Advertisement

Biodegradation of microcystin-RR and nutrient pollutants using Sphingopyxis sp. YF1 immobilized activated carbon fibers-sodium alginate

Abstract

A novel biological material named activated carbon fibers-sodium alginate@Sphingopyxis sp. YF1 (ACF-SA@YF1) was synthesized for microcystin-RR (MC-RR) and nutrient pollutant degradation in eutrophic water. The synthesized biomaterial was characterized by scanning electron microscopy (SEM). Box-Behnken design and response surface methodology (RSM) were utilized for the optimization of conditions during the MC-RR degradation. The degradation of MC-RR and nutrient pollutants was dynamically detected. The results revealed that the optimal conditions were temperature 32.51 °C, pH 6.860, and inoculum 14.97%. The removal efficiency of MC-RR, nitrogen, phosphorus, and chemical oxygen demand were 0.76 μg/mL/h, 32.45%, 94.57%, and 64.07%, respectively. In addition, ACF-SA@YF1 also performed satisfactory cyclic stability, while the MC-RR removal efficiency was 70.38% after seven cycles and 78.54% of initial activity after 20 days of storage. Therefore, it is reasonable to believe that ACF-SA@YF1 is an effective material which has a great prospect in removing MC-RR and nutrients from freshwater ecosystems.

This is a preview of subscription content, log in to check access.

Access options

Buy single article

Instant unlimited access to the full article PDF.

US$ 39.95

Price includes VAT for USA

Subscribe to journal

Immediate online access to all issues from 2019. Subscription will auto renew annually.

US$ 99

This is the net price. Taxes to be calculated in checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

References

  1. An XJ, Cheng Y, Huang MY, Sun YL, Wang HL (2018) Treating organic cyanide-containing groundwater by immobilization of a nitrile-degrading bacterium with a biofilm-forming bacterium using fluidized bed reactors. Environ Pollut 237:908–916. https://doi.org/10.1016/j.envpol.2018.01.087

  2. Babica P, Bláha L, Maršálek B (2005) Removal of microcystins by phototrophic biofilms. Environ Sci Pollut Res 12:369–374. https://doi.org/10.1065/espr2005.05.259

  3. Boshagh F, Rostami K, Moazami N (2019) Immobilization of Enterobacter aerogenes on carbon fiber and activated carbon to study hydrogen production enhancement. Biochem Eng J 144:64–72. https://doi.org/10.1016/j.bej.2019.01.014

  4. Cho JY, Jung HY, Kim JK (2019) Biodegraded mackerel wastewater selectively inhibits harmful algal blooms. J Hazard Mater 364:349–355. https://doi.org/10.1016/j.jhazmat.2018.10.053

  5. Daud NM, Abdullah SRS, Hasan H (2018) A response surface methodological analysis for the optimization of acid-catalyzed transesterification biodiesel wastewater pre-treatment using coagulation–flocculation process. Process Saf Environ Prot 113:184–192. https://doi.org/10.1016/j.psep.2017.10.006

  6. Díez-Quijada L, Puerto M, Gutiérrez-Praena D, Llana-Ruiz-Cabello M, Jos A, Cameán AM (2019) Microcystin-RR: occurrence, content in water and food and toxicological studies. A review. Environ Res 168:467–489. https://doi.org/10.1016/j.envres.2018.07.019

  7. Dziga D, Wasylewski M, Wladyka B, Nybom S, Meriluoto J (2013) Microbial degradation of microcystins. Chem Res Toxicol 26:841–852. https://doi.org/10.1021/tx4000045

  8. He Q, Kang L, Sun X, Jia R, Zhang Y, Ma J, Li H, Hi A (2018) Spatiotemporal distribution and potential risk assessment of microcystins in the Yulin River, a tributary of the three gorges reservoir, China. J Hazard Mater 347:184–195. https://doi.org/10.1016/j.jhazmat.2018.01.001

  9. He XX, Liu YL, Conklin A, Westrick J, Weavers LK, Dionysiou DD, Lenhart JJ, Mouser PJ, Szlag D, Walker HW (2016) Toxic cyanobacteria and drinking water: impacts, detection, and treatment. Harmful Algae 54:174–193. https://doi.org/10.1016/j.hal.2016.01.001

