Skip to main content
Top
Published in: Gut Pathogens 1/2014

Open Access 01-12-2014 | Research

The interplay between Campylobacter and Helicobacter species and other gastrointestinal microbiota of commercial broiler chickens

Authors: Nadeem O Kaakoush, Nidhi Sodhi, Jeremy W Chenu, Julian M Cox, Stephen M Riordan, Hazel M Mitchell

Published in: Gut Pathogens | Issue 1/2014

Login to get access

Abstract

Background

Poultry represent an important source of foodborne enteropathogens, in particular thermophilic Campylobacter species. Many of these organisms colonize the intestinal tract of broiler chickens as harmless commensals, and therefore, often remain undetected prior to slaughter. The exact reasons for the lack of clinical disease are unknown, but analysis of the gastrointestinal microbiota of broiler chickens may improve our understanding of the microbial interactions with the host.

Methods

In this study, the fecal microbiota of 31 market-age (56-day old) broiler chickens, from two different farms, was analyzed using high throughput sequencing. The samples were then screened for two emerging human pathogens, Campylobacter concisus and Helicobacter pullorum, using species-specific PCR.

Results

The gastrointestinal microbiota of chickens was classified into four potential enterotypes, similar to that of humans, where three enterotypes have been identified. The results indicated that variations between farms may have contributed to differences in the microbiota, though each of the four enterotypes were found in both farms suggesting that these groupings did not occur by chance. In addition to the identification of Campylobacter jejuni subspecies doylei and the emerging species, C. concisus, C. upsaliensis and H. pullorum, several differences in the prevalence of human pathogens within these enterotypes were observed. Further analysis revealed microbial taxa with the potential to increase the likelihood of colonization by a number of these pathogens, including C. jejuni.

