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Aflatoxins in the soil ecosystem: an overview of its occurrence, fate, effects and future perspectives

Abstract

Aflatoxins are secondary metabolites produced by specific strains of fungi, especially Aspergillus spp. These natural toxins are mainly found in soil, decaying vegetation and food storage systems and are particularly abundant during drought stress. Aflatoxin contamination is one of the most important threats to food safety and human health due to its toxic, mutagenic and carcinogenic properties. Therefore, most research focuses on post-harvest contamination of aflatoxins in feed and food commodities but very limited information is available about aflatoxin contamination and its toxicological consequences in the soil ecosystem. Current regulations provide minimal options for the disposal of aflatoxin-contaminated crops, amongst which is the incorporation of residues into the soil for natural degradation. This form of mycotoxin loading into the soil could potentially change its physicochemical characteristics and biotic parameters. Recent studies suggest that as climate conditions change, the occurrence and geographical distribution of aflatoxins might increase, posing significant health risks to the soil ecosystem, food crop production and human health. This review will focus on studies that look at the environmental and toxicological consequences of aflatoxin contamination with the aim of clarifying the risk that aflatoxin contamination poses to soil ecosystems. Many aspects of aflatoxin occurrence, degradation and the effects of its transformation products in the soil environment are still unknown and remain an important area of research for soil health and productivity. A climatic approach, in terms of changes in soil moisture and air temperature, is important for future risk assessments of aflatoxin contamination.

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References

  • Accinelli C, Abbas HK, Zablotowicz RM, Wilkinson JR (2008) Aspergillus flavus aflatoxin occurrence and expression of aflatoxin biosynthesis genes in soil. Can J Microbiol 54:371–379. https://doi.org/10.1139/W08-018

    CAS  Article  PubMed  Google Scholar 

  • Achaglinkame MA, Opoku N, Amagloh FK (2017) Aflatoxin contamination in cereals and legumes to reconsider usage as complimentary food ingredients for Ghanaian infants: a review. J Nutr Intermed Metab 10:1–7

    Google Scholar 

  • Angle JS (1986) Aflatoxin decomposition in various soils. J Environ Sci Health B 21:277–288

    CAS  PubMed  Google Scholar 

  • Angle JS, Wagner GH (1981) Aflatoxin B1 effects on soil microorganisms. Soil Biol Biochem 13:381–384

    CAS  Google Scholar 

  • Azab SG, Sadek MM, Crailsheim K (2001) Protein metabolism in larvae of the cotton leaf-worm Spodoptera littoralis (Lepidoptera: Noctuidae) and its response to three mycotoxins. Environ Entomol 30:817–823

    CAS  Google Scholar 

  • Battilani P, Toscano P, Van der Fels-Klerx HJ, Moretti A, Camardo Leggieri M, Brera C, Rortais A, Goumperis T, Robinson T (2016) Aflatoxin B1 contamination in maize in Europe increases due to climate change. Sci Rep 6:24328. https://doi.org/10.1038/srep24328

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Bennet JW, Klich M (2003) Mycotoxins. Clin Microbiol Rev 16:497–516

    Google Scholar 

  • Bradford KJ, Dahal P, van Asbrouck J, Kunusoth K, Bello P, Thompson J, Wu F (2018) The dry chain: reducing post-harvest losses and improving food safety in humid climates. Trends Food Sci Technol 71:84–93

    CAS  Google Scholar 

  • Cotty PJ (2006) Biocompetitive exclusion of toxigenic fungi. In: Barug D, Bhatnagar D, van Egmond HP, van der Kamp JW, van Osenbruggen WA, Visconti A (eds) The mycotoxin factbook. Wageningen Academic Publishers, Wageningen, pp 179–197

    Google Scholar 

  • Cotty PJ, Jaime-Garcia R (2007) Influences of climate on aflatoxin producing fungi and aflatoxin contamination. Int J Food Microbiol 119:109–115

    CAS  PubMed  Google Scholar 

  • Cserháti M, Kriszt B, Krifaton C, Szoboszlay S, Háhn J, Tóth S, Nagy I, Kukolya J (2013) Mycotoxin-degradation profile of Rhodococcus strains. Int J Food Microbiol 166:176–185

    PubMed  Google Scholar 

  • Desheng Q, Fan L, Yanhu Y, Niya Z (2005) Adsorption of aflatoxin B1 on montmorillonite. Poult Sci 84:959–961

