CoChat
Sign Up
Cited by 32Escherichia coli research studiesListeria monocytogenes in Food SafetyFecal contamination and water quality

Persistence of Pathogenic and Non-Pathogenic Escherichia coli Strains in Various Tropical Agricultural Soils of India

Open access
Naganandhini, S., Kennedy, Z. John, Uyttendaele, M., Balachandar, D.·2015·PLOS ONE
DOI 10.1371/journal.pone.0130038PMC PMC4477969
Open this paper in CoChat — free accountOpen PDF

Abstract

The persistence of Shiga-like toxin producing E. coli (STEC) strains in the agricultural soil creates serious threat to human health through fresh vegetables growing on them. However, the survival of STEC strains in Indian tropical soils is not yet understood thoroughly. Additionally how the survival of STEC strain in soil diverges with non-pathogenic and genetically modified E. coli strains is also not yet assessed. Hence in the present study, the survival pattern of STEC strain (O157-TNAU) was compared with non-pathogenic (MTCC433) and genetically modified (DH5α) strains on different tropical agricultural soils and on a vegetable growing medium, cocopeat under controlled condition. The survival pattern clearly discriminated DH5α from MTCC433 and O157-TNAU, which had shorter life (40 days) than those compared (60 days). Similarly, among the soils assessed, the red laterite and tropical latosol supported longer survival of O157-TNAU and MTCC433 as compared to wetland and black cotton soils. In cocopeat, O157 recorded significantly longer survival than other two strains. The survival data were successfully analyzed using Double-Weibull model and the modeling parameters were correlated with soil physico-chemical and biological properties using principal component analysis (PCA). The PCA of all the three strains revealed that pH, microbial biomass carbon, dehydrogenase activity and available N and P contents of the soil decided the survival of E. coli strains in those soils and cocopeat. The present research work suggests that the survival of O157 differs in tropical Indian soils due to varied physico-chemical and biological properties and the survival is much shorter than those reported in temperate soils. As the survival pattern of non-pathogenic strain, MTCC433 is similar to O157-TNAU in tropical soils, the former can be used as safe model organism for open field studies.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1371/journal.pone.0130038

Cites

1 of 1 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Fecal bacteria including antimicrobial-resistant E. coli that have been excreted into moist soil or pooled sewage may persist and grow when temperatures are maintained between 30 and 37 degrees Celsius, which is common in many sub-tropical countries.

    “Fecal bacteria including antimicrobial-resistant E. coli - that have been excreted into moist soil or pooled sewage may persist and grow when temperatures are maintained between 3037 ° C 54-56 , which is common in many sub-tropical countries.”

    From Urban informal settlements as hotspots of antimicrobial resistance and the need to curb environmental transmission. (2020) · cites this paper as [55]

    The Methods describe moist soils inoculated with E. coli and incubated at 30°C; the Results report that the strains persisted for a time, but their cell counts declined rather than grew. The study did not test persistence in pooled sewage or across 30–37°C. Its strains were given an ampicillin-resistance marker in the laboratory, so it does not establish the claim for excreted antimicrobial-resistant E. coli. (LLM, conf=0.88)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 67

