Skip to main content
SpringerLink
Log in

Survival of Escherichia coli O157:H7 in various soil particles: importance of the attached bacterial phenotype

  • Original Paper
  • Published:
Biology and Fertility of Soils Aims and scope Submit manuscript

Abstract

The risk of enteropathogens to food and water is highly dependent on their survival in soil environments. Here, the effects of soil type, particle size, the presence of natural organic matter (NOM) or Fe/Al (hydro)oxides on pathogenic Escherichia coli O157:H7 survival in sterilized soil particles were assessed through survival, attachment, metabolic activity, and qRT-PCR analyses. The abundance of inoculated E. coli O157:H7 in Brown soil (Alfisol) particles increased 0.6–1.4 log10 CFU/g within 3 days (except for NOM-stripped clay), while that in Red soil (Ultisol) particles decreased rapidly in 8 days post-inoculation. Additionally, survival of bacteria was significantly enhanced when Fe/Al (hydro)oxides had been removed from Red soil particles. For the two soils, E. coli O157:H7 survived the longest in NOM-present clays and the bacterial adenosine 5′-triphosphate (ATP) levels were 0.7–2.0 times greater in clays than in sands and silts on day 8. Moreover, clays were more effective than silts and sands in binding cells and changing the expressions of acetate pathway-associated genes (pta and ackA). For silts and sands, E. coli O157:H7 decayed more rapidly in the presence of NOM and similar trends of bacterial ATP levels were observed between NOM-stripped and NOM-present soil particles, indicating that the primary role of NOM was not as a nutrient supply. These findings indicate that soil particles function mainly through attachment to change the metabolic pathway of E. coli O157:H7 and ultimately impact the survival of bacterial pathogens in soils.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Asadishad B, Ghoshal S, Tufenkji N (2013) Short-term inactivation rates of selected gram-positive and gram-negative bacteria attached to metal oxide mineral surfaces: role of solution and surface chemistry. Environ Sci Technol 47:5729–5737

    Article  CAS  PubMed  Google Scholar 

  • Brennan FP, Moynihan E, Griffiths BS, Hillier S, Owen J, Pendlowski H, Avery LM (2014) Clay mineral type effect on bacterial enteropathogen survival in soil. Sci Total Environ 468:302–305

    Article  PubMed  Google Scholar 

  • Brookes PC, Tate KR, Jenkinson DS (1983) The adenylate energy charge of the soil microbial biomass. Soil Biol Biochem 15:9–16

    Article  CAS  Google Scholar 

  • Busscher HJ, van der Mei HC (2012) How do bacteria know they are on a surface and regulate their response to an adhering state? PLoS Pathog 8:e1002440

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cai P, Huang Q, Walker SL (2013) Deposition and survival of Escherichia coli O157:H7 on clay minerals in a parallel plate flow system. Environ Sci Technol 47:1896–1903

    Article  CAS  PubMed  Google Scholar 

  • Carson CD, Fanning DS, Dixon JB (1982) Alfisols and Ultisols with acid-sulfate weathering features in Texas. In: Kittrick, JA, Fanning DS, Hossner, LR (Eds), Acid Sulfate Weathering, Soil Sci. Soc. Am. Madison, WI, pp. 127–146

  • Chase-Topping M, Gally D, Low C, Matthews L, Woolhouse M (2008) Super-shedding and the link between human infection and livestock carriage of Escherichia coli O157. Nat Rev Microbiol 6:904–912

    Article  CAS  PubMed  Google Scholar 

  • Chekabab SM, Paquin-Veillette J, Dozois CM, Harel J (2013) The ecological habitat and transmission of Escherichia coli O157:H7. FEMS Microbiol Lett 341:1–12

    Article  CAS  PubMed  Google Scholar 

  • Cook KL, Bolster CH (2007) Survival of Campylobacter jejuni and Escherichia coli in groundwater during prolonged starvation at low temperatures. J Appl Microbiol 103:573–583

