Interaction between bacterial enteric pathogens and aquatic macrophytes. Can Salmonella be internalized in the plants used in phytoremediation processes?

References

• Alufasi R, Gere J, Chakauya E, Lebea P, Parawira W, Chingwaru W. 2017. Mechanisms of pathogen removal by macrophytes in constructed wetlands. Environ Technol Rev. 6(1):135–144. doi:10.1080/21622515.2017.1325940.
   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(9):2385–2397. doi:10.1111/j.1462-2920.2010.02297.x.
   PubMed Web of Science ®Google Scholar
• Bernardini A, Salvatori E, Guerrini V, Fusaro L, Canepari S, Manes F. 2016. Effects of high Zn and Pb concentrations on Phragmites australis (Cav.) Trin. Ex. Steudel: photosynthetic performance and metal accumulation capacity under controlled conditions. Int J Phytoremediation. 18(1):16–24. doi:10.1080/15226514.2015.1058327.
   PubMed Web of Science ®Google Scholar
• Beuchat LR, Scouten AJ, Allen RI, Hussey RS. 2003. Potential of a plant-parasitic nematode to facilitate internal contamination of tomato plants by Salmonella. J Food Prot. 66(8):1459–1461. doi:10.4315/0362-028x-66.8.1459.
   PubMed Web of Science ®Google Scholar
• Brandl M, Cox CE, Teplitski M. 2013. Salmonella interactions with plants and their associated microbiota. Phytopathology. 103(4):316–325. doi:10.1094/PHYTO-11-12-0295-RVW.
   PubMed Web of Science ®Google Scholar
• Brandl MT, Mandrell RE. 2002. Fitness of Salmonella enterica serovar Thompson in the cilantro phyllosphere. Appl Environ Microbiol. 68(7):3614–3621. doi:10.1128/aem.68.7.3614-3621.2002.
   PubMed Web of Science ®Google Scholar
• Burnett SL, Chen J, Beuchat LR. 2000. Attachment of Escherichia coli O157:H7 to the surfaces and internal structures of apples as detected by confocal scanning laser microscopy. Appl Environ Microbiol. 66(11):4679–4687. doi:10.1128/aem.66.11.4679-4687.2000.
   PubMed Web of Science ®Google Scholar
• CDC (Center for diseases control and prevention). 2017. Standard Operating Procedure for PulseNet PFGE of Escherichia coli O157:H7, Escherichia coli non-O157 (STEC), Salmonella serotypes, Shigella sonnei and Shigella flexneri. www.cdc.gov/pulsenet/pathogens/protocols.html.
   Google Scholar
• Chiudioni F, Trabace T, Di Gennaro S, Palma A, Manes F, Mancini L. 2017. Phytoremediation applications in natural condition and in mesocosm: the uptake of cadmium by Lemna minuta Kunth, a non-native species in Italian watercourses. Int J Phytoremediation. 19(4):371–376. doi:10.1080/15226514.2016.1225290.
   PubMed Web of Science ®Google Scholar
• Córdoba-Aguilar E, Coutiño-Rodríguez R, Giles-Ríos H, Hernández-Cruz P, Mosqueda-Aguilar A, Ríos-Cortés P, Montero H. 2018. Lectins from eichornia crassipens and lemna minor may be involved in Vibrio cholerae El Tor adhesion. Epidemiol Mikrobiol Imunol. 67(1):24–30.
   PubMed Web of Science ®Google Scholar
• Cordoba Aguilar E, Herrera Rivero M, Rubi A, Arroyo-Helguera O, Coutino Rodriguez R. 2014. Isolation of Vibrio cholera El Tor Inaba From Lemna minor and Eichhornia crassipens roots in Veracruz, Mexico. Jundishapur J Microbiol. 7(3):e6855. doi:10.5812/jjm.6855.
   PubMed Web of Science ®Google Scholar
• Dong Y, Iniguez AL, Ahmer BMM, 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(3):1783–1790. doi:10.1128/aem.69.3.1783-1790.2003.