Conclusion

Depletion of these taxa and the addition of taxa that compete with these pathogens, may form the basis of competitive exclusion strategies to eliminate them from the gastrointestinal tract of chickens.
Appendix
Available only for authorised users
Literature
1.
go back to reference European Food Safety Authority: Scientific opinion on Campylobacter in broiler meat production: control options and performance objectives and/or targets at different stages of the food chain. EFSA J. 2011, 9: 2105- European Food Safety Authority: Scientific opinion on Campylobacter in broiler meat production: control options and performance objectives and/or targets at different stages of the food chain. EFSA J. 2011, 9: 2105-
2.
go back to reference Ellis-Iversen J, Ridley A, Morris V, Sowa A, Harris J, Atterbury R, Sparks N, Allen V: Persistent environmental reservoirs on farms as risk factors for Campylobacter in commercial poultry. Epidemiol Infect. 2012, 140: 916-924. 10.1017/S095026881100118X.CrossRefPubMed Ellis-Iversen J, Ridley A, Morris V, Sowa A, Harris J, Atterbury R, Sparks N, Allen V: Persistent environmental reservoirs on farms as risk factors for Campylobacter in commercial poultry. Epidemiol Infect. 2012, 140: 916-924. 10.1017/S095026881100118X.CrossRefPubMed
3.
go back to reference Newell DG, Elvers KT, Dopfer D, Hansson I, Jones P, James S, Gittins J, Stern NJ, Davies R, Connerton I, Pearson D, Salvat G, Allen VM: Biosecurity-based interventions and strategies to reduce Campylobacter spp. on poultry farms. Appl Environ Microbiol. 2011, 77: 8605-8614. 10.1128/AEM.01090-10.PubMedCentralCrossRefPubMed Newell DG, Elvers KT, Dopfer D, Hansson I, Jones P, James S, Gittins J, Stern NJ, Davies R, Connerton I, Pearson D, Salvat G, Allen VM: Biosecurity-based interventions and strategies to reduce Campylobacter spp. on poultry farms. Appl Environ Microbiol. 2011, 77: 8605-8614. 10.1128/AEM.01090-10.PubMedCentralCrossRefPubMed
4.
go back to reference Lynch OA, Cagney C, McDowell DA, Duffy G: Occurrence of fastidious Campylobacter spp. in fresh meat and poultry using an adapted cultural protocol. Int J Food Microbiol. 2011, 150: 171-177. 10.1016/j.ijfoodmicro.2011.07.037.CrossRefPubMed Lynch OA, Cagney C, McDowell DA, Duffy G: Occurrence of fastidious Campylobacter spp. in fresh meat and poultry using an adapted cultural protocol. Int J Food Microbiol. 2011, 150: 171-177. 10.1016/j.ijfoodmicro.2011.07.037.CrossRefPubMed
5.
go back to reference Manfreda G, Parisi A, Lucchi A, Zanoni RG, De Cesare A: Prevalence of Helicobacter pullorum in conventional, organic, and free-range broilers and typing of isolates. Appl Environ Microbiol. 2011, 77: 479-484. 10.1128/AEM.01712-10.PubMedCentralCrossRefPubMed Manfreda G, Parisi A, Lucchi A, Zanoni RG, De Cesare A: Prevalence of Helicobacter pullorum in conventional, organic, and free-range broilers and typing of isolates. Appl Environ Microbiol. 2011, 77: 479-484. 10.1128/AEM.01712-10.PubMedCentralCrossRefPubMed
6.
go back to reference Batz MB, Hoffmann S, Morris JG: Ranking the disease burden of 14 pathogens in food sources in the United States using attribution data from outbreak investigations and expert elicitation. J Food Prot. 2012, 75: 1278-1291. 10.4315/0362-028X.JFP-11-418.CrossRefPubMed Batz MB, Hoffmann S, Morris JG: Ranking the disease burden of 14 pathogens in food sources in the United States using attribution data from outbreak investigations and expert elicitation. J Food Prot. 2012, 75: 1278-1291. 10.4315/0362-028X.JFP-11-418.CrossRefPubMed
7.
