149–1154, 10.1016/j.chemosphere.2012.02.020.
15. Hu, L.B., Yang, J.D., Zhou, W., Yin, Y.F., Chen, J., Shi, Z.Q., Isolation of a Methylobacillus sp. that degrades Microcyctin toxins associated with cyanobacteria. New Biotechnol. 26 (2009), 205–211, 10.1016/j.nbt.2009.09.001.
16. Ishii, H., Nishijima, M., Abe, T., Characterization of degradation process of cyanobacterial hepatotoxins by a gram-negative aerobic bacterium. Water Res. 38 (2004), 2667–2676, 10.1016/j.watres.2004.03.014.
17. Jiang, Y., Shao, J., Wu, X., Xu, Y., Li, R., Active and silent members in the mlr gene cluster of a microcystin-degrading bacterium isolated from Lake Taihu, China. Fems Microbiol. Lett. 322 (2011), 108–114, 10.1111/j.1574-6968.2011.02337.x.
18. Lam, A.K.-Y., Fedorak, P.M., Prepas, E.E., Biotransformation of the cyanobacterial hepatotoxin microcystin-LR, as determined by HPLC and protein phosphatase bioassay. Environ. Sci. Technol. 29 (1995), 242–246, 10.1021/es00001a030.
19. Lawton, L.A., Edwards, C., Codd, G.A., Extraction and high-performance liquid chromatographic method for the determination of microcystins in raw and treated waters. Analyst 119 (1994), 1525–1530, 10.1039/an9941901525.
20. Li, H., Pan, G., Enhanced and continued degradation of microcystins using microorganisms obtained through natural media. J. Microbiol. Methods 96 (2014), 73–80, 10.1016/j.mimet.2013.11.005.
21. Li, J., Shimizu, K., Maseda, H., Lu, Z., Utsumi, M., Zhang, Z., Sugiura, N., 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 (2012), 27–35, 10.1016/j.biortech.2011.11.099.
22. Manage, P.M., Edwards, C., Singh, B.K., Lawton, L.A., Isolation and identification of novel microcystin-degrading bacteria. Appl. Environ. Microbiol. 75 (2009), 6924–6928, 10.1128/aem.01928-09.
23. Maruyama, T., Park, H.D., Ozawa, K., Tanaka, Y., Sumino, T., Hamana, K., Hiraishi, A., Kato, K., Sphingosinicella microcystinivorans gen. nov., sp nov., a microcystin-degrading bacterium. Int. J. Syst. Evol. Microbiol. 56 (2006), 85–89, 10.1099/ijs.0.63789-0.
24. Okano, K., Shimizu, K., Kawauchi, Y., Maseda, H., Utsumi, M., Zhang, Z., Neilan, B.A., Sugiura, N., Characteristics of a microcystin-degrading bacterium under alkaline environmental conditions. J. Toxicol., 2009, 10.1155/2009/954291.
25. Park, H.-D., Sasaki, Y., Maruyama, T., Yanagisawa, E., Hiraishi, A., Kato, K., Degradation of the cyanobacterial hepatotoxin microcystin by a new bacterium isolated from a hypertrophic lake. Environ. Toxicol. 16 (2001), 337–343, 10.1002/tox.1041.
26. Ramani, A., Rein, K., Shetty, K.G., Jayachandran, K., Microbial degradation of microcystin in Florida's freshwaters. Biodegradation 23 (2012), 35–45, 10.1007/s10532-011-9484-y.
27. Rapala, J., Berg, K.A., Lyra, C., Niemi, R.M., Manz, W., Suomalainen, S., Paulin, L., Lahti, K., Paucibacter toxinivorans gen. nov., sp nov., a bacterium that degrades cyclic cyanobacterial hepatotoxins microcystins and nodularin. Int. J. Syst. Evol. Microbiol. 55 (2005), 1563–1568, 10.1099/ijs.0.63599-0.
28. Rastogi, R.P., Sinha, R.P., Incharoensakdi, A., The cyanotoxin-microcystins: current overview. Rev. Environ. Sci. Bio Technol. 13 (2014), 215–249, 10.1007/s11157-014-9334-6.
