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Poult Sci 2008. 87:329-334. doi:10.3382/ps.2007-00282
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METABOLISM AND NUTRITION: Research Notes

Identification of Lactic Acid Bacteria from Poultry Feces: Evidence on Anti-Campylobacter and Anti-Listeria Activities

L. Nazef, Y. Belguesmia, A. Tani, H. Prévost and D. Drider1

UMR INRA 1014 SECALIM, École Nationale D’Ingénieurs des Techniques des Industries Agro-Alimentaires, Rue de la Géraudière, BP 82225, 44322 Nantes Cedex 3, France

1 Corresponding author: drider{at}enitiaa-nantes.fr


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
Forty-five strains of lactic acid bacteria were isolated from poultry feces sampled from an industrial farm located in the Nantes area (France), and most of them belong to the Streptococcus or Lactobacillus genus according to the results obtained by Galerie API and molecular methods. The most representative lactic acid bacteria strains were screened for antibacterial compound production against 2 indicator organisms (Listeria innocua F and Campylobacter jejuni 11168) by means of the agar diffusion test. Strain S37, identified as Enterococcus faecalis, exhibited a clear antilisterial activity and a slight anti-Campylobacter activity, whereas strain S42, identified as Lactobacillus reuteri, exhibited only anti-Campylobacter activity. Regarding the results of proteolytic, heat, and neutralizing treatments of supernatants from the aforementioned strains, we can conclude that antagonism observed is attributed to antimicrobial peptide or bacteriocin in the case of strain S37, whereas it is ascribable to a nonbacteriocin, likely a reuterin, in the case of strain S42.

Key Words: lactic acid bacteria • poultry • antimicrobial activity • bacteriocin • feces


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
Campylobacter jejuni commonly causes foodborne illness worldwide. A significant source for human Campylobacter infections is contaminated poultry meats. Increasing resistance of Campylobacter to antibiotics raises an urgent demand for development of alternative strategies to control Campylobacter infections in both chickens and humans.

Lactic acid bacteria (LAB) are present in the microbiota of mammals and birds (Fuller, 1989), and those originating in the intestine have undergone intensive study for their potential probiotic properties and their rapid establishment as bacterial communities for the prevention of colonization by pathogenic bacteria. Different studies aimed to identify the microbiota of the gastrointestinal tract of poultry pointed out the predominance of lactobacilli such as Lactobacillus crispatus, which was isolated from chicken crops and intestine (Beasley et al., 2004); Lactobacillus rhamnosus TB1, from the intestinal tract of chicken and exhibiting good adherence and in vivo colonization (Bouzaine et al., 2005); Lactobacillus salivarius with antagonism against Escherichia coli and Salmonella Enteritidis were found in gastrointestinal tracts of chicks (Garriga et al., 1998); and, finally, strains of Lactobacillus thermotolerans G12, G22, G35T, G43, and G44 were isolated from chicken feces (Niamsup et al., 2003). Lactobacillus isolates from chicken origin are good sources of antimicrobial peptides, bacteriocins, or both (Lima et al., 2007), whereas L. salivarius UCC118, a recently sequenced and genetically tractable probiotic strain of human origin, produces a bacteriocin in vivo that can significantly protect mice against infection with the invasive foodborne pathogen, Listeria monocytogenes (Corr et al., 2007).

Antimicrobial peptides are short bactericidal peptides widely present in animal intestines that have become recognized as a novel class of antibiotics to control foodborne pathogens in poultry. Bacteriocins produced by LAB belonging to the Lactobacillus genus are active against some gram-positive bacteria and occasionally gram-negative bacteria (Todorov et al., 2004). Recent studies revealed the role of bacteriocins from Bacillus circulans, Paenibacillus polymyxa (Stern et al., 2005), and L. salivarius (Stern et al., 2006) in reducing cecal Campylobacter colonization in broiler chickens infected with C. jejuni.