    CAS  PubMed  Google Scholar 

  • Doyle MP, Applebaum RS, Brackett RE, Marth EH (1982) Physical, chemical and biological degradation of mycotoxins in foods and agricultural commodities. J Food Prot 45:964–971

    CAS  PubMed  Google Scholar 

  • EAC- East Africa Community (2018) Disposal and alternative uses of aflatoxin-contaminated food. EAC Policy Brief No. 8 on aflatoxin Prevention and Control. Available at: https://www.eac.int/documents/category/aflatoxin-prevention-and-control

  • Ehrlich KC (2014) Non-aflatoxigenic Aspergillus flavus to prevent aflatoxin contamination in crops: advantages and limitations. Front Microbiol 5:1–9

    Google Scholar 

  • Elmholt S (2008) Mycotoxins in the soil environment. In: Karlovsky P (ed) Secondary metabolites in soil ecology. Soil Biology. Springer, Heidelberg, pp 167–203

    Google Scholar 

  • Elshafie A, Al-bahry SN, Alkindi AY, Ba-omar T, Mahmound I (2007) Mycoflora and aflatoxins in soil, eggshells, and failed eggs of Chelonia mydas at Ras Al-Jinz, Oman. Chelonian Conserv Biol 6:267–270

  • Escrivá L, Font G, Manyes L, Berrada H (2017) Studies on the presence of mycotoxins in biological samples: an overview. Toxins (Basel) 9:1–33

    Google Scholar 

  • Feng W, Xue KS, Tang L, Williams PL, Wang J (2017) Aflatoxin B1-induced developmental and DNA damage in Caenorhabditis elegans. Toxins 9:1–12

    CAS  Google Scholar 

  • Fouché TC, Claassens S, Maboeta MS (2017) Ecotoxicological assessment of chemical fumigants utilising an earthworm (Eisenia andrei) bioassay and soil microbial communities. Water Air Soil Pollut 228:154. https://doi.org/10.1007/s11270-017-3339-z

    CAS  Article  Google Scholar 

  • Fountain JC, Scully BT, Ni X, Kemerait RC, Lee DR, Chen Z, Guo B (2014) Environmental influences on maize -Aspergillus flavus interactions and aflatoxin production. Front Microbiol 5:1–7

    Google Scholar 

  • Ghiglione J, Martin-Laurent F, Pesce S (2016) Microbial ecotoxicology: an emerging discipline facing contemporary environmental threats. Environ Sci Pollut Res 23:3981–3983

    Google Scholar 

  • Goldberg BS, Angle JS (1985) Aflatoxin movement in soil. J Environ Qual 14:224–228

    CAS  Google Scholar 

  • Grant PG, Phillips TD (1998) Isothermal adsorption of Aflatoxin B1 on HSCAS clay. J Agric Food Chem 46:599–605

    CAS  PubMed  Google Scholar 

  • Guchi E (2015) Aflatoxin contamination in groundnut (Arachis hypogaea L.) caused by Aspergillus species in Ethiopia. J Appl Environ Microbiol 3:11–19

    CAS  Google Scholar 

  • Hackbart HCS, Machado AR, Christ-Ribeiro A, Prietto L, Badiale-Furlong E (2014) Reduction of aflatoxins by Rhizopus oryzae and Trichoderma reesei. Mycotoxin Res 30:141–149

    CAS  PubMed  Google Scholar 

  • Hariprasad P, Vipin AV, Karuna S, Raksha RK, Venkateswaran G (2015) Natural aflatoxin uptake by sugarcane (Saccharum officinaurum L.) and its persistence in jaggery. Environ Sci Pollut Res 22:6246–6253

    CAS  Google Scholar 

  • Iheanacho H (2015) Cytotoxic effects of aflatoxin B1 standard in relation to aflatoxin extracts from South African compound feeds on human lymphocytes. Biomed Data Min 3:1–5

    Google Scholar 

  • IPCC, 2019: Climate change and land: an IPCC special report on climate change, desertification, land degradation, sustainable land management, food security, and greenhouse gas fluxes in terrestrial ecosystems [PR Shukla, J Skea, E Calvo Buendia, V Masson-Delmotte, HO Pörtner, DC Roberts, P Zhai, R Slade, S Connors, R van Diemen, M Ferrat, E Haughey, S Luz, S Neogi, M Pathak, J Petzold, J Portugal Pereira, P Vyas, E Huntley, K Kissick, M Belkacemi, J Malley (eds.)] In press

