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Ecotoxicology

, Volume 28, Issue 1, pp 37–47 | Cite as

Effect of Bacillus cereus on the ecotoxicity of metal-based fungicide spiked soils: Earthworm bioassay

  • Oluwatosin G. Oladipo
  • Adam F. Burt
  • Mark S. MaboetaEmail author
Article

Abstract

Soil microorganisms exhibit varying levels of metal tolerance across a diverse range of environmental conditions. The use of metal-based fungicides such as mancozeb and copper oxychloride could potentially result in increased levels of manganese, zinc and copper which may adversely affect soil mesofauna. Under standardized earthworm bioassay conditions (temperature, pH, soil type and water content), we investigated the effect of Bacillus cereus on mancozeb and copper oxychloride ecotoxicity towards Eisenia andrei. A metal-tolerant Bacillus cereus strain previously isolated from a gold mining site was introduced into fungicide spiked soils. Earthworms were exposed to bacterial inoculated and non-inoculated substrates of mancozeb (8, 44, 800 and 1250 mg kg−1) and copper oxychloride (200, 450, 675 and 1000 mg kg−1). Experimental trials assessed avoidance-behavior, growth and reproduction utilizing standardized protocols (ISO and OECD). In the avoidance-behavior, E. andrei showed significant (p< 0.05) preference for inoculated substrates. Further, significant (p< 0.05) increases in biomass, survival, cocoons, juveniles and lower soil and tissue Mn, Cu and Zn contents were recorded at 8 and 44 mg kg−1 mancozeb and copper oxychloride 200 and 450 mg kg−1 inoculated soils compared to non-inoculated. However, at 800 and 1250 mg kg−1 mancozeb and 675 and 1000 mg kg−1 copper oxychloride concentrations, reproductive success in both inoculated and non-inoculated treatments was negatively (p< 0.05) affected. In conclusion, Bacillus cereus decreased the ecotoxicity of metal-based fungicides towards Eisenia andrei at 8 and 44 mg kg−1 mancozeb and 200 and 450 mg kg−1 copper oxychloride concentrations. The outcome observed with the inoculated substrates at elevated fungicides concentrations maybe as a result of the environmental conditions (pH and temperature).

Keywords

Bacillus cereus Bioaugmentation Eisenia andrei Fungicides Heavy metals Soil pollution 

