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Reuterin Demonstrates Potent Antimicrobial Activity Against a Broad Panel of Human and Poultry Meat Campylobacter Spp. Isolates

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Reuterin Demonstrates Potent Antimicrobial Activity Against a Broad Panel of Human and Poultry Meat Campylobacter Spp. Isolates microorganisms Article Reuterin Demonstrates Potent Antimicrobial Activity Against a Broad Panel of Human and Poultry Meat Campylobacter spp. Isolates Paul Tetteh Asare 1 , Katrin Zurfluh 2, Anna Greppi 1, Denise Lynch 2, Clarissa Schwab 1, Roger Stephan 2 and Christophe Lacroix 1,* 1 Laboratory of Food Biotechnology, Institute of Food, Nutrition and Health, ETH Zürich, 8092 Zürich, Switzerland; [email protected] (P.T.A.); [email protected] (A.G.); [email protected] (C.S.) 2 Institute for Food Hygiene and Safety, University of Zürich, 8057 Zürich, Switzerland; katrin.zurfl[email protected] (K.Z.); [email protected] (D.L.); [email protected] (R.S.) * Correspondence: [email protected]; Tel.: +41-44-632-48-67 Received: 17 December 2019; Accepted: 4 January 2020; Published: 6 January 2020 Abstract: Reuterin is a broad-spectrum antimicrobial system produced by specific strains of Lactobacillus reuteri during anaerobic metabolism of glycerol. Acrolein is the main component responsible for its antimicrobial activity. Here, the sensitivity of Campylobacter jejuni (n = 51) and Campylobacter coli (n = 20) isolates from chicken meat and human stool samples to reuterin was investigated. The minimum inhibitory concentration (MIC) of C. jejuni and C. coli strains was measured between 1.5 and 3.0 µM of acrolein, below the MIC of the sensitive indicator strain Escherichia coli K12 (16.5 µM acrolein). The interaction of C. jejuni N16-1419 and the reuterin-producing L. reuteri PTA5_F13 was studied during 24 h co-cultures with or without glycerol. A high C. jejuni growth was observed in cultures without glycerol. In contrast, C. jejuni growth decreased from 7.3 0.1 log CFU/mL to below ± detection limit (1 log CFU/mL) during co-cultures added with 28 mM glycerol. This bactericidal effect could be attributed to in situ reuterin production. The low MIC observed and the high sensitivity towards in situ produced reuterin suggests L. reuteri combined with glycerol, as a possible intervention option to reduce Campylobacter in the food chain. Keywords: Acrolein; reuterin; antimicrobial; Lactobacillus reuteri; Campylobacter 1. Introduction Campylobacter spp., mainly C. jejuni and C. coli, are the most commonly reported foodborne pathogens in the European Union, with 246,307 confirmed cases of human campylobacteriosis in 2016 [1]. Related economic costs are estimated to be around 2.4 billion ¿ in the EU per year [2]. Most Campylobacter infections occur as sporadic cases rather than as outbreaks [3]. Several epidemiological studies indicated that improper handling of raw meat from chickens that carry a high load of Campylobacter is the major source of human infections [4]. Campylobacter infections in humans are usually self-limiting and do not require antibiotic therapy [5]. However, in severe cases, antibiotics such as ciprofloxacin, tetracycline and erythromycin can be prescribed [6]. However, the efficiency of antibiotics against Campylobacter infections is decreasing due to an increase in antibiotic resistance [7]. The use of antibiotics in poultry production may contribute to the emergence of resistant strains in human through the food chain [8]. Nowadays, there is an increasing interest in intervention strategies to reduce the presence of Campylobacter spp. in the poultry meat production chain to lower the risk of Campylobacter exposure. Microorganisms 2020, 8, 78; doi:10.3390/microorganisms8010078 www.mdpi.com/journal/microorganisms Microorganisms 2020, 8, 78 2 of 12 MicroorganismsReuterin 2020 is a, potent8, x FOR antimicrobialPEER REVIEW system produced by certain strains of Lactobacillus reuteri2 offrom 12 glycerol in a single reaction catalysed by the enzyme glycerol/diol dehydratase PduCDE [9]. Reuterin is ais dynamic a dynamic multi-compound multi-compound system system consisting consisting of 3-hydroxypropionaldehyde of 3-hydroxypropionaldehyde (3-HPA), (3-HPA), 3-HPA hydrate,3-HPA 3-HPAhydrate, dimer 3-HPA and dimer acrolein and [10 acrolein]. 