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Applied and Environmental Microbiology, January 2009, p. 281-285, Vol. 75, No. 1
0099-2240/09/$08.00+0     doi:10.1128/AEM.01803-08
Copyright © 2009, American Society for Microbiology. All Rights Reserved.

Autoinducer-2 Production in Campylobacter jejuni Contributes to Chicken Colonization {triangledown}

Beatriz Quiñones,* William G. Miller, Anna H. Bates, and Robert E. Mandrell

U.S. Department of Agriculture, Agricultural Research Service, Western Regional Research Center, Produce Safety and Microbiology Research Unit, Albany, California 94710

Received 4 August 2008/ Accepted 6 November 2008


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ABSTRACT
 
Inactivation of luxS, encoding an AI-2 biosynthesis enzyme, in Campylobacter jejuni strain 81-176 significantly reduced colonization of the chick lower gastrointestinal tract, chemotaxis toward organic acids, and in vitro adherence to LMH chicken hepatoma cells. Thus, AI-2 production in C. jejuni contributes to host colonization and interactions with epithelial cells.


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INTRODUCTION
 
The enteric food-borne pathogen Campylobacter jejuni is considered a significant contributor to human gastrointestinal disease (1, 24, 31). A major source of campylobacteriosis is the consumption and handling of undercooked poultry products. C. jejuni colonizes preferentially the avian gastrointestinal tract in a commensal relationship. During the slaughtering process, the gastrointestinal contents can be released and contaminate the chicken meat products. Furthermore, several studies have shown that a large proportion of retail chicken products contain C. jejuni (22, 26, 28). Thus, a better understanding of processes that contribute to the growth and survival of C. jejuni in chickens could lead to efficient intervention strategies for reducing C. jejuni population sizes in this natural reservoir.

Bacterial populations are capable of coordinating the expression of virulence and host colonization factors by detecting diffusible signal molecules (18, 39, 42). Most pathogenic enteric bacteria produce the signal autoinducer 2 (AI-2) (18, 35, 42), a collection of interchangeable molecules synthesized by a key enzyme known as LuxS (30). Both gram-positive and gram-negative bacteria produce AI-2, suggesting that this molecule may be a "universal" signal for interspecies communication (33, 35, 42). AI-2 synthesis is connected to cellular metabolism and may provide information about the fitness of the bacterial population (30, 39, 41). Recent studies that examined AI-2-controlled phenotypes in pathogenic bacteria demonstrated that AI-2 regulates "niche-specific" functions for host colonization and virulence (39, 42).

Several recent reports have examined AI-2 production in C. jejuni. AI-2 production was demonstrated to regulate swarming motility (8, 12, 15), autoagglutination (9, 15), biofilm formation (29), sensitivity to hydrogen peroxide (12), and the transcription of the cytolethal distending toxin genes (cdtABC) (16). Recently, AI-2 was detected in chicken broth and milk, demonstrating the production of this molecule in the food environment (6). In the present study, a luxS mutation in C. jejuni strain 81-176 was characterized to further understand the contribution of AI-2 production on the colonization of the chicken host and interactions with chicken epithelial cells.


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Bacterial strains, cell line, and culture conditions.
 
The bacterial strains and plasmids that were used in this study are described in Table 1. C. jejuni strains were grown at 42°C under microaerobic conditions on Oxoid anaerobe basal agar or anaerobe basal broth (Remel Inc., Lenexa, KS), as described in previous reports (28). Chloramphenicol and kanamycin were used at concentrations of 20 µg/ml and 50 µg/ml, respectively. The LMH chicken hepatoma cell line ATCC CRL-2117 (17) was maintained in 75-cm2 tissue culture flasks coated with 0.1% gelatin in Waymouth's MB152/1 medium supplemented with 10% fetal bovine serum, 2% chicken serum, and 1% antibiotic solution (Gibco, Grand Island, NY) at 37°C in a 5% CO2 humidified incubator.


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  		TABLE 1. Bacterial strains and plasmids used in this study


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Characterization of a luxS mutant of C. jejuni strain 81-176.
 