  • Jaime-Garcia R, Cotty PJ (2010) Crop rotation and soil temperature influence the community structure of Aspergillus flavus in soil. Soil Biol Biochem 42:1842–1847

    CAS  Google Scholar 

  • Jaynes WF, Zarman RE, Hudnall WH (2007) Aflatoxin B1 adsorption by clays from water and cornmeal. Appl Clay Sci 36:197–205

    CAS  Google Scholar 

  • Karlovsky P (2008) Secondary metabolites in soil ecology. In: Karlovsky P (eds) Secondary metabolites in soil ecology. Soil Biology, Berlin, Heidelberg, pp 1–19

  • Kolpin DW, Schenzel J, Meyer MT, Phillips PJ, Hubbard LE, Scott TM, Bucheli TD (2014) Mycotoxins: diffuse and point source contributions of natural contaminants of emerging concern to streams. Sci Total Environ 470–471:669–676

    PubMed  Google Scholar 

  • Krifaton C, Kriszt B, Szoboszlay S, Cserháti M, Szucs Á, Kukolya J (2011) Analysis of aflatoxin B1-degrading microbes by use of a combined toxicity-profiling method. Mutat Res Genet Toxicol Environ Mutagen 726:1–7

    CAS  Google Scholar 

  • Kumpiene J, Giagnoni L, Marschner B, Denys S, Mench M, Adriaensen K, Vangronsveld J, Puschenreiter M, Renella G (2017) Assessment of methods for determining bioavailability of trace elements in soils: a review. Pedosphere 27:389–406

    Google Scholar 

  • Lawson B, MacDonald S, Howard T, Macgregor SK, Cunningham AA (2006) Exposure of garden birds to aflatoxins in Britain. Sci Total Environ 361:124–131

    CAS  PubMed  Google Scholar 

  • Lillehoj EB, Ciegler A (1969) Biological activity of aflatoxin B2a. Appl Microbiol 17:516–519

    CAS  PubMed  PubMed Central  Google Scholar 

  • Luo X, Wang R, Wang L, Li Y, Wang Y, Chen Z (2014) Detoxification of aflatoxin in cornflour by ozone. J Sci Food Agric 94:2253–2258

    CAS  PubMed  Google Scholar 

  • Madden UA, Stahr HM (1993) Preliminary determination of mycotoxin binding to soil when leaching through soil with water. Int Biodeterior Biodegradation 31:265–275

    CAS  Google Scholar 

  • Medina Á, Rodriguez A, Magan N (2015) Climate change and mycotoxigenic fungi: impacts on mycotoxin production. Curr Opin Food Sci 5:99–104

    Google Scholar 

  • Medina Á, González-Jartín JM, Sainz MJ (2017) Impact of global warming on mycotoxins. Curr Opin Food Sci 18:76–81

    Google Scholar 

  • Mertz D, Edward T, Lee D, Zuber M (1981) Absorption of aflatoxin by lettuce seedlings grown in soil adulterated with aflatoxin B1. J Agric Food Chem 29:1168–1170

    CAS  PubMed  Google Scholar 

  • Mishra HN, Das C (2003) A review on biological control and metabolism of aflatoxin. Crit Rev Food Sci Nutr 43:245–264

    CAS  PubMed  Google Scholar 

  • Moretti A, Pascale M, Logrieco AF (2019) Mycotoxin risks under a climate change scenario in Europe. Trends Food Sci Technol 84:38–40

    CAS  Google Scholar 

  • Pankaj SK, Shi H, Keener KM (2018) A review of novel physical and chemical decontamination technologies for aflatoxin in food. Trends Food Sci Technol 71:73–78

    CAS  Google Scholar 

  • Parelho C, dos Santos RA, Bernardo F, Carmo Barreto M, Cunha L, Poeta P, Garcia P (2018) Biological endpoints in earthworms (Amynthas gracilis) as tools for the ecotoxicity assessment of soils from livestock production systems. Ecol Indic 95:984–990

    CAS  Google Scholar 

  • Pižl V, Nováková A (2003) Interactions between microfungi and Eisenia andrei (Oligochaeta) during cattle manure vermicomposting. Pedobiologia (Jena) 47:895–899

    Google Scholar 

  • Rajesh K, Pal SV, Anuradha S (2014) A study of biological control of Aspergillus flavus using Pseudomonas fluorescens and Bacillus subtilis. Int Res J Sci Eng 2(6):213–218