3-HPA [10]. can 3-HPA be further can be metabolised further metabolised to 1,3-propanediol to 1,3-propanediol (1,3-PDO) (1,3- and 3-hydroxypropionatePDO) and 3-hydroxypropionate (3-HP) by the(3-HP) enzymes by the encodedenzymes encoded by the propanediol-utilisation by the propanediol-utilisation (pdu) operon (pdu) (Figureoperon1). (Figure Several 1). studies Several found studies that found reuterin that reuterin solutions solutions exhibit antimicrobial exhibit antimicrobial activities activities against aagainst broad rangea broad of Gram-positiverange of Gram-positive and Gram-negative and Gram-negative bacteria, bacteria, yeasts, moulds, yeasts, moulds, and protozoa and protozoa [11]. This [11]. activity This hasactivity been attributedhas been attributed to reuterin to causing reuterin depletion causing of depletion free thiol of groups free thiol in glutathione groups in (GSH),glutathione proteins, (GSH), and enzymes,proteins, resultingand enzymes, in an resulting imbalance in of an the imbalance cellular redoxof the statuscellular which redox leads status to which bacterial leads cell to death bacterial [12]. Wecell recently death showed[12]. We that recently acrolein showed is the mainthat componentacrolein is responsiblethe main component for the antimicrobial responsible activity for the of reuterinantimicrobial [10,13 ].activity of reuterin [10,13]. HO OH + NAD 1,3-Propanediol NADH Glycerol PduQ HO OH H O HO O OH 2 3-HPA + PduP NAD Dehydratase PduCDE O PduL O PduW O NADH HO OPO 2- – HO S-CoA 3 ADP ATP HO O 3-Hydroxypropionyl-CoA 3-Hydroxypropionyl 3-Hydroxypropionate phosphate Reuterin system O OH HO O 3-HPA dimer O HO O OH Acrolein 3-HPA HO OH 3-HPA hydrate FigureFigure 1. 1.Glycerol Glycerol metabolismmetabolism byby reuterin-producingreuterin-producing L. reuteri. Anaerobic metabolism metabolism of of glycerol glycerol by by reuterinreuterin producing producingL. reuteri L. reuterito 3-hydroxypropionaldehyde to 3-hydroxypropionaldehyde (3-HPA) and (3-HPA) further toand 3-hydroxypropionate further to 3- (3-HP)hydroxypropionate and 1,3-propanediol (3-HP) (1,3-PDO).and 1,3-propanediol In an aqueous (1,3-PDO). environment, In an aqueous 3-HPA isenvironment, quickly dimerised 3-HPA and is hydratedquickly dimerised to form HPA-dimer and hydrated and to HPA-hydrate form HPA-dimer and alsoand spontaneouslyHPA-hydrate and dehydrates also spontaneously to acrolein. PduQ,dehydrates 1,3-PDO to acrolein. dehydrogenase; PduQ, 1,3-PDO PduP, CoA-dependentdehydrogenase; propionaldehydePduP, CoA-dependent dehydrogenase; propionaldehyde PduL, phosphotransacetylase;dehydrogenase; PduL, PduW,phosphotransac propionateetylase; kinase. PduW, propionate kinase. L. reuteri is known to form stable biofilms in the crop and to persist in poultry gastrointestinal L. reuteri is known to form stable biofilms in the crop and to persist in poultry gastrointestinal (GI)(GI) tracts tracts [ 14[14].]. In In the the poultrypoultry industry,industry, glycerolglycerol isis usedused asas energy feedstuff [15] [15] and and to to improve improve feed feed pelletpellet quality quality [16 [16].]. Therefore, Therefore, in in situ situ reuterin reuterin production production may may be be used used as as an an active active natural natural mechanism mechanism in chickenin chicken colonised colonised with reuterin-producingwith reuterin-producingL. reuteri L., to reuteri inhibit, enteropathogensto inhibit enteropathogens such as Campylobacter such as inCampylobacter the gastrointestinal in the tractgastrointestinal (GIT). However, tract (GIT). to our Howe knowledge,ver, to thereour isknowledge, limited information there is limited on the sensitivityinformation of Campylobacter on the sensitivityspp. of to Campylobacter this broad-spectrum spp. to antimicrobial this broad-spectr system.um Inantimicrobial this study, wesystem. assessed In thethis potential study, ofwe reuterin assessed to inhibitthe potentialCampylobacter of reuterinspp.The to inhibit antimicrobial Campylobacter efficacy ofspp. reuterin The wasantimicrobial evaluated onefficacy a panel of of reuterinC. jejuni wasand evaluatedC. coli isolated on a panel from variousof C. jejuni sources, and C. including coli isolated human from stools, various chicken sources, GIT andincluding meat. Thehuman bactericidal stools, chicken activity GIT of andin situ meat.-produced The bactericidal reuterin on activityC. jejuni of inwas situ tested-produced in co-cultures reuterin withon C. reuterin-producing jejuni was tested inL. co-cultures reuteri, in the with presence reuterin-producing and absence ofL. glycerol.reuteri, in the presence and absence of glycerol. 2. Materials and Methods 2.1. Bacterial Strains, Media and Growth Conditions Seventy-one (71) Campylobacter spp. (C. jejuni (n = 51) and C. coli (n = 20)) isolated from the chicken intestine (n = 2), human stool samples (n = 50) and chicken meat (n = 19) in 2016 and 2017 Microorganisms 2020, 8, 78 3 of 12 2. Materials and Methods 2.1. Bacterial Strains, Media and Growth Conditions Seventy-one (71) Campylobacter spp. (C. jejuni (n = 51) and C. coli (n = 20)) isolated from the chicken intestine (n = 2), human stool samples (n = 50) and chicken meat (n = 19) in 2016 and 2017 with different antibiotic resistance profiles were supplied by the National Centre for Enteropathogenic Bacteria and Listeria (NENT; University of Zurich, Zurich, Switzerland) (Table S1). Before use, Campylobacter strains were sub-cultured twice at 41 ◦C for 48 h on Blood Agar, 5% sheep blood (Oxoid AG, Pratteln, Switzerland)
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