go back to reference Wagenaar JA, French NP, Havelaar AH: Preventing Campylobacter at the source: why is it so difficult?. Clin Infect Dis. 2013, 57: 1600-1606. 10.1093/cid/cit555.CrossRefPubMed Wagenaar JA, French NP, Havelaar AH: Preventing Campylobacter at the source: why is it so difficult?. Clin Infect Dis. 2013, 57: 1600-1606. 10.1093/cid/cit555.CrossRefPubMed
8.
go back to reference Havelaar AH, van Pelt W, Ang CW, Wagenaar JA, van Putten JP, Gross U, Newell DG: Immunity to Campylobacter: its role in risk assessment and epidemiology. Crit Rev Microbiol. 2009, 35: 1-22. 10.1080/10408410802636017.CrossRefPubMed Havelaar AH, van Pelt W, Ang CW, Wagenaar JA, van Putten JP, Gross U, Newell DG: Immunity to Campylobacter: its role in risk assessment and epidemiology. Crit Rev Microbiol. 2009, 35: 1-22. 10.1080/10408410802636017.CrossRefPubMed
9.
go back to reference Cox JM, Pavic A: Advances in enteropathogen control in poultry production. J Appl Microbiol. 2010, 108: 745-755. 10.1111/j.1365-2672.2009.04456.x.CrossRefPubMed Cox JM, Pavic A: Advances in enteropathogen control in poultry production. J Appl Microbiol. 2010, 108: 745-755. 10.1111/j.1365-2672.2009.04456.x.CrossRefPubMed
10.
go back to reference Annamalai T, Pina-Mimbela R, Kumar A, Binjawadagi B, Liu Z, Renukaradhya GJ, Rajashekara G: Evaluation of nanoparticle-encapsulated outer membrane proteins for the control of Campylobacter jejuni colonization in chickens. Poult Sci. 2013, 92: 2201-2211. 10.3382/ps.2012-03004.CrossRefPubMed Annamalai T, Pina-Mimbela R, Kumar A, Binjawadagi B, Liu Z, Renukaradhya GJ, Rajashekara G: Evaluation of nanoparticle-encapsulated outer membrane proteins for the control of Campylobacter jejuni colonization in chickens. Poult Sci. 2013, 92: 2201-2211. 10.3382/ps.2012-03004.CrossRefPubMed
11.
go back to reference Ghareeb K, Awad WA, Mohnl M, Porta R, Biarnes M, Bohm J, Schatzmayr G: Evaluating the efficacy of an avian-specific probiotic to reduce the colonization of Campylobacter jejuni in broiler chickens. Poult Sci. 2012, 91: 1825-1832. 10.3382/ps.2012-02168.CrossRefPubMed Ghareeb K, Awad WA, Mohnl M, Porta R, Biarnes M, Bohm J, Schatzmayr G: Evaluating the efficacy of an avian-specific probiotic to reduce the colonization of Campylobacter jejuni in broiler chickens. Poult Sci. 2012, 91: 1825-1832. 10.3382/ps.2012-02168.CrossRefPubMed
12.
go back to reference Lammerding AM, Fazil A: Hazard identification and exposure assessment for microbial food safety risk assessment. Int J Food Microbiol. 2000, 58: 147-157. 10.1016/S0168-1605(00)00269-5.CrossRefPubMed Lammerding AM, Fazil A: Hazard identification and exposure assessment for microbial food safety risk assessment. Int J Food Microbiol. 2000, 58: 147-157. 10.1016/S0168-1605(00)00269-5.CrossRefPubMed
13.
go back to reference Rosenquist H, Nielsen NL, Sommer HM, Norrung B, Christensen BB: Quantitative risk assessment of human campylobacteriosis associated with thermophilic Campylobacter species in chickens. Int J Food Microbiol. 2003, 83: 87-103. 10.1016/S0168-1605(02)00317-3.CrossRefPubMed Rosenquist H, Nielsen NL, Sommer HM, Norrung B, Christensen BB: Quantitative risk assessment of human campylobacteriosis associated with thermophilic Campylobacter species in chickens. Int J Food Microbiol. 2003, 83: 87-103. 10.1016/S0168-1605(02)00317-3.CrossRefPubMed
14.