   PubMed Web of Science ®Google Scholar
• EFSA and ECDC (European Food Safety Authority and European Centre for Disease Prevention and Control). 2019. The European Union One Health 2018 Zoonoses report. EFSA J. 17(12):e05926.
   PubMed Web of Science ®Google Scholar
• Erickson M. 2012. Internalization of fresh produce by foodborne pathogens. Annu Rev Food Sci Technol. 3:283–310. doi:10.1146/annurev-food-022811-101211.
   PubMed Web of Science ®Google Scholar
• Fisher IS, Jourdan-Da Silva N, Hächler H, Weill FX, Schmid H, Danan C, Kérouanton A, Lane CR, Dionisi AM, Luzzi I. 2009. Human infections due to Salmonella Napoli: a multicountry, emerging enigma recognized by the Enter-net international surveillance network. Foodborne Pathog Dis. 6(5):613–619. doi:10.1089/fpd.2008.0206.
   PubMed Web of Science ®Google Scholar
• Fletcher J, Leach J, Eversole K, Tauxe R. 2013. Human pathogens on plants: designing a multidisciplinary strategy for research. Phytopathology. 103(4):306–315. doi:10.1094/PHYTO-09-12-0236-IA.test.
   PubMed Web of Science ®Google Scholar
• Gomes C, Da Silva P, Moreira RG, Castell-Perez E, Ellis EA, Pendleton M. 2009. Understanding E. coli internalization in lettuce leaves for optimization of irradiation treatment. Int J Food Microbiol. 135(3):238–247. doi:10.1016/j.ijfoodmicro.2009.08.026.
   PubMed Web of Science ®Google Scholar
• Graziani C, Losasso C, Luzzi I, Ricci A, Scavia G, Pasquali P. 2017. Salmonella. In: Dodd CER, Aldsworth T, Stein RA, Cliver DO, Riemann HP, editors. Foodborne diseases. 3rd ed. London: Elserivier- Academic Press. p. 133–169.
   Google Scholar
• Graziani C, Luzzi I, Owczarek S, Dionisi AM, Busani L. 2015. Salmonella enterica serovar Napoli infection in Italy from 2000 to 2013: spatial and spatio-temporal analysis of cases distribution and the effect of human and animal density on the risk of infection. PLoS One. 10(11):e0142419. doi:10.1371/journal.pone.0142419.
   PubMed Web of Science ®Google Scholar
• Graziani C, Mughini-Gras L, Owczarek S, Dionisi A, Luzzi I, Busani L. 2013. Distribution of Salmonella enterica isolates from human cases in Italy, 1980 to 2011. Euro Surveill. 18:205–219.
   Google Scholar
• Grimont PAD, Weill FX. 2007. Antigenic formulae of the Salmonella serovars 2007. 9th ed. WHO Collaborating Centre for Reference and Research on Salmonella. Paris, France: Institute Pasteur France.
   Google Scholar
• Gu G, Hu J, Cevallos-Cevallos JM, Richardson SM, Bartz JA, van Bruggen A. 2011. Internal colonization of Salmonella enterica serovar Typhimurium in tomato plants. PLoS ONE. 6(11):e27340. doi:10.1371/journal.pone.0027340.
   PubMed Web of Science ®Google Scholar
• Han Y, Linton RH, Nielsen SS, Nelson PE. 2000. Inactivation of Escherichia coli O157:H7 on surface-uninjured and -injured green pepper (Capsicum ann- uum L.) by chlorine dioxide gas as demonstrated by confocal laser scanning microscopy. Food Microbiol. 17(6):643–655. doi:10.1006/fmic.2000.0357.
   Web of Science ®Google Scholar
• Hirneisen KA, Sharma M, Kniel KE. 2012. Human enteric pathogen internalization by root uptake into food crops. Foodborne Path Dis. 9(5):396–405.
   PubMed Web of Science ®Google Scholar
• Hoagland DR, Arnon DI. 1950. The water-culture method for growing plants without soil. California Agricultural Experiment Station, Circular n. 347, p. 1–32.