    Article  CAS  PubMed  Google Scholar 

  • Courvoisier E, Dukan S (2009) Improvement of Escherichia coli growth by kaolinite. Appl Clay Sci 44:67–70

    Article  CAS  Google Scholar 

  • Donlan RM, Costerton JW (2002) Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 15:167–193

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duffitt AD, Reber RT, Whipple A, Chauret C (2010) Gene expression during survival of Escherichia coli O157:H7 in soil and water. Int J Microbiol 1:1–12

  • Franz E, Semenov AV, Termorshuizen AJ, De Vos OJ, Bokhorst JG, Van Bruggen AH (2008) Manure-amended soil characteristics affecting the survival of E. coli O157:H7 in 36 Dutch soils. Environ Microbiol 10:313–327

    Article  CAS  PubMed  Google Scholar 

  • Fredericks CE, Shibata S, Aizawa SI, Reimann SA, Wolfe AJ (2006) Acetyl phosphate-sensitive regulation of flagellar biogenesis and capsular biosynthesis depends on the Rcs phosphorelay. Mol Microbiol 61:734–747

    Article  CAS  PubMed  Google Scholar 

  • Fremaux B, Delignette-Muller ML, Prigent-Combaret C, Gleizal A, Vernozy-Rozand C (2007) Growth and survival of non-O157:H7 Shiga-toxin-producing Escherichia coli in cow manure. J Appl Microbiol 102:89–99

  • Gagliardi JV, Karns JS (2000) Leaching of Escherichia coli O157:H7 in diverse soils under various agricultural management practices. Appl Environ Microbiol 66:877–883

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Glasauer S, Langley S, Beveridge TJ (2001) Sorption of Fe (hydr) oxides to the surface of Shewanella putrefaciens: cell-bound fine-grained minerals are not always formed de novo. Appl Environ Microbiol 67:5544–5550

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang Q, Wu H, Cai P, Fein JB, Chen W (2015) Atomic force microscopy measurements of bacterial adhesion and biofilm formation onto clay-sized particles. Sci Rep 5:16857–16868

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang X, Morgan J, Doyle MP (2002) Fate of Escherichia coli O157:H7 in manure-amended soil. Appl Environ Microbiol 68:2605–2609

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones DL (1999) Potential health risks associated with the persistence of Escherichia coli O157 in agricultural environments. Soil Use Manage 15:76–83

    Article  Google Scholar 

  • Klein AH, Shulla A, Reimann SA, Keating DH, Wolfe AJ (2007) The intracellular concentration of acetyl phosphate in Escherichia coli is sufficient for direct phosphorylation of two-component response regulators. J Bacteriol 189:5574–5581

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kügler R, Bouloussa O, Rondelez F (2005) Evidence of a charge-density threshold for optimum efficiency of biocidal cationic surfaces. Microbiology 151:1341–1348

    Article  PubMed  Google Scholar 

  • Liu X, Zhao W, Huang Q, Cai P (2015) Relative attachment behaviors of pathogenic and nonpathogenic Escherichia coli to soil particles: influence of soil physicochemical properties. Geomicrobiol J 32:594–601

    Article  CAS  Google Scholar 

  • Mills AL (2003) Keeping in touch: microbial life on soil particle surfaces. Adv Agron 78:1–43

    Article  Google Scholar 

  • Monds RD, O’Toole GA (2009) The developmental model of microbial biofilms: ten years of a paradigm up for review. Trends Microbiol 17:73–87

    Article  CAS  PubMed  Google Scholar 

  • Moynihan EL, Richards KG, Ritz K, Tyrrel SF, Brennan FP (2013) Impact of soil type, biology and temperature on the survival of non-toxigenic Escherichia coli O157. Biol Environ Proc R Irish Acad 113:41–46

    Google Scholar 

  • Naganandhini S, Kennedy ZJ, Uyttendaele M, Balachandar D (2015) Persistence of pathogenic and non-pathogenic Escherichia coli strains in various tropical agricultural soils of India. PLoS One 10:e0130038