go back to reference Kerr AK, Farrar AM, Waddell LA, Wilkins W, Wilhelm BJ, Bucher O, Wills RW, Bailey RH, Varga C, McEwen SA, Rajic A: A systematic review-meta-analysis and meta-regression on the effect of selected competitive exclusion products on Salmonella spp. prevalence and concentration in broiler chickens. Prev Vet Med. 2013, 111: 112-125. 10.1016/j.prevetmed.2013.04.005.CrossRefPubMed Kerr AK, Farrar AM, Waddell LA, Wilkins W, Wilhelm BJ, Bucher O, Wills RW, Bailey RH, Varga C, McEwen SA, Rajic A: A systematic review-meta-analysis and meta-regression on the effect of selected competitive exclusion products on Salmonella spp. prevalence and concentration in broiler chickens. Prev Vet Med. 2013, 111: 112-125. 10.1016/j.prevetmed.2013.04.005.CrossRefPubMed
15.
go back to reference Nuotio L, Schneitz C, Nilsson O: Effect of competitive exclusion in reducing the occurrence of Escherichia coli producing extended-spectrum beta-lactamases in the ceca of broiler chicks. Poult Sci. 2013, 92: 250-254. 10.3382/ps.2012-02575.CrossRefPubMed Nuotio L, Schneitz C, Nilsson O: Effect of competitive exclusion in reducing the occurrence of Escherichia coli producing extended-spectrum beta-lactamases in the ceca of broiler chicks. Poult Sci. 2013, 92: 250-254. 10.3382/ps.2012-02575.CrossRefPubMed
17.
go back to reference Neal-McKinney JM, Lu X, Duong T, Larson CL, Call DR, Shah DH, Konkel ME: Production of organic acids by probiotic lactobacilli can be used to reduce pathogen load in poultry. PLoS One. 2012, 7: e43928-10.1371/journal.pone.0043928.PubMedCentralCrossRefPubMed Neal-McKinney JM, Lu X, Duong T, Larson CL, Call DR, Shah DH, Konkel ME: Production of organic acids by probiotic lactobacilli can be used to reduce pathogen load in poultry. PLoS One. 2012, 7: e43928-10.1371/journal.pone.0043928.PubMedCentralCrossRefPubMed
18.
go back to reference Zhang G, Ma L, Doyle MP: Potential competitive exclusion bacteria from poultry inhibitory to Campylobacter jejuni and Salmonella. J Food Prot. 2007, 70: 867-873.PubMed Zhang G, Ma L, Doyle MP: Potential competitive exclusion bacteria from poultry inhibitory to Campylobacter jejuni and Salmonella. J Food Prot. 2007, 70: 867-873.PubMed
19.
go back to reference Yeoman CJ, Chia N, Jeraldo P, Sipos M, Goldenfeld ND, White BA: The microbiome of the chicken gastrointestinal tract. Anim Health Res Rev. 2012, 13: 89-99. 10.1017/S1466252312000138.CrossRefPubMed Yeoman CJ, Chia N, Jeraldo P, Sipos M, Goldenfeld ND, White BA: The microbiome of the chicken gastrointestinal tract. Anim Health Res Rev. 2012, 13: 89-99. 10.1017/S1466252312000138.CrossRefPubMed
20.
go back to reference Torok VA, Allison GE, Percy NJ, Ophel-Keller K, Hughes RJ: Influence of antimicrobial feed additives on broiler commensal posthatch gut microbiota development and performance. Appl Environ Microbiol. 2011, 77: 3380-3390. 10.1128/AEM.02300-10.PubMedCentralCrossRefPubMed Torok VA, Allison GE, Percy NJ, Ophel-Keller K, Hughes RJ: Influence of antimicrobial feed additives on broiler commensal posthatch gut microbiota development and performance. Appl Environ Microbiol. 2011, 77: 3380-3390. 10.1128/AEM.02300-10.PubMedCentralCrossRefPubMed
21.
go back to reference Danzeisen JL, Kim HB, Isaacson RE, Tu ZJ, Johnson TJ: Modulations of the chicken cecal microbiome and metagenome in response to anticoccidial and growth promoter treatment. PLoS One. 2011, 6: e27949-10.1371/journal.pone.0027949.PubMedCentralCrossRefPubMed Danzeisen JL, Kim HB, Isaacson RE, Tu ZJ, Johnson TJ: Modulations of the chicken cecal microbiome and metagenome in response to anticoccidial and growth promoter treatment. PLoS One. 2011, 6: e27949-10.1371/journal.pone.0027949.PubMedCentralCrossRefPubMed
22.
