Human pathogenic bacteria on fresh produce and their control using bacteriophage treatment: an E. coli example from the Sunshine Coast region
Meg Allom A , Harrchun Panchalingam A , M. Katouli A and D. İpek Kurtböke A *A School of Science, Technology and Engineering, University of the Sunshine Coast, Maroochydore BC, Qld 4558, Australia.
Meg Allom is a UniSC recent graduate with first class Honours. She also holds a BSc in the Science Program of the UniSC. Over the past 2 years she conducted research with Dr İpek Kurtböke related to the application of various actinophages. She has worked with foodborne pathogens and microbial contaminants in her studies and has a keen interest in food safety. |
Harrchun Panchalingam has recently completed his PhD under Dr Kurtböke’s supervision. He is an international student from Sri Lanka and holds BSc from Monash University Malaysia and MSc from University of Peradeniya, Sri Lanka. His PhD project involved assessment of Trichoderma and actinomycetes spp. to control Pyrrhoderma noxium infections of heritage fig trees in Brisbane. Currently he is working as research assistant at (UniSC). His research interests are biological control of plant diseases, development of biofertilisers and bioremediation of hydrocarbons. |
Associate Professor Mohammad Katouli obtained his PhD in 1980 from University of Ulster in UK. He then joined the Research and Development Department of DP Pharmaceuticals. In 1985, he took the position of the Head of Microbiology Department at the Pasteur Institute in Tehran. Between 1988 and 1998, he worked as a senior research fellow at the Microbiology and Tumour Biology Centre of the Karolinska Institute, Stockholm, Sweden. In 1998, he took a teaching and research position at University of the Sunshine Coast. His current interest is gut microbiota and the role of E. coli in pathogenesis of IBD. |
D. İpek Kurtböke is currently a senior lecturer at the University of the Sunshine Coast (UniSC) in Australia and one of the members of the Genecology Research Centre of the UniSC, conducting research in applied, industrial and environmental microbiology. She is an internationally reputed actinomycetologist and she has been in the field of biodiscovery since 1982 conducting research into discovery of novel and potent therapeutic compounds produced by actinomycetes in Turkey, Italy, the UK, and Australia with leading pharmaceutical companies. She has been an Executive Board member of the World Federation of Culture Collections (WFCC) since 2000, currently serving her second term as the President of the Federation. She is also one of the members of the International Committee on Taxonomy of Viruses (ICTV)’s, Bacterial Viruses Subcommittee. She has editorial duties in different journals including Marine Drugs, Diversity and Frontiers Marine Science/Marine Biotechnology. |
Microbiology Australia 43(4) 194-198 https://doi.org/10.1071/MA22059
Submitted: 6 October 2022 Accepted: 22 November 2022 Published: 13 December 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing on behalf of the ASM. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)
Abstract
Consumers are placing increasing importance on an environmentally friendly way of food production and are turning to organically produced fruit and vegetables. Organic farming rejects the use of synthetic pesticides or fertilisers, growth promoters, antibiotics, or transgenic organisms. However, the use of manures that replace synthetic fertilisers is associated with a risk of contamination of produce with pathogenic microorganisms. There have been a considerable number of foodborne outbreaks associated with fresh produce, resulting in hospitalisations and deaths worldwide. Accordingly, bacteriophages have gained much attention as a safe, effective, and organic method for removal of pathogenic microorganisms from fresh produce. Bacteriophage treatments for control of pathogenic E. coli and other pathogens on fresh produce have several advantages over currently used treatments, including their host specificity, safety, low impact on sensory qualities of fresh produce, and their ease of isolation over other antimicrobial agents.
Keywords: antibiotic resistant pathogenic bacteria, bacteriophages, bacteriophage biocontrol, E. coli, E. coli phage, food borne pathogens, food security, fresh produce, phage inactivation.