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nannipieri P, Ascher J, Ceccherini M, Landi L, Pietramellara G, Renella G (2003) Microbial diversity and soil functions. Eur J Soil Sci 54:655–670

    Article  Google Scholar 

  • Ongeng D, Geeraerd AH, Springael D, Ryckeboer J, Muyanja C, Mauriello G (2015) Fate of Escherichia coli O157:H7 and Salmonella enterica in the manure-amended soil-plant ecosystem of fresh vegetable crops: a review. Crit Rev Microbiol 41:273–294

    Article  PubMed  Google Scholar 

  • Pennington H (2010) Escherichia coli O157. Lancet 376:1428–1435

    Article  CAS  PubMed  Google Scholar 

  • Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:2002–2007

    Article  Google Scholar 

  • Pronk GJ, Heister K, Kögel-Knabner I (2011) Iron oxides as major available interface component in loamy arable topsoils. Soil Sci Soc Am J 75:2158–2168

    Article  CAS  Google Scholar 

  • Prüß BM, Verma K, Samanta P, Sule P, Kumar S, Wu J, Christianson D, Horne SM, Stafslien SJ, Wolfe AJ, Denton A (2010) Environmental and genetic factors that contribute to Escherichia coli K-12 biofilm formation. Arch Microbiol 192:715–728

    Article  PubMed  PubMed Central  Google Scholar 

  • Rong X, Huang Q, Chen W (2007) Microcalorimetric investigation on the metabolic activity of Bacillus thuringiensis as influenced by kaolinite, montmorillonite and goethite. Appl Clay Sci 38:97–103

    Article  CAS  Google Scholar 

  • Santamaria J, Toranzos GA (2003) Enteric pathogens and soil: a short review. Int Microbiol 6:5–9

    PubMed  Google Scholar 

  • Semenov AV, Van Bruggen AH, Van Overbeek L, Termorshuizen AJ, Semenov AM (2007) Influence of temperature fluctuations on Escherichia coli O157:H7 and Salmonella enterica serovar Typhimurium in cow manure. FEMS Microbiol Ecol 60:419–428

    Article  CAS  PubMed  Google Scholar 

  • Stotzky G (1986) Influence of soil mineral colloids on metabolic processes, growth, adhesion, and ecology of microbs and virus. In: Huang M, Schnitzer M (eds) Interactions of soil minerals with natural organics and microbes. (special publication no 17). Soil Science Society of America, Madison, WI, pp. 305–428

    Google Scholar 

  • Tao H, Bausch C, Richmond C, Blattner FR, Conway T (1999) Functional genomics: expression analysis of Escherichia coli growing on minimal and rich media. J Bacteriol 181:6425–6440

    CAS  PubMed  PubMed Central  Google Scholar 

  • Taylor AA, Chowdhury I, Gong AS, Cwiertny DM, Walker SL (2014) Deposition and disinfection of Escherichia coli O157:H7 on naturally occurring photoactive materials in a parallel plate chamber. Environ Sci Processes Impacts 16:194–202

    Article  CAS  Google Scholar 

  • Terada A, Okuyama K, Nishikawa M, Tsuneda S, Hosomi M (2012) The effect of surface charge property on Escherichia coli initial adhesion and subsequent biofilm formation. Biotechnol Bioeng 109:1745–1754

    Article  CAS  PubMed  Google Scholar 

  • Thomas C, Hill D, Mabey M (2002) Culturability, injury and morphological dynamics of thermophilic Campylobacter spp. within a laboratory-based aquatic model system. J Appl Microbiol 92:433–442

    Article  CAS  PubMed  Google Scholar 

  • van Elsas JD, Semenov AV, Costa R, Trevors JT (2011) Survival of Escherichia coli in the environment: fundamental and public health aspects. ISME J 5:173–183

    Article  PubMed  Google Scholar 

  • Van Elsas JD, Hill P, Chroňáková A, Grekova M, Topalova Y, Elhottová D, Krištůfek V (2007) Survival of genetically marked Escherichia coli O157:H7 in soil as affected by soil microbial community shifts. ISME J 1:204–214