Notes

Acknowledgements

The financial assistance of the National Research Foundation (NRF), South Africa, towards this research is hereby acknowledged. Opinions expressed and conclusions arrived at, are those of the authors and are not necessarily to be attributed to the NRF. We also appreciate the North-West University, South Africa for the financial support.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Ahemad M, Khan MS (2012) Productivity of greengram in tebuconazole-stressed soil, by using a tolerant and plant growth-promoting Bradyrhizobium sp. MRM6 strain. Acta Physiol Plant 34:245–254CrossRefGoogle Scholar
  2. Ashraf MA, Hussain I, Rasheed R, Iqbal M, Riaz M, Arif MS (2017) Advances in microbe-assisted reclamation of heavy metal contaminated soils over the last decade: A review. J Environ Manag 198:132–143CrossRefGoogle Scholar
  3. Baćmaga M, Wyszkowska J, Kucharski J (2017) Bioaugmentation of soil contaminated with azoxystrobin. Water, Air & Soil Pollut 228:19CrossRefGoogle Scholar
  4. Bouyoucos GF (1962) Hydrometer method improved for making particle size analysis of soils. Agron J 54(5):464–465CrossRefGoogle Scholar
  5. Buch AC, Brown GG, Niva C, Sautter KD, Sousa JP (2013) Toxicity of three pesticides commonly used in Brazil to Pontoscolex corethrurus (Müller, 1857) and Eisenia andrei (Bouché, 1972). Appl Soil Ecol 69:32–38CrossRefGoogle Scholar
  6. Burrows LA, Edwards CA (2002) The use of integrated soil microcosms to predict effects of pesticides on soil ecosystems. Eur J Soil Biol 38:245–249CrossRefGoogle Scholar
  7. Cele EN, Maboeta M (2016) Amelioration of iron mine soils with biosolids: Effects on plant tissue metal content and earthworms. Environ Sci & Pollut Res 23:23005–23016CrossRefGoogle Scholar
  8. Chau JF, Bagtzoglou AC, Willig MR (2011) The effect of soil texture on richness and diversity of bacterial communities. Environ Forensics 12:333–341CrossRefGoogle Scholar
  9. Cycoń M, Mrozik A, Piotrowska-Seget Z (2017) Bioaugmentation as a strategy for the remediation of pesticide-polluted soil: A review. Chemosphere 172:52–71CrossRefGoogle Scholar
  10. Dai J, Becquer T, Rouiller JH, Reversat G, Bernhard-Reversat F, Nahmani J, Lavelle P (2004) Heavy metal accumulation by two earthworm species and its relationship to total and DTPA extractable metals in soils. Soil Biol Biochem 36:91–98CrossRefGoogle Scholar
  11. De Silva PMCS, Pathiratne A, van Gestel CAM (2010) Toxicity of chlorpyrifos, carbofuran, mancozeb and their formulations to the tropical earthworm Perionyx excavatus. Appl Soil Ecol 44:56–60CrossRefGoogle Scholar
  12. Demuynck S, Grumiaux F, Mottier V, Schikorski D, Lemière S, Lelprêtre A (2007) Cd/Zn exposure interactions on metallothionein response in Eisenia fetida (Annelida, Oligochaeta). Comperative Biochem Physiol 145:658–668Google Scholar
  13. Dybas MJ, Tatara GM, Knoll WH, Mayotte TJ, Criddle CS (1995) Niche adjustment for bioaugmentation with Pseudomonas sp. strain KC. In: Hinchee RE, Fredrickson J, Alleman BC (Eds.) Bioaugmentation for site remediation. Battelle Press, Columbus, p 77–84Google Scholar
  14. Eijsackers H, Beneke P, Maboeta M, Louw JPE, Reinecke AJ (2005) The implications of copper fungicide usage in vineyards for earthworm activity and resulting sustainable soil quality. Ecotoxicol & Environ Saf 62:99–111CrossRefGoogle Scholar
  15. Farhan M, Ali-Butt Z, Khan AU, Wahid A, Ahmad M, Ahmad F, Kanwal A (2014) Enhanced biodegradation of chlorpyrifos by agricultural soil isolate. Asian J Chem 26:3013–3017CrossRefGoogle Scholar
  16. Fashola MO, Ngole-Jeme VM, Babalola OO (2016) Heavy metal pollution from gold mines: environmental effects and bacterial strategies for resistance. Int J Environ Res & Public Health 13:1047CrossRefGoogle Scholar
  17. Fauziah SH, Agamuthu P, Hashim R, Izyani AK, Emenike CU (2017) Assessing the bioaugmentation potentials of individual isolates from landfill on metal-polluted soil. Environ & Earth Sci 76:401CrossRefGoogle Scholar