  10. He YF, Wu P, Li GY, Li L, Yi JC, Wang SL, Lu SY, Ding P, Chen CM, Pan HZ (2019a) Optimization on preparation of Fe3O4/chitosan as potential matrix material for the removal of microcystin-LR and its evaluation of adsorption properties. Int J Biol Macromol. https://doi.org/10.1016/j.ijbiomac.2019.11.209

  11. He YY, Wu P, Xiao W, Li GY, Yi JC, He YF, Chen CM, Ding P, Duan YY (2019b) Efficient removal of Pb(II) from aqueous solution by a novel ion imprinted magnetic biosorbent: adsorption kinetics and mechanisms. PLoS One 14:e0213377. https://doi.org/10.1371/journal.pone.0213377

  12. Hsieh F, Huang C, Lin TF, Chen YM, Lin JC (2008) Study of sodium tripolyphosphate-crosslinked chitosan beads entrapped with Pseudomonas putida for phenol degradation. Process Biochem 43:83–92. https://doi.org/10.1016/j.procbio.2007.10.016

  13. Jia J, Chen Q, Lauridsen TL (2016) A systematic investigation into the environmental fate of microcystins and the potential risk: study in lake Taihu. Toxins 8:170. https://doi.org/10.3390/toxins8060170

  14. Li C, Yang J, Xin W, Wang E, Li B, He R, Yuan H (2015) Removal of nitrogen by heterotrophic nitrification–aerobic denitrification of a phosphate accumulating bacterium Pseudomonas stutzeri YG-24. Bioresour Technol 182:18–25. https://doi.org/10.1016/j.biortech.2015.01.100

  15. Li CY, Li Y, Cheng XS, Feng LP, Xi CW, Zhang Y (2013) Immobilization of Rhodococcus rhodochrous BX2 (an acetonitrile-degrading bacterium) with biofilm- forming bacteria for wastewater treatment. Bioresour Technol 131:390–396. https://doi.org/10.1016/j.biortech.2012.12.140

  16. Li H, Ai H, Kang L, Sun X, He Q (2016) Simultaneous microcystis algicidal and microcystin degrading capability by a single Acinetobacter bacterial strain. Environ Sci Technol 50:11903–11911. https://doi.org/10.1021/acs.est.6b03986

  17. Li H, Pan G (2014) Enhanced and continued degradation of microcystins using microorganisms obtained through natural media. J Microbiol Methods 96:73–80. https://doi.org/10.1016/j.mimet.2013.11.005

  18. Li J, Li R, Li J (2017) Current research scenario for microcystins biodegradation - a review on fundamental knowledge, application prospects and challenges. Sci Total Environ 595:615–632. https://doi.org/10.1016/j.scitotenv.2017.03.285

  19. Lin K, Pei J, Li P, Ma J, Li Q, Yuan D (2018) Simultaneous determination of total dissolved nitrogen and total dissolved phosphorus in natural waters with an on-line UV and thermal digestion. Talanta 185:419–426. https://doi.org/10.1016/j.talanta.2018.03.085

  20. Liu QJ, Dai GZ, Bao YL (2017) Carbon nanotubes/carbon fiber hybrid material: a super support material for sludge biofilms. Environ Technol 39:2105–2116. https://doi.org/10.1080/09593330.2017.1351490

  21. Liu QJ, Zhang C, Bao YL, Dai GZ (2018) Carbon fibers with a nano-hydroxyapatite coating as an excellent biofilm support for bioreactors. Appl Surf Sci 443:255–265. https://doi.org/10.1016/j.apsusc.2018.02.120

  22. Liu YJ, Nikolausz M, Wang XC (2009) Biodegradation of phenol by using free and immobilized cells of Acinetobacter sp. XA05 and Sphingomonas sp. FG03. J Environ Sci Health A Tox Hazard Subst Environ Eng 44:130–136. https://doi.org/10.1016/j.bej.2008.12.001

  23. Ma XH, Li NJ, Jiang J, Xu QF, Li H, Wang LH, Lu JM (2013) Adsorption–synergic biodegradation of high-concentrated phenolic water by Pseudomonas putida immobilized on activated carbon fiber. J Environ Chem Eng 1:466–472. https://doi.org/10.1016/j.jece.2013.06.014