References
[1] Department of Agriculture, Water and the Environment (2020) Vegetable industry. Farm surveys and analysis. https://www.agriculture.gov.au/abares/researchtopics/surveys/vegetables (accessed 20 February 2021)[2] Slavin, JL and Lloyd, B (2012) Health benefits of fruits and vegetables. Adv Nutr 3, 506–516.
| Health benefits of fruits and vegetables.Crossref | GoogleScholarGoogle Scholar |
[3] Randhawa MA et al. (2015) Chapter 18 - Green Leafy Vegetables: A Health Promoting Source. In Handbook of Fertility (Watson RR, ed.). pp. 205–220. Academic Press.
[4] Ishii, S and Sadowsky, MJ (2008) Escherichia coli in the environment: implications for water quality and human health. Microbes Environ 23, 101–108.
| Escherichia coli in the environment: implications for water quality and human health.Crossref | GoogleScholarGoogle Scholar |
[5] Jang, J et al.. (2017) Environmental Escherichia coli: ecology and public health implications—a review. J Appl Microbiol 123, 570–581.
| Environmental Escherichia coli: ecology and public health implications—a review.Crossref | GoogleScholarGoogle Scholar |
[6] García, A et al.. (2010) Zoonotic enterohemorrhagic Escherichia coli: a One Health perspective. ILAR J 51, 221–232.
| Zoonotic enterohemorrhagic Escherichia coli: a One Health perspective.Crossref | GoogleScholarGoogle Scholar |
[7] Maffei, DF et al.. (2016) Microbiology of organic and conventionally grown fresh produce. Braz J Microbiol 47, 99–105.
| Microbiology of organic and conventionally grown fresh produce.Crossref | GoogleScholarGoogle Scholar |
[8] Murray, K et al.. (2017) Challenges in the microbiological food safety of fresh produce: limitations of post-harvest washing and the need for alternative interventions. Food Qual Saf 1, 289–301.
| Challenges in the microbiological food safety of fresh produce: limitations of post-harvest washing and the need for alternative interventions.Crossref | GoogleScholarGoogle Scholar |
[9] Machado-Moreira, B et al.. (2019) Microbial contamination of fresh produce: what, where, and how? Compr Rev Food Sci Food Saf 18, 1727–1750.
| Microbial contamination of fresh produce: what, where, and how?Crossref | GoogleScholarGoogle Scholar |
[10] Lu, Q et al.. (2012) Land application of biosolids in the USA: a review. Appl Environ Soil Sci 2012, 201462.
| Land application of biosolids in the USA: a review.Crossref | GoogleScholarGoogle Scholar |
[11] Alegbeleye, OO et al.. (2018) Sources and contamination routes of microbial pathogens to fresh produce during field cultivation: a review. Food Microbiol 73, 177–208.
| Sources and contamination routes of microbial pathogens to fresh produce during field cultivation: a review.Crossref | GoogleScholarGoogle Scholar |
[12] Monaghan, JM and Hutchison, ML (2012) Distribution and decline of human pathogenic bacteria in soil after application in irrigation water and the potential for soil-splash-mediated dispersal onto fresh produce. J Appl Microbiol 112, 1007–1019.
| Distribution and decline of human pathogenic bacteria in soil after application in irrigation water and the potential for soil-splash-mediated dispersal onto fresh produce.Crossref | GoogleScholarGoogle Scholar |
[13] Deering, AJ et al.. (2015) Movement of Salmonella serovar Typhimurium and E. coli O157:H7 to ripe tomato fruit following various routes of contamination. Microorganisms 3, 809–825.
| Movement of Salmonella serovar Typhimurium and E. coli O157:H7 to ripe tomato fruit following various routes of contamination.Crossref | GoogleScholarGoogle Scholar |
[14] Hutchison, ML et al.. (2017) Fate of Escherichia coli O145 present naturally in bovine slurry applied to vegetables before harvest, after washing and simulated wholesale and retail distribution. J Appl Microbiol 123, 1597–1606.