  18. García-Santos G, Keller-Forrer K (2011) Avoidance behaviour of Eisenia fetida to carbofuran, chlorpyrifos, mancozeb and metamidophos in natural soils from the highlands of Colombia. Chemosphere 84:651–656CrossRefGoogle Scholar
  19. Gomes MA, da C, Hauser-Davis RA, de Souza AN, Vitoria AP (2016) Metal phytoremediation: general strategies, genetically modified plants and applications in metal nanoparticle contamination. Ecotoxicol & Environ Saf 134:133–147CrossRefGoogle Scholar
  20. Helling B, Reinecke SA, Reinecke AJ (2000) Effects of the fungicide copper oxychloride on the growth and reproduction of Eisenia fetida (Oligochaeta). Ecotoxicol & Environ Saf 46(1):108–116CrossRefGoogle Scholar
  21. Hong Q, Zhang Z, Hong Y, Li SA (2007) Microcosm study on bioremediation of fenitrothion-contaminated soil using Burkholderia sp. FDS-1. Int J Biodeterior & Biodegrad 59:55–61CrossRefGoogle Scholar
  22. ISO (International Organization for Standardization) (2012). Soil quality - Effects of pollutants on earthworms – part 1: Determination of acute toxicity to Eisenia fetida/Eisenia andrei. Geneva.Google Scholar
  23. Jayanthi B, Emenike C, Auta S, Agamuthu P, Fauziah S (2017) Characterization of induced metal responses of bacteria isolates from active non-sanitary landfill in Malaysia. Int J Biodeterior & Biodegrad 119:467–475CrossRefGoogle Scholar
  24. Joly P, Bonnemoy F, Besse-Hoggan P, Perrière F, Crouzet O, Cheviron N, Mallet C (2015) Responses of limagne Bclay/organic matter-rich soil microbial communities to realistic formulated herbicide mixtures, including smetolachlor, mesotrione, and nicosulfuron. Water Air Soil Pollut 226:413CrossRefGoogle Scholar
  25. Khan S, Ali AS, Ali SA (2007) Biomass and behavioral responses of earthworm, Lumbricus terrestris to copper chloride. Iran J Toxicol 1(2):2–2Google Scholar
  26. Li P, Lin C, Cheng H, Duan X, Lei K (2015) Contamination and health risks of soil heavy metals around a lead/zinc smelter in southwestern China. Ecotoxicol & Environ Saf 113:391–399CrossRefGoogle Scholar
  27. Loureiro S, Soares AMVM, Nogueira AJA (2005) Terrestrial avoidance behaviour tests as screening tool to assess soil contamination. Environ Pollut 138:121–131CrossRefGoogle Scholar
  28. Lukkari T, Aatsinki M, Vaisanen A, Haimi J (2005) Toxicity of heavy metals assessed with three different earthworm tests. Appl Soil Ecol 30(2):133–146CrossRefGoogle Scholar
  29. Ma W (1984) Sublethal toxic effects of copper on growth, reproduction and litter breakdown activity in the earthworm Lumbricus rubellus, with observations on the influence of temperature and soil pH. Environ Pollut 33:207–219CrossRefGoogle Scholar
  30. Maboeta M, Reinecke S, Reinecke A (2004) The relationship between lysosomal biomarker and organismal responses in an acute toxicity test with Eisenia Fetida (Oligochaeta) exposed to the fungicide copper oxychloride. Environ Res 96(1):95–101CrossRefGoogle Scholar
  31. Mahbub KR, Krishnan K, Andrews S, Venter H, Naidu R, Megharaj M (2017) Bio-augmentation and nutrient amendment decrease concentration of mercury in contaminated soil. Sci Total Environ 576:303–309CrossRefGoogle Scholar
  32. Malecki MR, Neuhauser EF, Loehr RC (1982) The effect of metals on the growth and reproduction of Eisenia foetida (Oligochaeta, Lumbricidae). Pedobiologia 24:129–137Google Scholar
  33. Mani D, Kumar C (2014) Biotechnological advances in bioremediation of heavy metals contaminated ecosystems: An overview with special reference to phytoremediation. Int J Environ Sci & Technol 11:843–872CrossRefGoogle Scholar
  34. Morillo E, Villaverde J (2017) Advanced technologies for the remediation of pesticide-contaminated soils. Sci Total Environ 586:576–597CrossRefGoogle Scholar
  35. Mrozika A, Piotrowska-Seget Z (2010) Bioaugmentation as a strategy for cleaning up of soils contaminated with aromatic compounds. Microbiol Res 165:363–375CrossRefGoogle Scholar
  36. Neuhauser EF, Loehr RC, Milligan DL, Malecki MR (1985) Toxicity of metals to the earthworm Eisenia fetida. Biol & Fertil Soils 1:149–152CrossRefGoogle Scholar