   Google Scholar
• Kipasika HJ, Buza J, Smith WA, Njau KN. 2016. Removal capacity of faecal pathogens from wastewater by four wetland vegetation: Typha latifolia, Cyperus papyrus, Cyperus alternifolius and Phragmites australis. Afr J Microbiol Res. 10(19):654–661. doi:10.5897/AJMR2016.7931.
   Google Scholar
• Kleinheinz G, Coenan A, Zehms T, Preedit J, Leewis M, Becker D, McDermott C. 2009. Effect of aquatic macrophytes on the survival of Escherichia coli in a laboratory microcosm. Lake Reservoir Manage. 25 (2):149–154. doi:10.1080/07438140902821413.
   Web of Science ®Google Scholar
• Klerks MM, Franz E, van Gent-Pelzer MPE, Zijlstra C, van Bruggen A. 2007. Differential interaction of Salmonella enterica serovars with lettuce cultivars and plant-microbe factors influencing the colonization efficiency. Isme J. 1(7):620–631. doi:10.1038/ismej.2007.82.
   PubMed Web of Science ®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(19):6076–6086. doi:10.1128/AEM.01084-09.
   PubMed Web of Science ®Google Scholar
• Lim JA, Dong Hwan L, Sunggi H. 2014. The interaction of human enteric pathogens with plants. Plant Pathol J. 30(2):109–116. doi:10.5423/PPJ.RW.04.2014.0036.
   PubMed Web of Science ®Google Scholar
• Liu H, Whitehouse CA, Li B. 2018. Presence and persistence of Salmonella in water: the impact on microbial quality of water and food safety. Front Public Health. 6:159. doi:10.3389/fpubh.2018.00159.
   PubMed Web of Science ®Google Scholar
• Luzzi I, García-Fernández A, Dionisi AM, Lucarelli C, Gattuso A, Gianfranceschi M, Maugliani A, Caprioli A, Morabito S, Scavia G, 2017. Enter-Net Italia e Registro italiano della sindrome emolitico uremica: sorveglianza delle infezioni da Salmonella, Campylobacter, Escherichia coli produttore di Shiga-tossina e Listeria monocytogenes (2010–2015). Roma: Istituto Superiore di Sanità, Rapporti ISTISAN 17/34.
   Google Scholar
• Majowicz SE, Musto J, Scallan E, Angulo FJ, Kirk M, O'Brien SJ, Jones TF, Fazil A, Hoekstra RM, International Collaboration on Enteric Disease ‘Burden of Illness' Studies 2010. The global burden of nontyphoidal Salmonella gastroenteritis. Clin Infect Dis. 50(6):882–889. doi:10.1086/650733.
   PubMed Web of Science ®Google Scholar
• Mancini L, Marcheggiani S, D'Angelo AM, Puccinelli C, Chiudioni F, Rossi F, Delibato E, De Medici D, Dionisi AM, Owczarek S, et al. 2014. First isolation of Salmonella enterica serovar Napoli from wild birds in Italy. Annali Dell'Istituto Superiore di Sanità. 50(1):96–98.
   PubMed Web of Science ®Google Scholar
• Martinez-Urtaza J, Liebana E, Garcia-Migura L, Perez-Pi ∼ Neiro P, Saco M. 2004. Characterization of Salmonella enterica serovar Typhimurium from marine environments in coastal waters of Galicia (Spain). Appl Environ Microbiol. 70(7):4030–4034. doi:10.1128/AEM.70.7.4030-4034.2004.
   PubMed Web of Science ®Google Scholar
• Mastrorilli E, Petrin S, Orsini M, Longo A, Cozza D, Luzzi I, Ricci A, Barco L, Losasso C. 2020. Comparative genomic analysis reveals high intra-serovar plasticity within Salmonella Napoli isolated in 2005–2017. BMC Genomics. 21(1):202. doi:10.1186/s12864-020-6588-y.
   PubMed Web of Science ®Google Scholar
• Odinga CA, Kumar A, Mthembu MS, Bux F, Swalaha FM. 2019. Rhizofiltration system consisting of Phragmites australis and Kyllinga nemoralis: evaluation of efficient removal of metals and pathogenic microorganisms. DWT. 169:120–132. doi:10.5004/dwt.2019.24428.