The aim of the present study is to describe LAB present in poultry feces sampled from an industrial farm in the Nantes area (France). Upon biochemical and molecular identification of these isolates, the presence of strains with potential antagonism against C. jejuni and Listeria innocua F was investigated and charted.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 REFERENCES
 
In this study, we have used C. jejuni 11168 and Listeria innocua F as indicator organisms, whereas Carnobacterium divergens V41 (Pilet et al., 1995), L. salivarius NRRL B-30514 (Stern et al., 2006), and P. polymyxa NRRL B-30509 (Stern et al., 2006) were used as strains producing bacteriocins. Campylobacter jejuni 11168 was grown, at 43°C for 18 to 24 h, in Mueller-Hinton medium or Columbia medium containing 5% of horse blood, under a modified atmosphere of 85% N2, 10% CO2, and 5% O2. Listeria innocua F was grown, without aeration, at 30°C for 24 h in de Man-Rogosa-Sharpe medium (de Man et al., 1964). Growths of Carnobacterium divergens V41 and L. salivarius were realized at 30°C for 18 to 24h, without aeration, in de Man-Rogosa-Sharpe medium, whereas growth of P. polymyxa was realized in similar conditions but on Elliker agar medium.

Twenty-eight samples of poultry feces were sampled randomly in a farm located in the Nantes area (France); 0.5 g of each sample was diluted in 4.5 mL of sterile physiological water and roughly homogenized. Serial dilutions ranking from 10–3 to 10–7 were prepared. Afterwards, 100 µL of each dilution was plated in duplicate into Elliker agar medium. Plates were incubated for 24 to 48 h at 30°C. After this incubation time, plates were inspected, and those containing from 50 to 100 colonies were kept for a preliminary identification based on gram-staining and production of catalase, oxidase, and acid from glucose (Barrow and Feltham, 1993). The identification of LAB was performed by Galerie API-50 CH and API Web software (Biomérieux, Marcy, L’Etoile, France). Dendrograms showing similarities between LAB isolates were drawn using the statistical approach based on the Euclidian distance algorithm.

Molecular methods are known to be important for bacterial identification (Drancourt et al., 2000; Greetham et al., 2002). For this purpose, PCR targeting the 16S-23S rRNA intergenic region, commonly called internal transcribed spacer PCR, was performed for the most representative strains using the protocol and program previously described (Kabadjova et al., 2002). Sequencing of the entire 16S gene (~1,500 bases) was carried out as well on the most representative LAB with the Taq Dye-Deoxy terminator cycle sequencing method (Genome Express, Meylan, France). Sequences were compared with that available in the National Center for Biotechnology Information blast library.

Anti-Listeria activity assay was carried as follows: 10 mL of cell-free supernatant of each LAB isolate was obtained by centrifugation (8,000 x g; 6 min at 4°C) of bacteria culture grown at 30°C for 25 h. The entire cell-free supernatant was heated during 10 min at 100°C and stored at –20°C. Bacteriocin activity was determined by the agar diffusion assay against Listeria innocua F as indictor strains according to the following: 10 µL of the preheated supernatant (cell free) was added to Elliker soft agar plates containing 107 cfu/mL of Listeria indicator strain. The growth inhibition of the indicator strain was determined after 16 h of incubation at 30°C by observing the formation of zone of inhibition around the supernatant drop.

Anti-Campylobacter activity was assessed as described by Stern et al. (2006). Approximately 0.2 mL, containing 107 cfu of each most representative strain, was suspended in normal saline, distributed onto Elliker agar, and incubated at 37°C for 24 h. Agar blocks containing the isolated colonies were aseptically cut and transferred into media such as Mueller-Hinton agar, Colombia agar supplemented with 5% blood, or both, and freshly seeded with indicator organism C. jejuni 11168 at 107 cfu/mL. Plates were incubated at 43°C for 24 to 48 h under the microaerobic atmosphere described above. Activity was assessed by observing the zone of inhibition formed around the drop. Supernatants from cultures of the most representative isolates were used instead of the agar blocks.

Nevertheless, each supernatant was treated by catalase at 500 U/mL (Merck, Dijon, France) and proteinase K at 0.2 mg/mL (Boehringer, Mannheim, Germany) to determine the proteinaceous nature of antimicrobial substances. Each supernatant was also subjected to heat treatment (10 min at 80°C) and neutralizing action to pH 6.5 with 1 M of sodium hydroxide (Merck) to examine the stability of antimicrobial peptide and discard any erroneous interpretation due to organic acid or hydrogen peroxide production.