go back to reference Qu A, Brulc JM, Wilson MK, Law BF, Theoret JR, Joens LA, Konkel ME, Angly F, Dinsdale EA, Edwards RA, Nelson KE, White BA: Comparative metagenomics reveals host specific metavirulomes and horizontal gene transfer elements in the chicken cecum microbiome. PLoS One. 2008, 3: e2945-10.1371/journal.pone.0002945.PubMedCentralCrossRefPubMed Qu A, Brulc JM, Wilson MK, Law BF, Theoret JR, Joens LA, Konkel ME, Angly F, Dinsdale EA, Edwards RA, Nelson KE, White BA: Comparative metagenomics reveals host specific metavirulomes and horizontal gene transfer elements in the chicken cecum microbiome. PLoS One. 2008, 3: e2945-10.1371/journal.pone.0002945.PubMedCentralCrossRefPubMed
23.
go back to reference Rehman HU, Vahjen W, Awad WA, Zentek J: Indigenous bacteria and bacterial metabolic products in the gastrointestinal tract of broiler chickens. Arch Anim Nutr. 2007, 61: 319-335. 10.1080/17450390701556817.CrossRefPubMed Rehman HU, Vahjen W, Awad WA, Zentek J: Indigenous bacteria and bacterial metabolic products in the gastrointestinal tract of broiler chickens. Arch Anim Nutr. 2007, 61: 319-335. 10.1080/17450390701556817.CrossRefPubMed
24.
go back to reference Stanley D, Geier MS, Hughes RJ, Denman SE, Moore RJ: Highly variable microbiota development in the chicken gastrointestinal tract. PLoS One. 2013, 8: e84290-10.1371/journal.pone.0084290.PubMedCentralCrossRefPubMed Stanley D, Geier MS, Hughes RJ, Denman SE, Moore RJ: Highly variable microbiota development in the chicken gastrointestinal tract. PLoS One. 2013, 8: e84290-10.1371/journal.pone.0084290.PubMedCentralCrossRefPubMed
25.
go back to reference Lee JE, Lee S, Sung J, Ko G: Analysis of human and animal fecal microbiota for microbial source tracking. ISME J. 2011, 5: 362-365. 10.1038/ismej.2010.120.PubMedCentralCrossRefPubMed Lee JE, Lee S, Sung J, Ko G: Analysis of human and animal fecal microbiota for microbial source tracking. ISME J. 2011, 5: 362-365. 10.1038/ismej.2010.120.PubMedCentralCrossRefPubMed
26.
go back to reference Lei F, Yin Y, Wang Y, Deng B, Yu HD, Li L, Xiang C, Wang S, Zhu B, Wang X: Higher-level production of volatile fatty acids in vitro by chicken gut microbiotas than by human gut microbiotas as determined by functional analyses. Appl Environ Microbiol. 2012, 78: 5763-5772. 10.1128/AEM.00327-12.PubMedCentralCrossRefPubMed Lei F, Yin Y, Wang Y, Deng B, Yu HD, Li L, Xiang C, Wang S, Zhu B, Wang X: Higher-level production of volatile fatty acids in vitro by chicken gut microbiotas than by human gut microbiotas as determined by functional analyses. Appl Environ Microbiol. 2012, 78: 5763-5772. 10.1128/AEM.00327-12.PubMedCentralCrossRefPubMed
27.
go back to reference Kaakoush NO, Day AS, Huinao KD, Leach ST, Lemberg DA, Dowd SE, Mitchell HM: Microbial dysbiosis in pediatric patients with Crohn’s disease. J Clin Microbiol. 2012, 50: 3258-3266. 10.1128/JCM.01396-12.PubMedCentralCrossRefPubMed Kaakoush NO, Day AS, Huinao KD, Leach ST, Lemberg DA, Dowd SE, Mitchell HM: Microbial dysbiosis in pediatric patients with Crohn’s disease. J Clin Microbiol. 2012, 50: 3258-3266. 10.1128/JCM.01396-12.PubMedCentralCrossRefPubMed
28.
go back to reference Walker AW, Duncan SH, Louis P, Flint HJ: Phylogeny, culturing, and metagenomics of the human gut microbiota. Trends Microbiol. 2014, 22: 267-274. 10.1016/j.tim.2014.03.001.CrossRefPubMed Walker AW, Duncan SH, Louis P, Flint HJ: Phylogeny, culturing, and metagenomics of the human gut microbiota. Trends Microbiol. 2014, 22: 267-274. 10.1016/j.tim.2014.03.001.CrossRefPubMed
29.
go back to reference Parker CT, Miller WG, Horn ST, Lastovica AJ: Common genomic features of Campylobacter jejuni subsp. doylei strains distinguish them from C. jejuni subsp. jejuni. BMC Microbiol. 2007, 7: 50-10.1186/1471-2180-7-50.PubMedCentralCrossRefPubMed Parker CT, Miller WG, Horn ST, Lastovica AJ: Common genomic features of Campylobacter jejuni subsp. doylei strains distinguish them from C. jejuni subsp. jejuni. BMC Microbiol. 2007, 7: 50-10.1186/1471-2180-7-50.PubMedCentralCrossRefPubMed