  24. Ma Y, Tie Z, Zhou M, Wang N, Cao X, Xie Y (2016) Accurate determination of low-level chemical oxygen demand using a multistep chemical oxidation digestion process for treating drinking water samples. Anal Methods 8:3839. https://doi.org/10.1039/c6ay00277c

  25. Maghsoudi E, Fortin N, Greer C, Maynard C, Pagé A, Duy SV, Sauvé S, Prévost M, Dorner S (2016) Cyanotoxin degradation activity and mlr gene expression profiles of a Sphingopyxis sp. isolated from Lake Champlain, Canada. Environ Sci Process Impacts 18:1417–1426. https://doi.org/10.1039/c6em00001k

  26. Massey IY, Yang F, Ding Z, Yang S, Guo J, Tezi C, Al-Osman M, Kamegni RB, Zeng W (2018) Exposure routes and health effects of microcystins on animals and humans: a mini-review. Toxicon 151:156–162. https://doi.org/10.1016/j.toxicon.2018.07.010

  27. McLellan NL, Manderville RA (2017) Toxic mechanisms of microcystins in mammals. Toxicol Res 6:391–405. https://doi.org/10.1039/C7TX00043J

  28. Merel S, Walker D, Chicana R, Snyder S, Baures E, Thomas O (2013) State of knowledge and concerns on cyanobacterial blooms and cyanotoxins. Environ Int 59:303–327. https://doi.org/10.1016/j.envint.2013.06.013

  29. Min M, Wang L, Li Y, Mohr MJ, Hu B, Zhou W, Chen P, Ruan R (2011) Cultivating Chlorella sp. in a pilot-scale photobioreactor using centrate wastewater for microalgae biomass production and wastewater nutrient removal. Appl Biochem Biotechnol 165:123–137. https://doi.org/10.1007/s12010-011-9238-7

  30. Okano K, Shimizu K, Kawauchi Y, Maseda H, Utsumi M, Zhang Z, Neilan BA, Sugiura N (2009) Characteristics of a microcystin-degrading bacterium under alkaline environmental conditions. J Toxicol 2009:954291. https://doi.org/10.1155/2009/954291

  31. Preece EP, Hardy FJ, Moore BC, Bryan M (2017) A review of microcystin detections in estuarine and marine waters: environmental implications and human health risk. Harmful Algae 61:31–45. https://doi.org/10.1016/j.hal.2016.11.006

  32. Qiao RP, Li N, Qi XH, Wang QS, Zhuang YY (2005) Degradation of microcystin-RR by UV radiation in the presence of hydrogen peroxide. Toxicon 45(6):745–752. https://doi.org/10.1016/j.toxicon.2005.01.012

  33. Rastogi RP, Sinha RP, Incharoensakdi A (2014) The cyanotoxin-microcystins: current overview. Rev Environ Sci Biotechnol 13:215–249. https://doi.org/10.1007/s11157-014-9334-6

  34. Rezaa M, Cuenca MA (2016) Simultaneous biological removal of nitrogen and phosphorus in a vertical bioreactor. J Environ Chem Eng 4:130–136. https://doi.org/10.1016/j.jece.2015.10.035

  35. Ruan B, Wu P, Chen M, Lai X, Chen L, Yu L, Gong B, Kang C, Dang Z, Shi Z, Liu Z (2018) Immobilization of Sphingomonas sp. GY2B in polyvinyl alcohol-alginate-kaolin beads for efficient degradation of phenol against unfavorable environmental factors. Ecotoxicol Environ Saf 162:103–111. https://doi.org/10.1016/j.ecoenv.2018.06.058

  36. Shi J, Podola B, Melkonian M (2014) Application of a prototype-scale twin-layer photobioreactor for effective N and P removal from different process stages of municipal wastewater by immobilized microalgae. Bioresour Technol 154:260–266. https://doi.org/10.1016/j.biortech.2013.11.100

  37. Su JF, Liang DH, Huang TL, Wei L, Ma M, Lu JS (2017) Enhancement of simultaneous algicidal and denitrification of immobilized Acinetobacter sp. J25 with magnetic Fe3O4 nanoparticles. Environ Sci Pollut Res 24:17853–17860. https://doi.org/10.1007/s11356-017-9380-z