   Web of Science ®Google Scholar
• Oggioni C, Fontana G, Pavan A, Gramegna M, Ferretti V, Piatti A, Edefonti V, Tunnesi S, Sala G, Pontello M. 2010. Investigation of potential risk factors for Salmonella enterica subsp enterica serotype Napoli: a nested case–control study in Lombardia region [in Italian]. Ann Ig. 22(4):327–335.
   PubMedGoogle Scholar
• Oliveira RS, Dod JC, Castro P. 2001. The mycorrhizal status of Phragmites australis in several polluted soils and sediments of an industrialised region of northern Portugal. Mycorrhiza. 10(5):241–247. doi:10.1007/s005720000087.
   Web of Science ®Google Scholar
• Parker WF, Mee BJ. 1982. Survival of Salmonella Adelaide and fecal coliforms in coarse sands of the Swan Costal Plain, Western Australia. Appl Environ Microbiol. 43(5):981–986. doi:10.1128/AEM.43.5.981-986.1982.
   PubMed Web of Science ®Google Scholar
• Sabbatucci M, Dionisi AM, Pezzotti P, Lucarelli C, Barco L, Mancin M, Luzzi I. 2018. Molecular and epidemiologic analysis of reemergent Salmonella enterica Serovar Napoli, Italy, 2011–2015. Emerging Infect Dis. 24(3):562–565. doi:10.3201/eid2403.171178.
   PubMed Web of Science ®Google Scholar
• Schikora A, Virlogeux-Payant I, Bueso E, Garcia AV, Nilau T, Charrier A, Pelletier S, Menanteau P, Baccarini M, Velge P, et al. 2011. Conservation of Salmonella infection mechanisms in plants and animals. PLoS ONE. 6(9):e24112. doi:10.1371/journal.pone.0024112.
   PubMed Web of Science ®Google Scholar
• Schikora A, Garcia AV, Hirt H. 2012. Plants as alternative hosts for Salmonella. Trends Plant Sci. 17(5):245–249. doi:10.1016/j.tplants.2012.03.007.
   PubMed Web of Science ®Google Scholar
• Setti I, Rodriguez-Castro A, Pata MP, Cadarso-Suarez C, Yacoubi B, Bensmael L, Moukrim A, Martinez-Urtaza J. 2009. Characteristics and dynamics of Salmonella contamination along the Coast of Agadir. AEM. 75(24):7700–7709. doi:10.1128/AEM.01852-09.
   Google Scholar
• Shingare RP, Nanekar SV, Thawale PR, Karthik R, Juwarkar AA. 2017. Comparative study on removal of enteric pathogens from domestic wastewater using Typha latifolia and Cyperus rotundus along with different substrates. Int J Phytoremediation. 19(10):899–908. doi:10.1080/15226514.2017.1303809.
   PubMed Web of Science ®Google Scholar
• Srivastava J, Swinder JSK, Naraian R. 2014. Environmental perspectives of Phragmites australis. Appl Water Sci. 4(3):193–202. doi:10.1007/s13201-013-0142-x.
   Google Scholar
• Wiedemann A, Virlogeux-Payant I, Chaussé AM, Schikora A, Velge P. 2014. Interactions of Salmonella with animals and plants. Front Microbiol. 5:791. doi:10.3389/fmicb.2014.00791.
   PubMed Web of Science ®Google Scholar
• Winfield MD, Groisman EA. 2003. Role of non-host environments in the lifestyles of Salmonella and Escherichia coli. AEM. 69(7):3687–3694. doi:10.1128/AEM.69.7.3687-3694.2003.
   Google Scholar
• Zottola T, Montagnaro S, Magnapera C, Sasso S, De Martino L, Bragagnolo A, D'Amici L, Condoleo R, Pisanelli G, Iovane G, et al. 2013. Prevalence and antimicrobial susceptibility of Salmonella in European wild boar (Sus scrofa); Latium Region - Italy. Comp Immunol Microbiol Infect Dis. 36(2):161–168. doi:10.1016/j.cimid.2012.11.004.
   PubMed Web of Science ®Google Scholar