| Fate of Escherichia coli O145 present naturally in bovine slurry applied to vegetables before harvest, after washing and simulated wholesale and retail distribution.Crossref | GoogleScholarGoogle Scholar |
[15] Sharma, M and Reynnells, R (2016) Importance of soil amendments: survival of bacterial pathogens in manure and compost used as organic fertilizers. Microbiol Spectr 4, 4.4.36.
| Importance of soil amendments: survival of bacterial pathogens in manure and compost used as organic fertilizers.Crossref | GoogleScholarGoogle Scholar |
[16] Lin, H et al.. (2019) Fate of tetracycline and sulfonamide resistance genes in a grassland soil amended with different organic fertilizers. Ecotoxicol Environ Saf 170, 39–46.
| Fate of tetracycline and sulfonamide resistance genes in a grassland soil amended with different organic fertilizers.Crossref | GoogleScholarGoogle Scholar |
[17] White HE, Orlova EV (2019) Bacteriophages: their structural organisation and function. In Bacteriophages - Perspectives and Future (Savva R, ed.). InTech.
[18] Carvalho CM et al. (2012) Phages as therapeutic tools to control major foodborne pathogens: Campylobacter and Salmonella. In Bacteriophages (Kurtboke I, ed.). InTech.
[19] Połaska, M and Sokołowska, B (2019) Bacteriophages—a new hope or a huge problem in the food industry. AIMS Microbiol 5, 324–346.
| Bacteriophages—a new hope or a huge problem in the food industry.Crossref | GoogleScholarGoogle Scholar |
[20] Kurtböke, Dİ et al.. (2016) Isolation and characterization of Enterobacteriaceae species infesting post-harvest strawberries and their biological control using bacteriophages. Appl Microbiol Biotechnol 100, 8593–8606.
| Isolation and characterization of Enterobacteriaceae species infesting post-harvest strawberries and their biological control using bacteriophages.Crossref | GoogleScholarGoogle Scholar |
[21] El-Tarabily, KA (2008) Promotion of tomato (Lycopersicon esculentum Mill.) plant growth by rhizosphere competent 1-aminocyclopropane-1-carboxylic acid deaminase-producing streptomycete actinomycetes. Plant Soil 308, 161–174.
| Promotion of tomato (Lycopersicon esculentum Mill.) plant growth by rhizosphere competent 1-aminocyclopropane-1-carboxylic acid deaminase-producing streptomycete actinomycetes.Crossref | GoogleScholarGoogle Scholar |
[22] Jonns, JA et al.. (2017) Streptophage-mediated control of off-flavour taint producing streptomycetes isolated from barramundi ponds. Synth Syst Biotechnol 2, 105–112.
| Streptophage-mediated control of off-flavour taint producing streptomycetes isolated from barramundi ponds.Crossref | GoogleScholarGoogle Scholar |
[23] O’Flynn, G et al.. (2004) Evaluation of a cocktail of three bacteriophages for biocontrol of Escherichia coli O157:H7. Appl Environ Microbiol 70, 3417–3424.
| Evaluation of a cocktail of three bacteriophages for biocontrol of Escherichia coli O157:H7.Crossref | GoogleScholarGoogle Scholar |
[24] Wang, L et al.. (2017) Use of bacteriophages to control Escherichia coli O157:H7 in domestic ruminants, meat products, and fruits and vegetables. Foodborne Pathog Dis 14, 483–493.
| Use of bacteriophages to control Escherichia coli O157:H7 in domestic ruminants, meat products, and fruits and vegetables.Crossref | GoogleScholarGoogle Scholar |
[25] Duc, HM et al.. (2020) Isolation, characterization and application of a polyvalent phage capable of controlling Salmonella and Escherichia coli O157:H7 in different food matrices. Food Res Int 131, 108977.