  38. Sun ZY, Lv YK, Liu YX, Ren RP (2016) Removal of nitrogen by heterotrophic nitrification-aerobic denitrification of a novel metal resistant bacterium Cupriavidus sp. S1. Bioresour Technol 220:142–150. https://doi.org/10.1016/j.biortech.2016.07.110

  39. Sivasankar V, Nkonde MA, Govender P, Omine K, Kuvarega AT, Prabhakaran M, Msagati TAM (2017) Dendrimer supported Fe/Ni bimetallic composites immobilized in polyethersulfone membranes for effective degradation of arginine containing microcystins. Eur Polym J 98:456–467. https://doi.org/10.1016/j.eurpolymj.2017.11.049

  40. Tsao S, Wei DJ, Chang YT, Lee JF (2017) Aerobic biodegradation of microcystin-LR by an indigenous bacterial mixed culture isolated in Taiwan. Int Biodeterior Biodegradation 124:101–108. https://doi.org/10.1016/j.ibiod.2017.04.011

  41. Valeria AM, Ricardo EJ, Stephan P, Alberto WD (2006) Degradation of microcystin-RR by Sphingomonas sp. CBA4 isolated from San Roque reservoir (Co’rdoba – Argentina). Biodegradation 17:447–455. https://doi.org/10.1007/s10532-005-9015-9

  42. Wan WJ, He DL, Xue ZJ (2017) Removal of nitrogen and phosphorus by heterotrophic nitrification-aerobic denitrification of a denitrifying phosphorus-accumulating bacterium Enterobacter cloacae HW−15. Ecol Eng 99:199–208. https://doi.org/10.1016/j.ecoleng.2016.11.030

  43. Wang B, Xin M, Wei Q, Xie L (2018) A historical overview of coastal eutrophication in the China seas. Mar Pollut Bull 136:394–400. https://doi.org/10.1016/j.marpolbul.2018.09.044

  44. Wang X, Utsumi M, Yang YN, Shimizu K, Li DW, Zhang ZY, Sugiura N (2013) Removal of microcystins (−LR, -YR, −RR) by highly efficient photocatalyst Ag/Ag3PO4 under simulated solar light condition. Chem Eng J 230:172–179. https://doi.org/10.1016/j.cej.2013.06.076

  45. Wu P, Li GY, He YF, Luo D, Li L, Guo J, Ding P, Yang F (2019) High-efficient and sustainable biodegradation of microcystin-LR using Sphingopyxis sp. YF1 immobilized Fe3O4@chitosan. Colloid surface B 110633. https://doi.org/10.1016/j.colsurfb.2019.110633

  46. Wu L, Ge G, Wan L (2009) Biodegradation of oil wastewater by free and immobilized Yarrowia lipolytica W29. J Environ Sci 21:237–242. https://doi.org/10.1016/S1001-0742(08)62257-3

  47. Wu YP, He JZ, Yang LZ (2010) Evaluating adsorption and biodegradation mechanisms during the removal of microcystin-RR by periphyton. Environ Sci Technol 44(16):6319–6324. https://doi.org/10.1021/es903761y

  48. Wei J, Xie X, Huang F, Xiang L, Wang Y, Han TR, Massey IY, Liang GY, Pu XY, Yang F (2019) Simultaneous microcystis algicidal and microcystin synthesis inhibition by a red pigment prodigiosin. Environ Pollut 256:11344. https://doi.org/10.1016/j.envpol.2019.113444

  49. Xie GJ, Liu BF, Ding J, Xing DF, Ren HY, Guo WQ, Ren NQ (2012) Enhanced photo-H2 production by Rhodopseudomonas faecalis RLD-53 immobilization on activated carbon fibers. Biomass Bioenergy 44:122–129. https://doi.org/10.1016/j.biombioe.2012.05.002

  50. Yang F, Zhou Y, Sun R, Wei H, Li Y, Yin L, Pu Y (2014) Biodegradation of microcystin-LR and-RR by a novel microcystin-degrading bacterium isolated from Lake Taihu. Biodegradation 25:447–457. https://doi.org/10.1007/s10532-013-9673-y

  51. Yang F, Massey IY, Guo J, Yang S, Pu YP, Zeng W, Tan H (2018) Microcystin-LR degradation utilizing a novel effective indigenous bacterial community YFMCD1 from Lake Taihu. J Toxicol Environ Health A 81:184–193. https://doi.org/10.1080/15287394.2018.1423803