  1. [1]Nataro JP, Kaper JB. Diarrheagenic Escherichia coli. Clin Microbiol Rev. 1998; 11(1): 142– 201. 9457432 PMC121379
  2. [2]Paton JC, Paton AW. Pathogenesis and diagnosis of Shiga toxin-producing Escherichia coli infections. Clin Microbiol Rev. 1998; 11(3): 450– 79. 9665978 PMC88891
  3. [3]Riley LW, Remis RS, Helgerson SD, McGee HB, Wells JG, Davis BR, et al Hemorrhagic colitis associated with a rare Escherichia coli serotype. New Engl J Med. 1983; 308(12): 681– 5. 6338386
  4. [4]O’Brien AD, Kaper JB. Shiga toxin-producing Escherichia coli: yesterday, today and tomorrow In: Kaper JB, O’Brien AD, editors. Escherichia coli O157:H7 and Other Shiga Toxin-Producing E coli Strains. Washington DC: ASM Press; 1998 p. 1– 11.
  5. [5]Hepburn N, MacRae M, Ogden I. Survival of Escherichia coli O157 in abattoir waste products. Lett Appl Microbiol. 2002; 35(3): 233– 6. 12180947
  6. [6]Guan TY, Holley RA. Pathogen survival in swine manure environments and transmission of human enteric illness—a review. J Environ Qual. 2003; 32(2): 383– 92. 12708660
  7. [7]Hilborn ED, Mermin JH, Mshar PA, Hadler JL, Voetsch A, Wojtkunski C, et al A multistate outbreak of Escherichia coli O157: H7 infections associated with consumption of mesclun lettuce. Arch Internal Med. 1999; 159(15): 1758– 64. 10448779
  8. [8]Michino H, Araki K, Minami S, Takaya S, Sakai N, Miyazaki M, et al Massive outbreak of Escherichia coli O157: H7 infection in schoolchildren in Sakai City, Japan, associated with consumption of white radish sprouts. Am J Epidemiol. 1999; 150(8): 787– 96. 10522649
  9. [9]Bolton D. The survival characteristics of a non toxigenic strain of Escherichia coli O157: H7. J Appl Microbiol. 1999; 86(3): 407– 11. 10196745
  10. [10]Maule A. Environmental aspects of E. coli O157. Int Food Hygine. 1999; 9: 21– 3.
  11. [11]Chart H. VTEC enteropathogenicity. J Appl Microbiol. 2000; 88(S1): 12S– 23S. 10880175
  12. [12]Hahesy T, Scanlon M, Carton O, Quinn P, Lenehan J. Cattle manure and the spread of bovine tuberculosis. Irish Vet J. 1992; 45(4–6): 122– 3.
  13. [14]Cooley M, Carychao D, Crawford-Miksza L, Jay MT, Myers C, Rose C, et al Incidence and tracking of Escherichia coli O157: H7 in a major produce production region in California. PloS one. 2007; 2(11): e1159 10.1371/journal.pone.0001159 18174909 PMC2174234 · DOI
  14. [15]Mukherjee A, Cho S, Scheftel J, Jawahir S, Smith K, Diez-Gonzalez F. Soil survival of Escherichia coli O157: H7 acquired by a child from garden soil recently fertilized with cattle manure. J Appl Microbiol. 2006; 101(2): 429– 36. 16882151
  15. [16]Williams A, Avery L, Killham K, Jones D. Survival of Escherichia coli O157: H7 in the rhizosphere of maize grown in waste-amended soil. J Appl Microbiol. 2007; 102(2): 319– 26. 17241336
  16. [17]Franz E, Semenov AV, Termorshuizen AJ, De Vos O, Bokhorst JG, Van Bruggen AH. Manure-amended soil characteristics affecting the survival of E. coli O157: H7 in 36 Dutch soils. Environ Microbiol. 2008; 10(2): 313– 27. 10.1111/j.1462-2920.2007.01453.x 18199123 · DOI
  17. [18]Ongeng D, Muyanja C, Geeraerd A, Springael D, Ryckeboer J. Survival of Escherichia coli O157: H7 and Salmonella enterica serovar Typhimurium in manure and manure-amended soil under tropical climatic conditions in Sub-Saharan Africa. J Appl Microbiol. 2011; 110(4): 1007– 22. 10.1111/j.1365-2672.2011.04956.x 21276146 · DOI
  18. [19]Oliveira M, Viñas I, Usall J, Anguera M, Abadias M. Presence and survival of Escherichia coli O157: H7 on lettuce leaves and in soil treated with contaminated compost and irrigation water. Int J Food Microbiol. 2012; 156(2): 133– 40. 10.1016/j.ijfoodmicro.2012.03.014 22483400 · DOI
  19. [20]Zhang T, Wang H, Wu L, Lou J, Wu J, Brookes PC, et al Survival of Escherichia coli O157: H7 in soils from Jiangsu Province, China. PloS one. 2013; 8(12): e81178 10.1371/journal.pone.0081178 24312534 PMC3846838 · DOI
  20. [21]Ma J, Mark Ibekwe A, Crowley DE, Yang C-H. Persistence of Escherichia coli O157 and non-O157 strains in agricultural soils. Sci Total Environ. 2014; 490: 822– 9. 10.1016/j.scitotenv.2014.05.069 24907617 · DOI
  21. [22]Ngole V, Mpuchane S, Totolo O. Survival of faecal coliforms in four different types of sludge-amended soils in Botswana. Eur J Soil Biol. 2006; 42(4): 208– 18.
  22. [23]Lang N, Smith S. Influence of soil type, moisture content and biosolids application on the fate of Escherichia coli in agricultural soil under controlled laboratory conditions. J Appl Microbiol. 2007; 103(6): 2122– 31. 17973917
  23. [24]Ibekwe AM, Papiernik SK, Grieve CM, Yang C-H. Quantification of persistence of Escherichia coli O157:H7 in contrasting soils. Int J Microbiol. 2011; 2011 10.1155/2011/421379 PMC2943103 20871863 · DOI