30.
go back to reference Fox JG, Taylor NS, Howe S, Tidd M, Xu S, Paster BJ, Dewhirst FE: Helicobacter anseris sp. nov. and Helicobacter brantae sp. nov., isolated from feces of resident Canada geese in the greater Boston area. Appl Environ Microbiol. 2006, 72: 4633-4637. 10.1128/AEM.02876-05.PubMedCentralCrossRefPubMed Fox JG, Taylor NS, Howe S, Tidd M, Xu S, Paster BJ, Dewhirst FE: Helicobacter anseris sp. nov. and Helicobacter brantae sp. nov., isolated from feces of resident Canada geese in the greater Boston area. Appl Environ Microbiol. 2006, 72: 4633-4637. 10.1128/AEM.02876-05.PubMedCentralCrossRefPubMed
32.
go back to reference Man SM: The clinical importance of emerging Campylobacter species. Nat Rev Gastroenterol Hepatol. 2011, 8: 669-685. 10.1038/nrgastro.2011.191.CrossRefPubMed Man SM: The clinical importance of emerging Campylobacter species. Nat Rev Gastroenterol Hepatol. 2011, 8: 669-685. 10.1038/nrgastro.2011.191.CrossRefPubMed
33.
go back to reference Bereswill S, Plickert R, Fischer A, Kuhl AA, Loddenkemper C, Batra A, Siegmund B, Gobel UB, Heimesaat MM: What you eat is what you get: Novel Campylobacter models in the quadrangle relationship between nutrition, obesity, microbiota and susceptibility to infection. Eur J Microbiol Immunol. 2011, 1: 237-248. 10.1556/EuJMI.1.2011.3.8.CrossRef Bereswill S, Plickert R, Fischer A, Kuhl AA, Loddenkemper C, Batra A, Siegmund B, Gobel UB, Heimesaat MM: What you eat is what you get: Novel Campylobacter models in the quadrangle relationship between nutrition, obesity, microbiota and susceptibility to infection. Eur J Microbiol Immunol. 2011, 1: 237-248. 10.1556/EuJMI.1.2011.3.8.CrossRef
34.
go back to reference Masanta WO, Heimesaat MM, Bereswill S, Tareen AM, Lugert R, Gross U, Zautner AE: Modification of intestinal microbiota and its consequences for innate immune response in the pathogenesis of campylobacteriosis. Clin Dev Immunol. 2013, 2013: 526860-PubMedCentralCrossRefPubMed Masanta WO, Heimesaat MM, Bereswill S, Tareen AM, Lugert R, Gross U, Zautner AE: Modification of intestinal microbiota and its consequences for innate immune response in the pathogenesis of campylobacteriosis. Clin Dev Immunol. 2013, 2013: 526860-PubMedCentralCrossRefPubMed
35.
go back to reference Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, Mende DR, Fernandes GR, Tap J, Bruls T, Batto JM, Bertalan M, Borruel N, Casellas F, Fernandez L, Gautier L, Hansen T, Hattori M, Hayashi T, Kleerebezem M, Kurokawa K, Leclerc M, Levenez F, Manichanh C, Nielsen HB, Nielsen T, Pons N, Poulain J, Qin J, Sicheritz-Ponten T, Tims S: Enterotypes of the human gut microbiome. Nature. 2011, 473: 174-180. 10.1038/nature09944.PubMedCentralCrossRefPubMed Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, Mende DR, Fernandes GR, Tap J, Bruls T, Batto JM, Bertalan M, Borruel N, Casellas F, Fernandez L, Gautier L, Hansen T, Hattori M, Hayashi T, Kleerebezem M, Kurokawa K, Leclerc M, Levenez F, Manichanh C, Nielsen HB, Nielsen T, Pons N, Poulain J, Qin J, Sicheritz-Ponten T, Tims S: Enterotypes of the human gut microbiome. Nature. 2011, 473: 174-180. 10.1038/nature09944.PubMedCentralCrossRefPubMed
36.
go back to reference Sekelja M, Rud I, Knutsen SH, Denstadli V, Westereng B, Næs T, Rudi K: Abrupt temporal fluctuations in the chicken fecal microbiota are explained by its gastrointestinal origin. Appl Environ Microbiol. 2012, 78: 2941-2948. 10.1128/AEM.05391-11.PubMedCentralCrossRefPubMed Sekelja M, Rud I, Knutsen SH, Denstadli V, Westereng B, Næs T, Rudi K: Abrupt temporal fluctuations in the chicken fecal microbiota are explained by its gastrointestinal origin. Appl Environ Microbiol. 2012, 78: 2941-2948. 10.1128/AEM.05391-11.PubMedCentralCrossRefPubMed