    Google Scholar 

  • Raksha Rao K, Vipin AV, Hariprasad P, Anu Appaiah KA, Venkateswaran G (2017) Biological detoxification of Aflatoxin B1 by Bacillus licheniformis CFR1. Food Control 71:234–241

    CAS  Google Scholar 

  • Ray PK, Singh KP, Raisuddin PAK (1991) Immunological responses to aflatoxins and other chemical carcinogens. J Toxicol 10:63–85. https://doi.org/10.3109/15569549109058576

    CAS  Article  Google Scholar 

  • Sanders TH, Blankenship PD, Cole RJ, Hill RA (1984) Effect of soil temperature and drought on peanut pod and stem temperatures relative to Aspergillus flavus invasion and aflatoxin contamination. Mycopathologia 86:51–54

    CAS  PubMed  Google Scholar 

  • Spencer Smith JS, Williams WP, Windham GL (2019) Aflatoxin in maize: a review of the early literature from “moldy-corn toxicosis” to the genetics of aflatoxin accumulation resistance. Mycotoxin Res 35:111–128

    CAS  PubMed  Google Scholar 

  • Starr JM, Selim MI (2008) Supercritical fluid extraction of aflatoxin B1 from soil. J Chromatogr A 1209:37–43

    CAS  PubMed  Google Scholar 

  • Starr JM, Rushing BR, Selim MI (2017) Solvent-dependent transformation of aflatoxin B1 in soil. Mycotoxin Res 33:197–205

    CAS  PubMed  Google Scholar 

  • Szabó-Fodor J, Bors I, Nagy G, Kovács M (2017) Toxicological effects of aflatoxin B1 on the earthworm Eisenia fetida as determined in a contact paper test. Mycotoxin Res 33:109–112

    PubMed  Google Scholar 

  • Theumer MG, Henneb Y, Khoury L, Snini SP, Tadrist S, Canlet C, Puel O, Oswald IP, Audebert M (2018) Genotoxicity of aflatoxins and their precursors in human cells. Toxicol Lett 287:100–107

    CAS  PubMed  Google Scholar 

  • van Gestel CAM (2012) Soil ecotoxicology: state of the art and future directions. Zookeys. 176:275–296

    Google Scholar 

  • Verheecke C, Liboz T, Mathieu F (2016) Microbial degradation of aflatoxin B1: current status and future advances. Int J Food Microbiol 237:1–9

    CAS  PubMed  Google Scholar 

  • WHO - World Health Organisation (2018) Aflatoxins In: Food safety digest. Department of Food Safety and Zoonoses. Ref no: WHO/NHM/FOS/RAM/18.1 Available from: https://www.who.int/foodsafety/foodsafetydigest/en/

  • Wolfarth F, Schrader S, Oldenburg E, Brunotte J (2016) Mycotoxin contamination and its regulation by the earthworm species Lumbricus terrestris in presence of other soil fauna in an agroecosystem. Plant Soil 402:331–342

    CAS  Google Scholar 

  • Zain ME (2011) Impact of mycotoxins on humans and animals. J Saudi Chem Soc 15:129–144

    CAS  Google Scholar 

  • Zhang S, Lu J, Wang S, Mao D, Miao S, Ji S (2016) Multi-mycotoxins analysis in Pheretima using ultra-high-performance liquid chromatography-tandem mass spectrometry based on a modified QuEChERS method. J Chromatogr B 1035:31–41

    CAS  Google Scholar 

  • Zhao X, Wang D, Fields PG, Li H (2018) Effect of aflatoxin B1 on development, survival and fecundity of Ahasverus advena (Waltl). J Stored Prod Res 77:225–230

    Google Scholar 

  • Zirbes L, Mescher M, Vrancken V, Wathelet JP, Verheggen FJ, Thonart P, Haubruge E (2011) Earthworms use odor cues to locate and feed on microorganisms in soil. PLoS One 6:1–7

    Google Scholar 

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Correspondence to Tanya Fouché.

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Fouché, T., Claassens, S. & Maboeta, M. Aflatoxins in the soil ecosystem: an overview of its occurrence, fate, effects and future perspectives. Mycotoxin Res 36, 303–309 (2020). https://doi.org/10.1007/s12550-020-00393-w

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  • DOI: https://doi.org/10.1007/s12550-020-00393-w

Keywords

  • Aflatoxins
  • Ecotoxicology
  • Soil
  • Climate change
  • Food safety