29. Saito, T., Okano, K., Park, H.D., Itayama, T., Inamori, Y., Neilan, B.A., Burns, B.P., Sugiura, N., Detection and sequencing of the microcystin LR-degrading gene, mlrA, from new bacteria isolated from Japanese lakes. Fems Microbiol. Lett. 229 (2003), 271–276, 10.1016/S0378-1097(03)00847-4.
30. Shimizu, K., Maseda, H., Okano, K., Itayama, T., Kawauchi, Y., Chen, R., Utsumi, M., Zhang, Z., Sugiura, N., How microcystin-degrading bacteria express microcystin degradation activity. Lakes Reservoirs Res. Manag. 16 (2011), 169–178, 10.1111/j.1440-1770.2011.00480.x.
31. Shimizu, K., Maseda, H., Okano, K., Kurashima, T., Kawauchi, Y., Xue, Q., Utsumi, M., Zhang, Z., Sugiura, N., Enzymatic pathway for biodegrading microcystin LR in Sphingopyxis sp. C-1. J. Biosci. Bioeng. 114 (2012), 630–634, 10.1016/j.jbiosc.2012.07.004.
32. Somdee, T., Thunders, M., Ruck, J., Lys, I., Allison, M., Page, R., Degradation of Dha(7) MC-LR by a microcystin degrading bacterium isolated from lake Rotoiti, New Zealand. ISRN Microbiol., 2013, 2013, 10.1155/2013/596429 596429–596429.
33. Song, H., Reichwaldt, E.S., Ghadouani, A., Contribution of sediments in the removal of microcystin-LR from water. Toxicon 83 (2014), 84–90, 10.1016/j.toxicon.2014.02.019.
34. Song, L.R., Chen, W., Peng, L., Wan, N., Gan, N.Q., Zhang, X.M., 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 (2007), 2853–2864, 10.1016/j.watres.2007.02.013.
35. Svirčev, Z., Baltić, V., Gantar, M., Juković, M., Stojanović, D., Baltić, M., Molecular aspects of microcystin-induced hepatotoxicity and hepatocarcinogenesis. J. Environ. Sci. Health, Part C 28 (2010), 39–59, 10.1080/10590500903585382.
36. Valeria, A.M., Ricardo, E.J., Pflugmacher, S., Alberto, W.D., Degradation of microcystin-RR by Sphingomonas sp. CBA4 isolated from San Roque reservoir (Córdoba – Argentina). Biodegradation 17 (2006), 447–455, 10.1007/s10532-005-9015-9.
37. Yan, H., Wang, J., Chen, J., Wei, W., Wang, H., Wang, H., Characterization of the first step involved in enzymatic pathway for microcystin-RR biodegraded by Sphingopyxis sp. USTB-05. Chemosphere 87 (2012), 12–18, 10.1016/j.chemosphere.2011.11.030.
38. Yang, F., Zhou, Y., Sun, R., Wei, H., Li, Y., Yin, L., Pu, Y., Biodegradation of microcystin-LR and-RR by a novel microcystin-degrading bacterium isolated from Lake Taihu. Biodegradation 25 (2014), 447–457, 10.1007/s10532-013-9673-y.
39. Yang, F., Zhou, Y., Yin, L., Zhu, G., Liang, G., Pu, Y., Microcystin-degrading activity of an indigenous bacterial strain Stenotrophomonas acidaminiphila MC-LTH2 Isolated from Lake Taihu. PloS One, 9, 2014, e86216, 10.1371/journal.pone.0086216.
40. Yang, Z., Rannala, B., Molecular phylogenetics: principles and practice. Nat. Rev. Genet. 13 (2012), 303–314, 10.1038/nrg3186.
41. You, D.-J., Chen, X.-G., Xiang, H.-Y., Ouyang, L., Yang, B., Isolation, identification and characterization of a microcystin-degrading bacterium Paucibacter sp. strain CH. Environ. Sci. (in Chinese) 35 (2014), 313–318.
42. Zhang, M.L., Yan, H., Pan, G., Microbial degradation of microcystin-LR by Ralstonia solanacearum. Environmental Technology 32 (2011), 1779–1787, 10.1080/09593330.2011.556148.