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The dark side of organic vegetables: interactions of human enteropathogenic bacteria with plants

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Abstract

Many recent studies reported that several pathogenic bacteria rely on multiple hosts during their life cycle. Specifically, Gram-negative enteropathogenic bacteria, such as Salmonella or Escherichia coli O157:H7, infect both human and plant hosts. These multi-kingdom pathogenic bacteria cause food-associated outbreaks in human by active invasion of the host. In the current review, we cover the interactions between human enteropathogenic bacteria and plants. In particular, we describe the current state of knowledge on the mechanisms of adhesion, invasion, and colonization of the plant hosts by human enteropathogenic bacteria, and describe plant innate immune responses to virulence factors produced by these bacteria.

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References

  • Asai S, Shirasu K (2015) Plant cells under siege: plant immune system versus pathogen effectors. Curr Opin Plant Biol 28:1–8

    Article  CAS  PubMed  Google Scholar 

  • Barak JD, Gorski L, Naraghi-Arani P, Charkowski AO (2005) Salmonella enterica virulence genes are required for bacterial attachment to plant tissue. Appl Environ Microbiol 71:5685–5691

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barak JD, Jahn CE, Gibson DL, Charkowski AO (2007) The role of cellulose and O-antigen capsule in the colonization of plants by Salmonella enterica. Mol Plant Microbe Interact 20:1083–1091

    Article  CAS  PubMed  Google Scholar 

  • Berger CN, Shaw RK, Brown DJ, Mather H, Clare S, Dougan G, Pallen MJ, Frankel G (2009) Interaction of Salmonella enterica with basil and other salad leaves. ISME J 3:261–265

    Article  CAS  PubMed  Google Scholar 

  • Berger CN, Sodha SV, Shaw RK, Griffin PM, Pink D, Hand P, Frankel G (2010) Fresh fruit and vegetables as vehicles for the transmission of human pathogens. Environ Microbiol 12:2385–2397

    Article  PubMed  Google Scholar 

  • Bhavsar AP, Brown NF, Stoepel J, Wiermer M, Martin DD, Hsu KJ, Imami K, Ross CJ, Hayden MR, Foster LJ, Li X, Hieter P, Finlay BB (2013) The Salmonella type III effector SspH2 specifically exploits the NLR co-chaperone activity of SGT1 to subvert immunity. PLoS Pathog 9:e1003518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cevallos-Cevallos JM, Gu G, Danyluk MD, van Bruggen AH (2012) Adhesion and splash dispersal of Salmonella enterica Typhimurium on tomato leaflets: effects of rdar morphotype and trichome density. Int J Food Microbiol 160:58–64

    Article  PubMed  Google Scholar 

  • Cooley MB, Miller WG, Mandrell RE (2003) Colonization of Arabidopsis thaliana with Salmonella enterica and enterohemorrhagic Escherichia coli O157:H7 and competition by Enterobacter asburiae. Appl Environ Microbiol 69:4915–4926

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dong Y, Iniguez AL, Ahmer BM, Triplett EW (2003) Kinetics and strain specificity of rhizosphere and endophytic colonization by enteric bacteria on seedlings of Medicago sativa and Medicago truncatula. Appl Environ Microbiol 69:1783–1790

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Erickson MC, Webb CC, Diaz-Perez JC, Phatak SC, Silvoy JJ, Davey L, Payton AS, Liao J, Ma L, Doyle MP (2010) Infrequent internalization of Escherichia coli O157:H7 into field-grown leafy greens. J Food Prot 73:500–506

    Article  PubMed  Google Scholar 

  • Garcia AV, Charrier A, Schikora A, Bigeard J, Pateyron S, de Tauzia-Moreau ML, Evrard A, Mithofer A, Martin-Magniette ML, Virlogeux-Payant I, Hirt H (2014) Salmonella enterica flagellin is recognized via FLS2 and activates PAMP-triggered immunity in Arabidopsis thaliana. Mol Plant 7:657–674

    Article  CAS  PubMed  Google Scholar 

  • Golberg D, Kroupitski Y, Belausov E, Pinto R, Sela S (2011) Salmonella Typhimurium internalization is variable in leafy vegetables and fresh herbs. Int J Food Microbiol 145:250–257

    Article  PubMed  Google Scholar 

  • Gomez-Gomez L, Boller T (2000) FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell 5:1003–1011

    Article  CAS  PubMed  Google Scholar 

  • Gu G, Hu J, Cevallos-Cevallos JM, Richardson SM, Bartz JA, van Bruggen AH (2011) Internal colonization of Salmonella enterica serovar Typhimurium in tomato plants. PLoS One 6:e27340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hussain MA, Dawson CO (2013) Economic impact of food safety outbreaks on food businesses. Foods 2:585–589