C. jejuni strain 81-176 elicits gastroenteritis in humans (4, 20) and also colonizes the gastrointestinal tract in the newborn chick model (13). To characterize AI-2 production and its contribution to the colonization of the chicken host, the luxS mutant strain LXS3 was constructed. The luxS gene in strain RM1221 was PCR amplified with primers LuxF2 (5'-GCAATAAATCAGGATCAGGAAAATAG-3') and LuxR (5'-CCTTCGCTAGTATAACCTCTAAA-3'), using parameters described previously (28), and then cloned into pCR4-TOPO (Invitrogen, Carlsbad, CA) to yield pCR4-lux. Strain RM1221 was selected for PCR amplification of the luxS gene because the genome sequence information was available at the time when the LXS3 strain was constructed. A 0.8-kb fragment containing the chloramphenicol resistance cassette from pRY109 (44) was then cloned at an internal HincII site of luxS, resulting in pBQ100, which was introduced into strain 81-176 by electroporation (10). The high DNA sequence identity (96.8%) between the luxS genes of strains RM1221 and 81-176 allowed for an allelic exchange to occur without plasmid integration in strain LXS3. This result was confirmed by PCR amplification and DNA sequencing of the luxS gene in strain LXS3 after selection with chloramphenicol. The integration of the chloramphenicol cassette was verified to be stable after the luxS mutant was grown for 100 generations in the absence of chloramphenicol. To complement the luxS mutation in strain LXS3, a 1.3-kb fragment containing the promoter-proximal region and intact luxS gene was PCR amplified from strain 81-176 with primers Uplux3 (5'-TCTACTATAGGGATATCAAATTGTGAA-3') and Downlux1 (5'-CCTATTTTAGAAGCAATTTCTCTTA-3'), sequenced to confirm the absence of point mutations, and cloned into the EcoRI site of pCR4-TOPO, resulting in pBQ7. The luxS gene was then subcloned into the EcoRI site of pWM1015, a plasmid isogenic to pWM1007 (23), to yield pBQ117. Plasmids pBQ117 and pWM1015 were introduced into strain LXS3 by triparental mating with the mobilization helper plasmid pRK2073, as in previous studies (23).

The amount of extracellular AI-2 produced by C. jejuni wild-type 81-176(pWM1007) and the luxS mutant LXS3, LXS3(pBQ117), and LXS3(pWM1015) strains (Table 1) was determined at various cell concentrations by measuring the induction of luminescence in the Vibrio harveyi reporter strain BB170, by following previously described procedures (5, 34). The results demonstrated that AI-2 production in the wild-type strain peaked during mid- to late-exponential growth and rapidly decreased at high cell concentrations during entry into the stationary growth phase (Fig. 1A). In contrast, AI-2 production was completely abolished in the luxS mutant at all stages of growth (Fig. 1A). Complementation of the luxS mutation by expressing an intact copy of luxS on the plasmid pBQ117 in strain LXS3 restored AI-2 production to levels similar to those in the wild-type strain, while introduction of the isogenic plasmid pWM1015 alone did not rescue AI-2 production (Fig. 1A). Strain LXS3 showed slower growth than the wild type or the complemented LXS3(pBQ117) strain during the exponential growth phase, but all strains reached stationary growth phase at the same time (Fig. 1B), confirming that the reduced AI-2 production in the luxS mutant was not due to altered growth of the cells. Although a previous report documented that extracellular AI-2 levels in C. jejuni strain 11168 increased steadily without any decline (8), the present study is the first one to demonstrate the rapid decrease in extracellular AI-2 production in C. jejuni at high cell concentrations (Fig. 1A). Our finding suggests that a LuxS-regulated import system may operate in C. jejuni, as described for Salmonella enterica serovar Typhimurium and Escherichia coli (36, 37, 43). Finally, the luxS mutant LXS3 strain displayed limited swarming motility at 37°C on semisolid agar, as in other studies (12); motility was fully recovered in the complemented LXS3(pBQ117) strain (data not shown).


Figure 1
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  		FIG. 1. Characterization of a luxS mutant of C. jejuni strain 81-176. (A) The production of extracellular AI-2 as measured by using a Vibrio harveyi bioluminescence assay is shown in cultures of the C. jejuni wild type ({blacktriangleup}) and the luxS mutant strains LXS3 (•), LXS3(pBQ117) ({triangleup}), and LXS3(pWM1015) ({circ}) grown to various cell concentrations. (B) Population sizes of the various C. jejuni strains at different times after inoculation. OD600, optical density at 600 nm.