  24. [25]Cools D, Merckx R, Vlassak K, Verhaegen J. Survival of E. coli and Enterococcus spp. derived from pig slurry in soils of different texture. Appl Soil Ecol. 2001; 17(1): 53– 62.
  25. [26]Vidovic S, Block HC, Korber DR. Effect of soil composition, temperature, indigenous microflora, and environmental conditions on the survival of Escherichia coli O157: H7. Can J Microbiol. 2007; 53(7): 822– 9. 17898837
  26. [27]Mubiru D, Coyne MS, Grove JH. Mortality of Escherichia coli O157: H7 in two soils with different physical and chemical properties. J Environ Qual. 2000; 29(6): 1821– 5.
  27. [28]Entry JA, Bjorneberg DL, Verwey S. Influence of tillage and daily manure application on the survival of bacterial pathogens indicators in soil and on radish. Appl Environ Soil Sci. 2010; 2010 10.1155/2010/973925 · DOI
  28. [29]Wang H, Zhang T, Wei G, Wu L, Wu J, Xu J. Survival of Escherichia coli O157: H7 in soils under different land use types. Environ Sci Pollut Res. 2014; 21(1): 518– 24. 10.1007/s11356-013-1938-9 23812736 · DOI
  29. [30]Van Elsas JD, Hill P, Chroňáková A, Grekova M, Topalova Y, Elhottová D, et al Survival of genetically marked Escherichia coli O157: H7 in soil as affected by soil microbial community shifts. ISME J. 2007; 1(3): 204– 14. 18043631
  30. [31]Yao Z, Wang H, Wu L, Wu J, Brookes PC, Xu J. Interaction between the microbial community and Invading Escherichia coli O157: H7 in soils from vegetable fields. Appl Environ Microbiol. 2014; 80(1): 70– 6. 10.1128/AEM.03046-13 24123745 PMC3911026 · DOI
  31. [32]van Elsas JD, Chiurazzi M, Mallon CA, Elhottovā D, Krištůfek V, Salles JF. Microbial diversity determines the invasion of soil by a bacterial pathogen. PNAS. 2012; 109(4): 1159– 64. 10.1073/pnas.1109326109 22232669 PMC3268289 · DOI
  32. [33]Wang G, Zhao T, Doyle MP. Fate of enterohemorrhagic Escherichia coli O157: H7 in bovine feces. Appl Environ Microbiol. 1996; 62(7): 2567– 70. 8779595 PMC168038
  33. [34]Recorbet G, Steinberg C, Faurie G. Survival in soil of genetically engineered Escherichia coli as related to inoculum density, predation and competition. FEMS Microbiol Lett. 1992; 101(4): 251– 60. 10.1111/j.1574-6968.1992.tb05782.x · DOI
  34. [35]Miller WG, Lindow SE. An improved GFP cloning cassette designed for prokaryotic transcriptional fusions. Gene. 1997; 191(2): 149– 53. 9218713
  35. [36]Cebula TA, Payne WL, Feng P. Simultaneous identification of strains of Escherichia coli serotype O157: H7 and their Shiga-like toxin type by mismatch amplification mutation assay-multiplex PCR. J Clin Microbiol. 1995; 33(1): 248– 50. 7535315 PMC227922
  36. [37]Versalovic J, Schneider M, De Bruijn FJ, Lupski JR. Genomic fingerprinting of bacteria using repetitive sequence-based polymerase chain reaction. Methods Mole Cell Biol. 1994; 5(1): 25– 40.
  37. [38]Urzì C, Brusetti L, Salamone P, Sorlini C, Stackebrandt E, Daffonchio D. Biodiversity of Geodermatophilaceae isolated from altered stones and monuments in the Mediterranean basin. Environ Microbiol. 2001; 3(7): 471– 9. 11553237
  38. [39]Walkley A, Black IA. An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method. Soil Sci. 1934; 37(1): 29– 38.
  39. [40]Waring SA, Bremner JM. Ammonium production in soil under waterlogged conditions as an index of nitrogen availability. Nature. 1964; 201(4922): 951– 2.
  40. [42]Hanway J, Heidel H. Soil analysis methods as used in Iowa state college soil testing laboratory. Iowa agric. 1952; 57: 1– 31.
  41. [44]Klein DA, Loh TC, Goulding RL. A rapid procedure to evaluate the dehydrogenase activity of soils low in organic matter. Soil Biol Biochem. 1971; 3(4): 385– 7. 10.1016/0038-0717(71)90049-6 · DOI
  42. [45]Sambrook J, Fritsch EF, Maniatis T. Molecular cloning: Cold spring harbor laboratory press New York; 1989.
  43. [47]Geeraerd A, Valdramidis V, Van Impe J. GInaFiT, a freeware tool to assess non-log-linear microbial survivor curves. Int J Food Microbiol. 2005; 102(1): 95– 105. 15893399
  44. [48]Coroller L, Leguérinel I, Mettler E, Savy N, Mafart P. General model, based on two mixed Weibull distributions of bacterial resistance, for describing various shapes of inactivation curves. Appl Environ Microbiol. 2006; 72(10): 6493– 502. 17021197 PMC1610288
  45. [49]Wold S, Esbensen K, Geladi P. Principal component analysis. Chemom Intell Lab Syst. 1987; 2(1): 37– 52.
  46. [50]Jiang X, Morgan J, Doyle MP. Fate of Escherichia coli O157: H7 in manure-amended soil. Appl Environ Microbiol. 2002; 68(5): 2605– 9. 11976144 PMC127522
  47. [51]Islam M, Doyle MP, Phatak SC, Millner P, Jiang X. Survival of Escherichia coli O157: H7 in soil and on carrots and onions grown in fields treated with contaminated manure composts or irrigation water. Food Microbiol. 2005; 22(1): 63– 70.