    Article  CAS  PubMed  Google Scholar 

  • van Loosdrecht MC, Lyklema J, Norde W, Zehnder AJ (1990) Influence of interfaces on microbial activity. Microbiol Rev 54:75–87

    PubMed  PubMed Central  Google Scholar 

  • Wang H, Ibekwe AM, Ma J, Wu L, Lou J, Wu Z, Xu J, Yates SR (2014a) A glimpse of Escherichia coli O157:H7 survival in soils from eastern China. Sci Total Environ 476:49–56

    Article  PubMed  Google Scholar 

  • Wang H, Zhang T, Wei G, Wu L, Wu J, Xu J (2014b) Survival of Escherichia coli O157:H7 in soils under different land use types. Environ Sci Pollut Res 21:518–524

    Article  Google Scholar 

  • Wen G, Voroney RP, Curtin D, Schoenau JJ, Qian PY, Inanaga S (2005) Modification and application of a soil ATP determination method. Soil Biol Biochem 37:1999–2006

    Article  CAS  Google Scholar 

  • Williams LB, Metge DW, Eberl DD, Harvey RW, Turner AG, Prapaipong P, Poret-Peterson AT (2011) What makes a natural clay antibacterial? Environ Sci Technol 45:3768–3773

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wolfe AJ (2005) The acetate switch. Microbiol Mol Biol Rev 69:12–50

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu H, Chen W, Rong X, Cai P, Dai K, Huang Q (2014) Soil colloids and minerals modulate metabolic activity of Pseudomonas putida measured using microcalorimetry. Geomicrobiol J 31:590–596

    Article  CAS  Google Scholar 

  • Xiong Y (1985) Soil Colloids, First edn. Science Press, Beijing

    Google Scholar 

  • Yao Z, Wang H, Wu L, Wu J, Brookes PC, Xu J (2014) Interaction between the microbial community and invading Escherichia coli O157:H7 in soils from vegetable fields. Appl Environ Microbiol 80:70–76

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yao Z, Yang L, Wang H, Wu J, Xu J (2015) Fate of Escherichia coli O157:H7 in agricultural soils amended with different organic fertilizers. J Hazard Mater 296:30–36

    Article  CAS  PubMed  Google Scholar 

  • Zhang T, Wang H, Wu L, Lou J, Wu J, Brookes PC, Xu J (2013) Survival of Escherichia coli O157:H7 in soils from Jiangsu Province, China. PLoS One 8:e81178

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhao WQ, Walker SL, Huang QY, Cai P (2014) Adhesion of bacterial pathogens to soil colloidal particles: influences of cell type, natural organic matter, and solution chemistry. Water Res 53:35–46

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Key Research Program of China (2016YFD0800206), National Natural Science Foundation of China (41522106), and the National Basic Research Program of China (2015CB150504). In addition, we also thank Editor-in-Chief and two anonymous reviewers for their valuable suggestions that improved an earlier version of the manuscript.

Author information

Authors and Affiliations

  1. State Key Laboratory of Agricultural Microbiology, College of Resources and Environment, Huazhong Agricultural University, Wuhan, 430070, China

    Xing Liu, Chunhui Gao, Dandan Ji, Qiaoyun Huang & Peng Cai

  2. Department of Chemical and Environmental Engineering, University of California, Riverside, CA, 92521, USA

    Sharon L. Walker

Authors
  1. Xing Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chunhui Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dandan Ji
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sharon L. Walker
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Qiaoyun Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Peng Cai
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Peng Cai.

Electronic supplementary material

ᅟ

ESM 1

(DOCX 19 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, X., Gao, C., Ji, D. et al. Survival of Escherichia coli O157:H7 in various soil particles: importance of the attached bacterial phenotype. Biol Fertil Soils 53, 209–219 (2017). https://doi.org/10.1007/s00374-016-1172-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00374-016-1172-y

Keywords

Search

Navigation