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Chicken colonization.
 
To examine the role of AI-2 production in chick colonization, 3-day-old, white leghorn chicks were inoculated orally in separate groups with either wild-type 81-176(pWM1007) or the luxS mutant LXS3 strain at approximately 107 CFU for the first trial (50 chicks) or 106 CFU for the second trial (79 chicks). At days 4 and 7 after inoculation for each independent trial, chicks were euthanized, and the intestines, consisting of the duodenum and cecum, were removed and homogenized, as in previous studies (5, 13). Duplicate samples of each homogenate were serially diluted 10-fold in phosphate-buffered saline and plated on Campylobacter blood-free selective agar base (Remel Inc., Lenexa, KS), amended with 30 µg/ml cefoperazone and 10 µg/ml trimethoprim and either kanamycin or chloramphenicol to select for growth of the wild type or luxS mutant, respectively. After a 48- to 72-h incubation at 42°C under microaerobic conditions, the recovered C. jejuni colonies were enumerated, reported as the number of CFU/gram of intestinal content, and further examined by PCR and AI-2 assays to confirm their identity. A P value of less than 0.01 was considered to indicate a statistically significant difference between the medians of the numbers of CFU/gram of intestinal content per strain, according to the Mann-Whitney test (KaleidaGraph version 4.0; Synergy Software, Reading, PA).

The results from the first trial demonstrated that the luxS mutant was below the threshold detection value of 100 CFU/g of intestinal content in 69% (9 of 13) of the chicks at 4 days (Fig. 2A). In contrast, 26% (4 of 15) of the chicks inoculated with the wild type did not show detectable C. jejuni. By day 7, the colonization capability of the wild type was significantly greater (Mann-Whitney test, P < 0.01) than that detected for the luxS mutant (Fig. 2A). For the second trial, the infectious dose of each strain was reduced 10-fold, and the luxS mutant was not recovered at day 4 from 53% (10 of 19) of the chicks compared to 5% (1 of 18) of the chicks inoculated with the wild type (Fig. 2B). In agreement with the results obtained in the first trial (Fig. 2A), significant differences in levels of colonization (Mann-Whitney test, P < 0.01) were observed 7 days after inoculation (Fig. 2B); the luxS mutant was not detected in nearly half (9 of 21) of the chicks (Fig. 2B). The fact that some chicks were colonized by the luxS mutant, mostly in the second trial, may indicate that significant amounts of AI-2, a "universal" bacterial signal (42), could have been supplied by the dominant groups of the endogenous bacterial flora, including members of the Enterobacteriaceae and enterococci (38). As shown for other gastrointestinal bacterial pathogens (5, 21, 25), our findings indicate that LuxS-dependent phenotypes in C. jejuni may contribute to the growth and survival and potentially to adaptation in the chicken host environment.


Figure 2
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  		FIG. 2. Intestinal colonization by C. jejuni strains in 3-day-old chicks. (A) Trial 1. Chickens were inoculated with approximately 107 CFU of either the C. jejuni wild-type ({blacktriangleup}) or the luxS mutant (•) strain, and the numbers of CFU of C. jejuni strains recovered were determined at 4 or 7 days. (B) Trial 2. Chickens were inoculated with approximately 106 CFU per strain. Both panels show the results from two independent experiments. The horizontal bars for each strain represent the log10-transformed mean numbers of CFU/gram of intestine content from all chicks. The n indicates the number of chicks euthanized, and each symbol represents the log10-transformed number of CFU/gram of intestine content from an individual chick.


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Chemotactic response to amino acids and organic acids.
 