   RESULTS AND DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
REFERENCES
 
The microbiological analysis allowed isolation of 900 colonies, in which only 45 colonies satisfied the basic taxonomical criteria of LAB (Barrow and Feltham 1993). These LAB isolates were numbered from S1 to S45, and their identification was carried out, in the first instance, with a biochemical approach using Galerie API-50 CH (Biomérieux) and then completed when necessary with the heterofermentation test using the Durham tube method. Data from Galerie API-50 CH were statistically interpreted using the Euclidian distance matrix, leading to a dendrogram in which LAB isolates were divided into clusters relying on morphological and biochemical characters (Figure 1AGo).


Figure 1
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  		Figure 1. (A) Dendrogram of dissimilarity obtained from biochemical data, after similarity elucidation with Euclidean distance approach. (B) Amplification of the spacers between 16S-23S genes of the most representative lactic acid bacteria isolates. Twenty microliters of PCR product was loaded on 2% agarose gel stained in ethidium bromide and photographed on an ultraviolet transluminator.

 
In regard to Galerie API LAB results, the LAB isolates S34, S24, S39, S4, S17, S3, S41, S36, S42, S25, S44, and S35 were considered as the most representative ones. Afterwards, we have studied the intergenic region 16S-23S for the most representative strains and revealed their patterns (Figures 1BGo and 1B’Go).

The polymorphism between 16S and 23S rRNA genes has received a great deal of attention for rapid discrimination of bacteria (Jensen and Straus, 1993; Grtler and Stanisich, 1996; Baudart et al., 2000; Kabadjova et al., 2002). As evident from Figure 1BGo, the intergenic region 16S-23S rDNA of LAB isolates S4, S11, S17, and S3 is composed of one major intergenic spacer region (ISR) of approximately 0.7 kb in size. This type of polymorphism is usually found in Leuconostoc (0.6 kb), Lactococcus (0.5 kb), and Streptococcus (0.55 kb; Kabadjova et al., 2002). In direct line, the LAB isolates S4, S11, S17, and S3 were identified, by sequencing their 16 rDNA, as Streptococcus gallolyticus (Table 1Go). Streptococcus gallolyticus has undergone extensive taxonomic revisions, and most isolates belonging to biotypes I and II of the Streptococcus bovis species have been reclassified as Streptococcus gallolyticus. This potentially pathogenic bacterium was found in the microbiota of pigeon intestines (Baele et al., 2002) and is responsible for mastitis in cattle, septicemia in pigeons, and even meningitis and endocarditis in humans (Facklam, 2002). Strains of Streptococcus gallolyticus with different levels of virulence (high and low levels) were shown to attach to the intestinal tract of pigeons (Kimpe et al., 2003). Finally, Streptococcus gallolyticus was considered as 1 of the pathogens most frequently responsible for endocarditis and infection in certain countries, such as France (Leclercq et al., 2005).


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  		Table 1. Main lactic acid bacteria (LAB) isolates identified with 16S rDNA sequence
 
Molecular characterization of LAB using ISR-PCR showed that 3 ISR within the intergenic region 16S-23S are specific to Carnobacterium (Kabadjova et al., 2002). Amplification of the spacers between 16S-23S rDNA genes of LAB isolates S25 and S44, which were identified as Lactobacillus ingluviei (Table 1Go), has revealed the presence of 3 ISR. This result is in good agreement with that reported by Valcheva et al. (2007), who reported the presence of 3 ISR for Lactobacillus sanfranciscensis.

Lactobacillus ingluviei was isolated from the intestinal tract of pigeons and identified for the first time by Baele et al. (2003). Lactobacillus ingluviei was shown to be phenotypically close to L. salivarius in regard to transferred DNA-PCR fingerprints (Baele et al., 2003). The 16S-23S intergenic region of L. ingluviei deserves more investigation. For this purpose, cloning and sequencing of each ISR from a significant number of isolates will facilitate identification of this strain with specific probes.

Noteworthy, the strain S41 was identified as Lactobacillus murinus (Table 1Go). This bacterium was reported early in the literature as being present in the digestive tracts of mice and rats (Hemme et al., 1980). Almost 2 decades after its isolation, the subcommittee on the taxonomy of Bifidobacterium, Lactobacillus, and related organisms suggested more analysis mainly by targeting 16S rDNA sequences and DNA homologies of separate species (Klein, 2001). Recently, a study carried out on L. murinus has revealed an antagonism effect exerted against Bacillus cereus and Shigella sonnei through synthesis of 2 low molecular weight compounds (Nardi et al., 2005).