  52. Yang F, Huang F, Feng H, Wei J, Hu, Li B, Massey IY, Zhang F, Li L, Liang G, Kacew S, Zhang X, Pu Y (2019) A complete route for biodegradation of potentially carcinogenic cyanotoxin microcystin-LR in a novel indigenous bacterium. Water Res (in press)

  53. Yi JC, Wu P, Li GY, Xiao W, Li L, He YY, He YF, Ding P, Chen CM (2019) A composite prepared from carboxymethyl chitosan and aptamer-modified gold nanoparticles for the colorimetric determination of Salmonella typhimurium. Microchim Acta 186(11):711. https://doi.org/10.1007/s00604-019-3827-5

  54. Yi YL, Yu XB, Zhang C, Wang GX (2015) Growth inhibition and microcystin degradation effects of Acinetobacter guillouiae A2 on Microcystis aeruginosa. Res Microbiol 166:93–101. https://doi.org/10.1016/j.resmic.2014.12.013

  55. Zhang CY, Fu DG, Gu ZZ (2009) Degradation of microcystin-RR using boron-doped diamond electrode. J Hazard Mater 172:847–853. https://doi.org/10.1016/j.jhazmat.2009.07.071

  56. Zhang J, Lu Q, Ding Q, Yin L, PuY (2017) A novel and native microcystin-degrading bacterium of Sphingopyxis sp. Isolated from Lake Taihu. Int J Environ Res Public Health 14:1187. https://doi.org/10.3390/ijerph14101187

  57. Zhou DK, Hai RT, Wang WX, Zhao DL, Wang S (2012) Activated carbon fiber filler in aerated bioreactor for industrial wastewater treatment. Water Sci Technol 65:1753–1758. https://doi.org/10.2166/wst.2012.077

  58. Zhong Y, Jin XC, Qiao RP, Qi XH, Zhuang YY (2009) Destruction of microcystin-RR by Fenton oxidation. J Hazard Mater 167:1114–1118. https://doi.org/10.1016/j.jhazmat.2009.01.117

  59. Zhou J, Qin B, Han X, Zhu L (2016) Turbulence increases the risk of microcystin exposure in a eutrophic lake (Lake Taihu) during cyanobacterial bloom periods. Harmful Algae 55:213–220. https://doi.org/10.1016/j.hal.2016.03.016

  60. Zhu Y, Tu X, Chai XS, Wei Q, Guo L (2018) Biological activities and nitrogen and phosphorus removal during the anabaena flos-aquae biofilm growth using different nutrient form. Bioresour Technol 251:7–12. https://doi.org/10.1016/j.biortech.2017.12.003

  61. Zuo XJ, Cao YQ, Gong AJ, Ding SL, Zhang TW, Wang YJ (2016) Removal of microcystins by highly efficient photo-catalyst Bi2WO6-activated carbon under simulated light. Water Air Soil Pollut 227:97. https://doi.org/10.1007/s11270-016-2798-y

Download references

Author information

Conceptualization, Guofeng Ren, Xinghou He, Pian Wu, and Xinli Song; data curation, Guofeng Ren, Xinghou He, Yong Zhang, Shibiao Tang, and Yuandan Wei; formal analysis, Yong Zhang; methodology, Xinghou He, Pian Wu, Yayuan He, Xinli Song, and Yafei He; resources, Ping Ding and Fei Yang; supervision, Ping Ding; writing, original draft, Xinghou He; writing, review and editing, Pian Wu, Ping Ding, and Fei Yang.

Correspondence to Ping Ding or Fei Yang.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Responsible Editor: Vitor Manuel Oliveira Vasconcelos

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Ren, G., He, X., Wu, P. et al. Biodegradation of microcystin-RR and nutrient pollutants using Sphingopyxis sp. YF1 immobilized activated carbon fibers-sodium alginate. Environ Sci Pollut Res (2020). https://doi.org/10.1007/s11356-020-07640-8

Download citation

Keywords

  • Microcystin-RR
  • Biodegradation
  • Activated carbon fibers
  • Sphingopyxis sp. YF1
  • Nutrient pollutants