37.
go back to reference Griffiths RI, Whiteley AS, O’Donnell AG, Bailey MJ: Rapid method for coextraction of DNA and RNA from natural environments for analysis of ribosomal DNA- and rRNA-based microbial community composition. Appl Environ Microbiol. 2000, 66: 5488-5491. 10.1128/AEM.66.12.5488-5491.2000.PubMedCentralCrossRefPubMed Griffiths RI, Whiteley AS, O’Donnell AG, Bailey MJ: Rapid method for coextraction of DNA and RNA from natural environments for analysis of ribosomal DNA- and rRNA-based microbial community composition. Appl Environ Microbiol. 2000, 66: 5488-5491. 10.1128/AEM.66.12.5488-5491.2000.PubMedCentralCrossRefPubMed
38.
go back to reference Andreotti R, de Leon AA P, Dowd SE, Guerrero FD, Bendele KG, Scoles GA: Assessment of bacterial diversity in the cattle tick Rhipicephalus (Boophilus) microplus through tag-encoded pyrosequencing. BMC Microbiol. 2011, 11: 6-10.1186/1471-2180-11-6.PubMedCentralCrossRefPubMed Andreotti R, de Leon AA P, Dowd SE, Guerrero FD, Bendele KG, Scoles GA: Assessment of bacterial diversity in the cattle tick Rhipicephalus (Boophilus) microplus through tag-encoded pyrosequencing. BMC Microbiol. 2011, 11: 6-10.1186/1471-2180-11-6.PubMedCentralCrossRefPubMed
39.
go back to reference Bailey MT, Dowd SE, Parry NM, Galley JD, Schauer DB, Lyte M: Stressor exposure disrupts commensal microbial populations in the intestines and leads to increased colonization by Citrobacter rodentium. Infect Immun. 2010, 78: 1509-1519. 10.1128/IAI.00862-09.PubMedCentralCrossRefPubMed Bailey MT, Dowd SE, Parry NM, Galley JD, Schauer DB, Lyte M: Stressor exposure disrupts commensal microbial populations in the intestines and leads to increased colonization by Citrobacter rodentium. Infect Immun. 2010, 78: 1509-1519. 10.1128/IAI.00862-09.PubMedCentralCrossRefPubMed
40.
go back to reference Dowd SE, Callaway TR, Wolcott RD, Sun Y, McKeehan T, Hagevoort RG, Edrington TS: Evaluation of the bacterial diversity in the feces of cattle using 16S rDNA bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP). BMC Microbiol. 2008, 8: 125-10.1186/1471-2180-8-125.PubMedCentralCrossRefPubMed Dowd SE, Callaway TR, Wolcott RD, Sun Y, McKeehan T, Hagevoort RG, Edrington TS: Evaluation of the bacterial diversity in the feces of cattle using 16S rDNA bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP). BMC Microbiol. 2008, 8: 125-10.1186/1471-2180-8-125.PubMedCentralCrossRefPubMed
41.
go back to reference Dowd SE, Delton Hanson J, Rees E, Wolcott RD, Zischau AM, Sun Y, White J, Smith DM, Kennedy J, Jones CE: Survey of fungi and yeast in polymicrobial infections in chronic wounds. J Wound Care. 2011, 20: 40-47. 10.12968/jowc.2011.20.1.40.CrossRefPubMed Dowd SE, Delton Hanson J, Rees E, Wolcott RD, Zischau AM, Sun Y, White J, Smith DM, Kennedy J, Jones CE: Survey of fungi and yeast in polymicrobial infections in chronic wounds. J Wound Care. 2011, 20: 40-47. 10.12968/jowc.2011.20.1.40.CrossRefPubMed
42.
go back to reference Dowd SE, Sun Y, Wolcott RD, Domingo A, Carroll JA: Bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP) for microbiome studies: bacterial diversity in the ileum of newly weaned Salmonella-infected pigs. Foodborne Pathog Dis. 2008, 5: 459-472. 10.1089/fpd.2008.0107.CrossRefPubMed Dowd SE, Sun Y, Wolcott RD, Domingo A, Carroll JA: Bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP) for microbiome studies: bacterial diversity in the ileum of newly weaned Salmonella-infected pigs. Foodborne Pathog Dis. 2008, 5: 459-472. 10.1089/fpd.2008.0107.CrossRefPubMed