    Article  PubMed  PubMed Central  Google Scholar 

  • Irvine WN, Gillespie IA, Smyth FB, Rooney PJ, McClenaghan A, Devine MJ, Tohani VK, Outbreak Control T (2009) Investigation of an outbreak of Salmonella enterica serovar Newport infection. Epidemiol Infect 137:1449–1456

    Article  CAS  PubMed  Google Scholar 

  • Jayaraman D, Valdes-Lopez O, Kaspar CW, Ane JM (2014) Response of Medicago truncatula seedlings to colonization by Salmonella enterica and Escherichia coli O157:H7. PLoS One 9:e87970

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kalily E, Hollander A, Korin B, Cymerman I, Yaron S (2016) Mechanisms of resistance to linalool in Salmonella Senftenberg and their role in survival on basil. Environ Microbiol 18:3673–3688

    Article  CAS  PubMed  Google Scholar 

  • Kisluk G, Kalily E, Yaron S (2013) Resistance to essential oils affects survival of Salmonella enterica serovars in growing and harvested basil. Environ Microbiol 15:2787–2798

    PubMed  Google Scholar 

  • Klerks MM, Franz E, van Gent-Pelzer M, Zijlstra C, van Bruggen AH (2007) Differential interaction of Salmonella enterica serovars with lettuce cultivars and plant-microbe factors influencing the colonization efficiency. ISME J 1:620–631

    Article  PubMed  Google Scholar 

  • Klerks MM, van Gent-Pelzer M, Franz E, Zijlstra C, van Bruggen AH (2007) Physiological and molecular responses of Lactuca sativa to colonization by Salmonella enterica serovar Dublin. Appl Environ Microbiol 73:4905–4914

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kroupitski Y, Golberg D, Belausov E, Pinto R, Swartzberg D, Granot D, Sela S (2009) Internalization of Salmonella enterica in leaves is induced by light and involves chemotaxis and penetration through open stomata. Appl Environ Microbiol 75:6076–6086

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kwan G, Charkowski AO, Barak JD (2013) Salmonella enterica suppresses Pectobacterium carotovorum subsp. carotovorum population and soft rot progression by acidifying the microaerophilic environment. mBio 4:e00557–12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Xu H, Zhou Y, Zhang J, Long C, Li S, Chen S, Zhou JM, Shao F (2007) The phosphothreonine lyase activity of a bacterial type III effector family. Science 315:1000–1003

    Article  CAS  PubMed  Google Scholar 

  • Lim JA, Lee DH, Heu S (2014) The interaction of human enteric pathogens with plants. Plant Pathol J 30:109–116

    Article  PubMed  PubMed Central  Google Scholar 

  • Martinez-Vaz BM, Fink RC, Diez-Gonzalez F, Sadowsky MJ (2014) Enteric pathogen–plant interactions: molecular connections leading to colonization and growth and implications for food safety. Microbes Environ 29:123–135

    Article  PubMed  PubMed Central  Google Scholar 

  • Marvasi M, Noel JT, George AS, Farias MA, Jenkins KT, Hochmuth G, Xu Y, Giovanonni JJ, Teplitski M (2014) Ethylene signalling affects susceptibility of tomatoes to Salmonella. Microb Biotechnol 7:545–555

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meng F, Altier C, Martin GB (2013) Salmonella colonization activates the plant immune system and benefits from association with plant pathogenic bacteria. Environ Microbiol 15:2418–2430

    Article  CAS  PubMed  Google Scholar 

  • Milillo SR, Badamo JM, Boor KJ, Wiedmann M (2008) Growth and persistence of Listeria monocytogenes isolates on the plant model Arabidopsis thaliana. Food Microbiol 25:698–704

    Article  CAS  PubMed  Google Scholar 

  • Mootian G, Wu WH, Matthews KR (2009) Transfer of Escherichia coli O157:H7 from soil, water, and manure contaminated with low numbers of the pathogen to lettuce plants. J Food Prot 72:2308–2312

    Article  PubMed  Google Scholar 

  • Neumann C, Fraiture M, Hernandez-Reyes C, Akum FN, Virlogeux-Payant I, Chen Y, Pateyron S, Colcombet J, Kogel KH, Hirt H, Brunner F, Schikora A (2014) The Salmonella effector protein SpvC, a phosphothreonine lyase is functional in plant cells. Front Microbiol 5:548

    PubMed  PubMed Central  Google Scholar 

  • Ohl ME, Miller SI (2001) Salmonella: a model for bacterial pathogenesis. Annu Rev Med 52:259–274

    Article  CAS  PubMed  Google Scholar 

  • Ongeng D, Vasquez GA, Muyanja C, Ryckeboer J, Geeraerd AH, Springael D (2011) 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 145:301–310