  48. [52]Posada-Izquierdo GD, Pérez-Rodríguez F, López-Gálvez F, Allende A, Selma MV, Gil MI, et al Modelling growth of Escherichia coli O157:H7 in fresh-cut lettuce submitted to commercial process conditions: Chlorine washing and modified atmosphere packaging. Food Microbiol. 2013; 33(2): 131– 8. 10.1016/j.fm.2012.08.010 23200644 · DOI
  49. [53]Ongeng D, Vasquez G, Muyanja C, Ryckeboer J, Geeraerd A, Springael D. Transfer and internalisation of Escherichia coli O157: H7 and Salmonella enterica serovar Typhimurium in cabbage cultivated on contaminated manure-amended soil under tropical field conditions in Sub-Saharan Africa. Int J Food Microbiol. 2011; 145(1): 301– 10. 10.1016/j.ijfoodmicro.2011.01.018 21269720 · DOI
  50. [54]Moyne A-L, Harris LJ, Marco ML. Assessments of total and viable Escherichia coli O157: H7 on field and laboratory grown lettuce. PloS one. 2013; 8(7): e70643 10.1371/journal.pone.0070643 23936235 PMC3728298 · DOI
  51. [55]Ma J, Ibekwe AM, Yi X, Wang H, Yamazaki A, Crowley DE, et al Persistence of Escherichia coli O157: H7 and its mutants in soils. PloS one. 2011; 6(8): e23191 10.1371/journal.pone.0023191 21826238 PMC3149627 · DOI
  52. [56]Franz E, van Diepeningen AD, de Vos OJ, van Bruggen AH. Effects of cattle feeding regimen and soil management type on the fate of Escherichia coli O157: H7 and Salmonella enterica serovar Typhimurium in manure, manure-amended soil, and lettuce. Appl Environ Microbiol. 2005; 71(10): 6165– 74. 16204535 PMC1265955
  53. [57]Fremaux B, Prigent-Combaret C, Delignette-Muller M, Mallen B, Dothal M, Gleizal A, et al Persistence of Shiga toxin-producing Escherichia coli O26 in various manure-amended soil types. J Appl Microbiol. 2008; 104(1): 296– 304. 17850320
  54. [58]Semenov AV, Franz E, Van Overbeek L, Termorshuizen AJ, Van Bruggen AH. Estimating the stability of Escherichia coli O157: H7 survival in manure-amended soils with different management histories. Environ Microbiol. 2008; 10(6): 1450– 9. 10.1111/j.1462-2920.2007.01558.x 18218027 · DOI
  55. [59]Olive DM, Bean P. Principles and applications of methods for DNA-based typing of microbial organisms. J Clin Microbiol. 1999; 37(6): 1661– 9. 10325304 PMC84917
  56. [60]Ibekwe AM, Ma J. Effects of fumigants on microbial diversity and persistence of E. coli O15: H7 in contrasting soil microcosms. Sci Total Environ. 2011; 409(19): 3740– 8. 10.1016/j.scitotenv.2011.06.033 21757224 · DOI
  57. [61]Kudva IT, Blanch K, Hovde CJ. Analysis of Escherichia coli O157: H7 survival in ovine or bovine manure and manure slurry. Appl Environ Microbiol. 1998; 64(9): 3166– 74. 9726855 PMC106705
  58. [62]Hutchison M, Walters L, Moore A, Crookes K, Avery S. Effect of length of time before incorporation on survival of pathogenic bacteria present in livestock wastes applied to agricultural soil. Appl Environ Microbiol. 2004; 70(9): 5111– 8. 15345389 PMC520911
  59. [63]Islam M, Doyle MP, Phatak SC, Millner P, Jiang X. Persistence of enterohemorrhagic Escherichia coli O157: H7 in soil and on leaf lettuce and parsley grown in fields treated with contaminated manure composts or irrigation water. J Food Protect. 2004; 67(7): 1365– 70. 15270487
  60. [64]Nicholson FA, Groves SJ, Chambers BJ. Pathogen survival during livestock manure storage and following land application. Bioresour Technol. 2005; 96(2): 135– 43. 15381209
  61. [65]Chinnadurai C, Gopalaswamy G, Balachandar D. Impact of long-term organic and inorganic nutrient managements on the biological properties and eubacterial community diversity of the Indian semi-arid Alfisol. Arch Agron Soil Sci. 2014; 60(4): 531– 48. 10.1080/03650340.2013.803072 · DOI
  62. [66]Cai P, Huang Q, Walker SL. Deposition and survival of Escherichia coli O157: H7 on clay minerals in a parallel plate flow system. Environ Sci Technol. 2013; 47(4): 1896– 903. 10.1021/es304686a 23346967 · DOI
  63. [67]Ogden ID, Fenlon DR, Vinten AJ, Lewis D. The fate of Escherichia coli O157 in soil and its potential to contaminate drinking water. Int J Food Microbiol. 2001; 66(1): 111– 7. 11407540
  64. [68]Ma J, Ibekwe AM, Crowley DE, Yang C-H. Persistence of Escherichia coli O157: H7 in major leafy green producing soils. Environ Sci Technol. 2012; 46(21): 12154– 61. 10.1021/es302738z 23030401 · DOI
  65. [70]Fremaux B, Prigent-Combaret C, Vernozy-Rozand C. Long-term survival of Shiga toxin-producing Escherichia coli in cattle effluents and environment: An updated review. Vet Microbiol. 2008; 132(1): 1– 18. 18586416
  66. [71]Woodcock D, Crowther P, Doherty J, Jefferson S, DeCruz E, Noyer-Weidner M, et al Quantitative evaluation of Escherichia coli host strains for tolerance to cytosine methylation in plasmid and phage recombinants. Nucleic Acids Res. 1989; 17(9): 3469– 78. 2657660 PMC317789
  67. [72]Castellani A, Chalmers AJ. Manual of tropical medicine, 3rd edition New York, US: Williams, Wood and Co.; 1919.