43.
go back to reference Gontcharova V, Youn E, Wolcott RD, Hollister EB, Gentry TJ, Dowd SE: Black Box Chimera Check (B2C2): a Windows-Based Software for Batch Depletion of Chimeras from Bacterial 16S rRNA Gene Datasets. Open Microbiol J. 2010, 4: 47-52. 10.2174/1874285801004010047.PubMedCentralCrossRefPubMed Gontcharova V, Youn E, Wolcott RD, Hollister EB, Gentry TJ, Dowd SE: Black Box Chimera Check (B2C2): a Windows-Based Software for Batch Depletion of Chimeras from Bacterial 16S rRNA Gene Datasets. Open Microbiol J. 2010, 4: 47-52. 10.2174/1874285801004010047.PubMedCentralCrossRefPubMed
44.
go back to reference DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL: Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol. 2006, 72: 5069-5072. 10.1128/AEM.03006-05.PubMedCentralCrossRefPubMed DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL: Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol. 2006, 72: 5069-5072. 10.1128/AEM.03006-05.PubMedCentralCrossRefPubMed
45.
go back to reference Clarke KR: Non-parametric multivariate analyses of changes in community structure. Austr J Ecol. 1993, 18: 117-143. 10.1111/j.1442-9993.1993.tb00438.x.CrossRef Clarke KR: Non-parametric multivariate analyses of changes in community structure. Austr J Ecol. 1993, 18: 117-143. 10.1111/j.1442-9993.1993.tb00438.x.CrossRef
46.
go back to reference Linton D, Owen RJ, Stanley J: Rapid identification by PCR of the genus Campylobacter and of five Campylobacter species enteropathogenic for man and animals. Res Microbiol. 1996, 147: 707-718. 10.1016/S0923-2508(97)85118-2.CrossRefPubMed Linton D, Owen RJ, Stanley J: Rapid identification by PCR of the genus Campylobacter and of five Campylobacter species enteropathogenic for man and animals. Res Microbiol. 1996, 147: 707-718. 10.1016/S0923-2508(97)85118-2.CrossRefPubMed
47.
go back to reference Man SM, Zhang L, Day AS, Leach ST, Lemberg DA, Mitchell H: Campylobacter concisus and other Campylobacter species in children with newly diagnosed Crohn’s disease. Inflamm Bowel Dis. 2010, 16: 1008-1016. 10.1002/ibd.21157.CrossRefPubMed Man SM, Zhang L, Day AS, Leach ST, Lemberg DA, Mitchell H: Campylobacter concisus and other Campylobacter species in children with newly diagnosed Crohn’s disease. Inflamm Bowel Dis. 2010, 16: 1008-1016. 10.1002/ibd.21157.CrossRefPubMed
48.
go back to reference Stanley J, Linton D, Burnens AP, Dewhirst FE, On SL, Porter A, Owen RJ, Costas M: Helicobacter pullorum sp. nov.-genotype and phenotype of a new species isolated from poultry and from human patients with gastroenteritis. Microbiology. 1994, 140: 3441-3449. 10.1099/13500872-140-12-3441.CrossRefPubMed Stanley J, Linton D, Burnens AP, Dewhirst FE, On SL, Porter A, Owen RJ, Costas M: Helicobacter pullorum sp. nov.-genotype and phenotype of a new species isolated from poultry and from human patients with gastroenteritis. Microbiology. 1994, 140: 3441-3449. 10.1099/13500872-140-12-3441.CrossRefPubMed
Metadata
Title
The interplay between Campylobacter and Helicobacter species and other gastrointestinal microbiota of commercial broiler chickens
Authors
Nadeem O Kaakoush
Nidhi Sodhi
Jeremy W Chenu
Julian M Cox
Stephen M Riordan
Hazel M Mitchell
Publication date
01-12-2014
Publisher
BioMed Central
Published in
Gut Pathogens / Issue 1/2014
Electronic ISSN: 1757-4749
DOI
https://doi.org/10.1186/1757-4749-6-18

Other articles of this Issue 1/2014

Gut Pathogens 1/2014 Go to the issue