  37. OECD (2016). OECD guideline for the testing of chemicals draft updated TG 222. Earthworm reproduction test (Eisenia fetida/Eisenia andrei). 19pp.Google Scholar
  38. Oladipo OG, Awotoye OO, Olayinka A, Bezuidenhout CC, Maboeta MS (2018a) Heavy metal tolerance traits of filamentous fungi isolated from gold and gemstone mining sites. Braz J Microbiol 49:29–37CrossRefGoogle Scholar
  39. Oladipo OG, Awotoye OO, Olayinka A, Ezeokoli OT, Maboeta MS, Bezuidenhout CC (2016b) Heavy metal tolerance potential of Aspergillus strains isolated from mining sites. Bioremediation. Journal 20:287–297Google Scholar
  40. Oladipo OG, Ezeokoli OT, Maboeta MS, Bezuidenhout JJ, Tiedt LR, Jordaan A, Bezuidenhout CC (2018b) Tolerance and growth kinetics of bacteria isolated from gold and gemstone mining sites in response to heavy metal concentrations. J Environ Manag 212C:357–366CrossRefGoogle Scholar
  41. Oladipo OG, Olayinka A, Awotoye OO (2016a) Maize (Zea mays) performance in organically remediated mine site soils. J Environ Manag 181:435–442CrossRefGoogle Scholar
  42. Oladipo OG, Olayinka A, Aladesanmi OT, Sanni M, Famurewa AJ, Siyanbola WO (2010) Risk mitigation strategies and policy implications for CO2 emission in organically-amended soils. Afr J Environ Sci & Technol 4(11):801–806Google Scholar
  43. Oladipo OG, Olayinka A, Awotoye OO (2014) Ecological impact of mining on soils of Southwestern Nigeria. Environ & Exp Biol 12:179–186Google Scholar
  44. Reinecke AJ, Maboeta MS, Vermeulen LA, Reinecke SA (2002a) Assessment of lead nitrate and mancozeb toxicity in earthworms using the avoidance response. Bull Environ Contam & Toxicol 68:779–786CrossRefGoogle Scholar
  45. Reinecke SA, Helling B, Reinecke AJ (2002b) Lysosomal response of earthworm (Eisenia fetida) coelomocytes to the fungicide copper oxychloride and relation to life-cycle parameters. Environ Toxicol & Chem 21:1026–1031CrossRefGoogle Scholar
  46. Reinecke SA, Reinecke AJ (1997) The influence of lead and manganese on spermatozoa of Eisenia fetida (Oligochaeta). Soil Biol Biochem 29:737–742CrossRefGoogle Scholar
  47. Ronen Z, Vasiluk L, Abeliovih A, Nejidat A (2000) Activity and survival of tribromophenol-degrading bacteria in a contaminated desert soil. Soil Biol Biochem 32:1643–1650CrossRefGoogle Scholar
  48. Spurgeon DJ, Sturzenbaum SR, Svendsen C, Hankarda PK, Morgan AJ, Weeks JM, Kille P (2004) Toxicological, cellular and gene expression responses in earthworms exposed to copper and cadmium. Comp Biochem & Physiol 138:11–21Google Scholar
  49. Syed S, Chinthala P (2015) Heavy metal detoxification by different Bacillus species isolated from solar salterns. Scientifica 2015:Article ID319760.  https://doi.org/10.1155/2015/31976 CrossRefGoogle Scholar
  50. Vermeulen L, Reinecke A, Reinecke S (2001) Evaluation of the fungicide manganese-zinc ethylene bis (dithiocarbamate) (mancozeb) for sublethal and acute toxicity to Eisenia fetida (oligochaeta) Ecotoxicol & Environ Saf 48:183–189CrossRefGoogle Scholar
  51. Vogel TM (1996) Bioaugmentation as a soil bioremediation approach. Curr Opin Biotechnol 7:311–316CrossRefGoogle Scholar
  52. Wang Y, Wu S, Chen L, Wu C, Yu R, Wang Q, Zhao X (2012) Toxicity assessment of 45 pesticides to the epigeic earthworm Eisenia fetida. Chemosphere 88(4):484–491CrossRefGoogle Scholar
  53. Wilke BM (2010) Determination of chemical and physical soil properties. In: Margesin R, Schinner F (Eds.), Manual of soil analysis: Monitoring and assessing soil bioremediation. pp. 47–95Google Scholar
  54. Zhang H, Zhang Y, Hou Z, Wang X, Wang J, Lu Z, Zhao X, Sun F, Pan H (2016) Biodegradation potential of deltamethrin by the Bacillus cereus strain Y1 in both culture and contaminated soil. Int J Biodeterior & Biodegrad 106:53–59CrossRefGoogle Scholar
  55. Zhou SP, Duan CQ, Michelle WHG, Yang FZ, Wang XH (2011) Individual and combined toxic effects of cypermethrin and chlorpyrifos on earthworm. J Environ Sci 23:676–680CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Unit for Environmental Sciences and ManagementNorth West UniversityPotchefstroomSouth Africa

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