| Isolation, characterization and application of a polyvalent phage capable of controlling Salmonella and Escherichia coli O157:H7 in different food matrices.Crossref | GoogleScholarGoogle Scholar |
[26] Manohar, P et al.. (2019) Therapeutic characterization and efficacy of bacteriophage cocktails infecting Escherichia coli, Klebsiella pneumoniae, and Enterobacter species. Front Microbiol 10, 574.
| Therapeutic characterization and efficacy of bacteriophage cocktails infecting Escherichia coli, Klebsiella pneumoniae, and Enterobacter species.Crossref | GoogleScholarGoogle Scholar |
[27] Yazdi, M et al.. (2020) Isolation, characterization and genomic analysis of a novel bacteriophage VB_EcoS-Golestan infecting multidrug-resistant Escherichia coli isolated from urinary tract infection. Sci Rep 10, 7690.
| Isolation, characterization and genomic analysis of a novel bacteriophage VB_EcoS-Golestan infecting multidrug-resistant Escherichia coli isolated from urinary tract infection.Crossref | GoogleScholarGoogle Scholar |
[28] Jończyk, E et al.. (2011) The influence of external factors on bacteriophages—review. Folia Microbiol (Praha) 56, 191–200.
| The influence of external factors on bacteriophages—review.Crossref | GoogleScholarGoogle Scholar |
[29] Sillankorva, SM et al.. (2012) Bacteriophages and their role in food safety. Int J Microbiol 2012, 863945.
| Bacteriophages and their role in food safety.Crossref | GoogleScholarGoogle Scholar |
[30] Guenther, S et al.. (2009) Virulent bacteriophage for efficient biocontrol of Listeria monocytogenes in ready-to-eat foods. Appl Environ Microbiol 75, 93–100.
| Virulent bacteriophage for efficient biocontrol of Listeria monocytogenes in ready-to-eat foods.Crossref | GoogleScholarGoogle Scholar |
[31] Sharma, M et al.. (2009) Effectiveness of bacteriophages in reducing Escherichia coli O157:H7 on fresh-cut cantaloupes and lettuce. J Food Prot 72, 1481–1485.
| Effectiveness of bacteriophages in reducing Escherichia coli O157:H7 on fresh-cut cantaloupes and lettuce.Crossref | GoogleScholarGoogle Scholar |
[32] Kazi, M and Annapure, US (2016) Bacteriophage biocontrol of foodborne pathogens. J Food Sci Technol 53, 1355–1362.
| Bacteriophage biocontrol of foodborne pathogens.Crossref | GoogleScholarGoogle Scholar |
[33] Boyacioglu, O et al.. (2013) Biocontrol of Escherichia coli O157: H7 on fresh-cut leafy greens. Bacteriophage 3, e24620.
| Biocontrol of Escherichia coli O157: H7 on fresh-cut leafy greens.Crossref | GoogleScholarGoogle Scholar |
[34] Snyder, AB et al.. (2016) Developing and optimizing bacteriophage treatment to control enterohemorrhagic Escherichia coli on fresh produce. Int J Food Microbiol 236, 90–97.
| Developing and optimizing bacteriophage treatment to control enterohemorrhagic Escherichia coli on fresh produce.Crossref | GoogleScholarGoogle Scholar |
[35] Tanji, Y et al.. (2004) Toward rational control of Escherichia coli O157:H7 by a phage cocktail. Appl Microbiol Biotechnol 64, 270–274.
| Toward rational control of Escherichia coli O157:H7 by a phage cocktail.Crossref | GoogleScholarGoogle Scholar |
[36] Loc-Carrillo, C and Abedon, ST (2011) Pros and cons of phage therapy. Bacteriophage 1, 111–114.
| Pros and cons of phage therapy.Crossref | GoogleScholarGoogle Scholar |
[37] Kim, B-o et al.. (2019) Phage-derived antibacterials: harnessing the simplicity, plasticity, and diversity of phages. Viruses 11, 268.
| Phage-derived antibacterials: harnessing the simplicity, plasticity, and diversity of phages.Crossref | GoogleScholarGoogle Scholar |