Cited by

Sorted by citations

Authors
Naganandhini, S., Kennedy, Z. J., Uyttendaele, M., & Balachandar, D.
Affiliations
  • Tamil Nadu Agricultural University (IN)
  • Ghent University (BE)
Corresponding author
Balachandar, D.
ORCID
Venue
PLOS ONE
Publisher
Public Library of Science (PLoS)
Published
2015-06-23
Volume
10
Issue
6
Pages
e0130038
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0130038
PMC
PMC4477969
OpenAlex
W840264840
Cited by
32
References
1
Citations by year
2024: 6 · 2023: 2 · 2022: 2 · 2021: 5 · 2020: 4 · 2019: 6 · 2018: 4 · 2016: 3
FWCI
1.82
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Ghent University Academic Bibliography (Ghent University) (submittedVersion, other-oa)
  • RePEc: Research Papers in Economics (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
  • Figshare (submittedVersion, cc-by)
Funders
  • European Commission (244994)
  • Institute of Genetics
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Escherichia coli research studies
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Listeria monocytogenes in Food Safety
  • Physical Sciences › Environmental Science › Water Science and Technology › Fecal contamination and water quality
Keywords
Escherichia coli O157, tropical agricultural soils, soil physicochemical properties, soil microbial biomass carbon, dehydrogenase activity, cocopeat, laterite, Oxisol, Vertisols, wetland soils, India
MeSH terms
Agriculture, Culture Media, Escherichia coli, India, Soil Microbiology, Tropical Climate, Principal Component Analysis, Green Fluorescent Proteins

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review