    Article  CAS  PubMed  Google Scholar 

  • Plotnikova JM, Rahme LG, Ausubel FM (2000) Pathogenesis of the human opportunistic pathogen Pseudomonas aeruginosa PA14 in Arabidopsis. Plant Physiol 124:1766–1774

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Prithiviraj B, Bais HP, Jha AK, Vivanco JM (2005) Staphylococcus aureus pathogenicity on Arabidopsis thaliana is mediated either by a direct effect of salicylic acid on the pathogen or by SA-dependent, NPR1-independent host responses. Plant J 42:417–432

    Article  CAS  PubMed  Google Scholar 

  • Rossez Y, Holmes A, Wolfson EB, Gally DL, Mahajan A, Pedersen HL, Willats WG, Toth IK, Holden NJ (2014) Flagella interact with ionic plant lipids to mediate adherence of pathogenic Escherichia coli to fresh produce plants. Environ Microbiol 16:2181–2195

    Article  CAS  PubMed  Google Scholar 

  • Roy D, Panchal S, Rosa BA, Melotto M (2013) Escherichia coli O157:H7 induces stronger plant immunity than Salmonella enterica Typhimurium SL1344. Phytopathology 103:326–332

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saldana Z, Sanchez E, Xicohtencatl-Cortes J, Puente JL, Giron JA (2011) Surface structures involved in plant stomata and leaf colonization by Shiga-toxigenic Escherichia coli O157:H7. Front Microbiol 2:119

    Article  PubMed  PubMed Central  Google Scholar 

  • Schikora A, Carreri A, Charpentier E, Hirt H (2008) The dark side of the salad: Salmonella typhimurium overcomes the innate immune response of Arabidopsis thaliana and shows an endopathogenic lifestyle. PLoS One 3:e2279

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schikora A, Virlogeux-Payant I, Bueso E, Garcia AV, Nilau T, Charrier A, Pelletier S, Menanteau P, Baccarini M, Velge P, Hirt H (2011) Conservation of Salmonella infection mechanisms in plants and animals. PLoS One 6:e24112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seo S, Matthews KR (2012) Influence of the plant defense response to Escherichia coli O157:H7 cell surface structures on survival of that enteric pathogen on plant surfaces. Appl Environ Microbiol 78:5882–5889

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shirron N, Yaron S (2011) Active suppression of early immune response in tobacco by the human pathogen Salmonella Typhimurium. PLoS One 6:e18855

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Solomon EB, Yaron S, Matthews KR (2002) Transmission of Escherichia coli O157:H7 from contaminated manure and irrigation water to lettuce plant tissue and its subsequent internalization. Appl Environ Microbiol 68:397–400

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ustun S, Muller P, Palmisano R, Hensel M, Bornke F (2012) SseF, a type III effector protein from the mammalian pathogen Salmonella enterica, requires resistance-gene-mediated signalling to activate cell death in the model plant Nicotiana benthamiana. New Phytol 194:1046–1060

    Article  CAS  PubMed  Google Scholar 

  • Wachtel MR, Charkowski AO (2002) Cross-contamination of lettuce with Escherichia coli O157:H7. J Food Prot 65:465–470

    Article  PubMed  Google Scholar 

  • Xicohtencatl-Cortes J, Sanchez Chacon E, Saldana Z, Freer E, Giron JA (2009) Interaction of Escherichia coli O157:H7 with leafy green produce. J Food Prot 72:1531–1537

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Shao F, Li Y, Cui H, Chen L, Li H, Zou Y, Long C, Lan L, Chai J, Chen S, Tang X, Zhou JM (2007) A Pseudomonas syringae effector inactivates MAPKs to suppress PAMP-induced immunity in plants. Cell Host Microbe 1:175–185

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the KRIBB Initiative Program and the Basic Research Program of National Research Foundation of Korea (NRF-2017R1A2B4012820 to J.M.P.) funded by the Ministry of Science and ICT.

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Authors and Affiliations

  1. Plant Systems Engineering Research Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB), Daejeon, South Korea

    Sung Hee Jo & Jeong Mee Park

  2. Department of Biosystems and Bioengineering, KRIBB School of Biotechnology, Korea University of Science and Technology (UST), Daejeon, South Korea

    Sung Hee Jo & Jeong Mee Park

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  1. Sung Hee Jo
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  2. Jeong Mee Park
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Correspondence to Jeong Mee Park.

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Jo, S.H., Park, J.M. The dark side of organic vegetables: interactions of human enteropathogenic bacteria with plants. Plant Biotechnol Rep 13, 105–110 (2019). https://doi.org/10.1007/s11816-019-00536-1

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