Listericidal activity was only observed with supernatant prepared from Enterococcus faecalis (strain S37) as supported by a clear zone of inhibition shown on Figure 2DGo. This inhibition is attributed to a compound of proteinaceous nature, which is either a bacteriocin or antimicrobial peptide. Enterococci are LAB of importance in food, public health, and medical microbiology, and many strains produce bacteriocins called enterocins, some of which are genetically characterized (Franz et al., 2007). The potency of enterocins was established in many occasions and recently was confirmed in mastering the growth of pathogenic Staphylococcus aureus (Ananou et al., 2007).


Figure 2
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  		Figure 2. (A) Inhibition zones corresponding to anti-Listeria activity obtained with divercin V41, used as positive control, and supernatant from Enterococcus faecalis (strain S37). (B) Anti-Campylobacter obtained with parcels of colonies from (1) Paenibacillus polymyxa NRRL B-30509, (2) Lactobacillus salivarius NRRL B-30514, (3) L. salivarius + strain S42, and (4) P. polymyxa NRRL B-30509 + strain S42. (C) Colony 42 (L. reuteri). (D) Colony S37 (E. faecalis).

 
Attempts to unravel anti-Campylobacter activities were assessed with class IIa bacteriocins such as divercin V41 produced by Carnobacterium divergens V41 (Métivier et al., 1998), enterocin P produced by Enterococcus faecium P13 (Cintas et al., 1997), mesentericin Y105 produced by Leuconostoc mesenteroides Y105 (Fleury et al., 1996), sakacin A produced by Lactobacillus sakei Lb 706 (Holck et al., 1994), and substances ST31 and ST13BR known for their inhibitory activity against gram-negative bacteria (Todorov et al., 2004). All these assays were unsuccessful.

To our knowledge, only reuterin (Arques et al., 2004), bacteriocin OR-7 (Stern et al., 2006), and bacteriocin B602 produced by P. polymyxa NRRL B-30509 (Svetoch et al., 2005) were able to exert an antagonistic effect against C. jejuni. Bacteriocin OR-7 is nearly identical to acidocin A, a bacteriocin produced by Lactobacillus acidophilus (Kanatani et al., 1995).

In this study, the anti-Campylobacter activity was observed with isolates S37 and mainly S42 (Lactobacillus reuteri). Characterization of supernatant from strain S42 indicated that antimicrobial substance is insensitive to proteolytic treatment, which indicates the nonprotein nature of the antimicrobial substance. Furthermore, combination of P. polymyxa NRRL B-30509 and strain 42 allowed formation of highest zone of inhibition, which could be interpreted by a synergistic effect.

Lactobacillus reuteri is a prominent member of the Lactobacillus gastrointestinal ecosystem of humans and poultry (Talarico et al., 1988). This bacterium is known to convert glycerol into 3-hydroxypropionaldehyde, which is a potent antimicrobial substance. Exploration of its application as food preservative or as a therapeutic auxiliary agent has been demonstrated through the literature. The addition of reuterin on the inoculated tissue was shown to reduce viability of Pseudomonas aeruginosa, a common cause of nosocomial biomaterial-related infections (Liang et al., 2003). Another study pointed out the role of reuterin in the prevention of adhesion of Staphylococcus aureus into gastrointestinal tract (Vesterlund et al., 2006).

Throughout this report, we have initiated the description of poultry gastrointestinal microbiota, which contains a rich ecosystem comprising various LAB and pathogenic strains. The LAB found in poultry feces demonstrates their abilities to resist the harsh condition of gastrointestine. Lactic acid bacteria isolates exhibiting anti-Campylobacter activity constitute an interesting trait that deserves more investigation to demonstrate the probiotic function and improve chicken health and food safety.


   ACKNOWLEDGMENTS
 
We would like to thank Philippe Courcoux (École Nationale D’Ingénieurs des Techniques des Industries Agro-Alimentaires, Nantes, France) for his assistance in statistical analysis. Research at UMR INRA 1014 SECALIM École Nationale D’Ingénieurs des Techniques des Industries Agro-Alimentaires-ENVN was supported by la region des pays de la Loire through VANAM II.

Received for publication July 12, 2007. Accepted for publication October 11, 2007.


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