Chemotaxis in C. jejuni has been demonstrated to be required for the colonization of the chick gastrointestinal tract (13). Several chemoattractants, such as amino acids and organic acids, were tested by the hard-agar plug method (14). Chemotaxis was determined by measuring the radius of bacterial accumulation from the edge of the agar plug with the test chemoattractant after incubation for 24 h at 37°C under microaerobic conditions (Table 2). The zones of bacterial accumulation around agar plugs that contained the amino acids asparagine, aspartate, glutamate, or glutamine were significantly greater for the luxS mutant than for the wild type (Table 2). In contrast, the wild type displayed an increased chemotactic response toward all tested organic acids (Table 2), and no bacterial accumulation was observed when agar plugs containing phosphate-buffered saline were tested (data not shown). Given that C. jejuni ferments organic acids in the avian gastrointestinal tract for energy (31), the weaker chemoattraction to organic acids in the luxS mutant may have contributed to its reduced ability to colonize chicks. Interestingly, the increased chemotactic behavior toward some amino acids by the luxS mutant may have resulted consequently from disrupted amino acid biosynthesis and transport as well as altered carbon compound catabolism, as previously shown for the enteric food-borne pathogen E. coli O157:H7 (32, 40).


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  		TABLE 2. Chemotaxis in the presence of several chemoattractants


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Adherence to LMH cells.
 
To explore the role of AI-2 production in regulating adherence to host epithelial cells, LMH cells were seeded at 7 x 104 cells per well on 24-well tissue culture plates precoated with 0.1% gelatin (19). Cultures of the C. jejuni wild-type, luxS mutant LXS3, and complemented LXS3(pBQ117) strains were incubated with the LMH cell monolayer at a multiplicity of infection of 100 to 200 in Waymouth's MB 752/1 complete growth medium without antibiotics for 1 h at 37°C with 5% CO2, and adherence was determined as previously described (19). Adherence to the LMH cells was significantly reduced in the luxS mutant strain (Fig. 3), and this defect was fully restored in the complemented LXS3(pBQ117) strain (Fig. 3). These findings indicated that LuxS-dependent phenotypes may facilitate the interactions of C. jejuni with the chicken host cells. Gentamicin protection assays showed that only a small fraction (0.08 to 0.1%) of C. jejuni wild-type cells effectively invaded LMH cells (data not shown). Therefore, the adherence results, presented in Fig. 3, represented the vast majority of C. jejuni wild-type cells that interacted with the LMH cells. Several studies have identified a strong correlation between the colonization of the chick intestine and the interactions with human intestinal cells, suggesting that determinants regulating the commensal colonization may be linked to factors regulating virulence (11, 27, 45). Given that in many examples of pathogenic bacteria LuxS-dependent phenotypes have been implicated in the regulation of virulence (18, 39), additional genomic analyses of traits regulated by AI-2 in C. jejuni may provide new insights into the regulation of growth and survival in the food supply as well as virulence.


Figure 3
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  		FIG. 3. Adherence to LMH chicken cells. Adherence was expressed as the percentage of the inoculum that remained associated with the epithelial cells. Results are the means and standard errors from two independent experiments, each consisting of three replicates. Bars with the same lowercase letter were not significantly different at a P of <0.01, according to Tukey's multiple-comparison test (KaleidaGraph version 4.0; Synergy Software, Reading, PA).


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ACKNOWLEDGMENTS
 
This work was supported by the U.S. Department of Agriculture, Agricultural Research Service, CRIS project number 5325-42000-045.

We thank Felicidad Bautista, Michelle S. Swimley, and Rommel D. Alfonso for technical assistance and Glenn Dulla, Jeri Barak, and Craig T. Parker for critical reading of the manuscript. Bonnie Bassler is acknowledged for kindly providing the Vibrio harveyi reporter strain BB170.


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FOOTNOTES
 
* Corresponding author. Mailing address: U.S. Department of Agriculture, Agricultural Research Service, Western Regional Research Center, Produce Safety and Microbiology Research Unit, 800 Buchanan Street, Albany, CA 94710. Phone: (510) 559-6097. Fax: (510) 559-6162. E-mail: Beatriz.Quinones{at}ars.usda.gov Back

{triangledown} Published ahead of print on 14 November 2008. Back


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Applied and Environmental Microbiology, January 2009, p. 281-285, Vol. 75, No. 1
0099-2240/09/$08.00+0     doi:10.1128/AEM.01803-08
Copyright © 2009, American Society for Microbiology. All Rights Reserved.




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