Gut microbiota composition before infection determines the Salmonella super- and low-shedder phenotypes in chicken

. 2020 Sep ; 13 (5) : 1611-1630. [epub] 20200708

Jazyk angličtina Země Spojené státy americké Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid32639676

Heterogeneity of infection and extreme shedding patterns are common features of animal infectious diseases. Individual hosts that are super-shedders are key targets for control strategies. Nevertheless, the mechanisms associated with the emergence of super-shedders remain largely unknown. During chicken salmonellosis, a high heterogeneity of infection is observed when animal-to-animal cross-contaminations and reinfections are reduced. We hypothesized that unlike super-shedders, low-shedders would be able to block the first Salmonella colonization thanks to a different gut microbiota. The present study demonstrates that (i) axenic and antibiotic-treated chicks are more prone to become super-shedders; (ii) super or low-shedder phenotypes can be acquired through microbiota transfer; (iii) specific gut microbiota taxonomic features determine whether the chicks develop a low- and super-shedder phenotype after Salmonella infection in isolator; (iv) partial protection can be conferred by inoculation of four commensal bacteria prior to Salmonella infection. This study demonstrates the key role plays by gut microbiota composition in the heterogeneity of infection and pave the way for developing predictive biomarkers and protective probiotics.

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Bearson, S.M. , Allen, H.K. , Bearson, B.L. , Looft, T. , Brunelle, B.W. , Kich, J.D. , et al (2013) Profiling the gastrointestinal microbiota in response to Salmonella: low versus high Salmonella shedding in the natural porcine host. Infect Genet Evol 16: 330–340. PubMed

Bogomolnaya, L.M. , Santiviago, C.A. , Yang, H.J. , Baumler, A.J. , and Andrews‐Polymenis, H.L. (2008) 'Form variation' of the O12 antigen is critical for persistence of Salmonella Typhimurium in the murine intestine. Mol Microbiol 70: 1105–1119. PubMed

Bolger, A.M. , Lohse, M. , and Usadel, B. (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30: 2114–2120. PubMed PMC

Boudeau, J. , Glasser, A.L. , Julien, S. , Colombel, J.F. , and Darfeuille‐Michaud, A. (2003) Inhibitory effect of probiotic Escherichia coli strain Nissle 1917 on adhesion to and invasion of intestinal epithelial cells by adherent‐invasive E. coli strains isolated from patients with Crohn's disease. Aliment Pharmacol Ther 18: 45–56. PubMed

Brugiroux, S. , Beutler, M. , Pfann, C. , Garzetti, D. , Ruscheweyh, H.J. , Ring, D. , et al (2016) Genome‐guided design of a defined mouse microbiota that confers colonization resistance against Salmonella enterica serovar Typhimurium. Nat Microbiol 2: 16215. PubMed

Calenge, F. , Kaiser, P. , Vignal, A. , and Beaumont, C. (2010) Genetic control of resistance to salmonellosis and to Salmonella carrier‐state in fowl: a review. Genet Sel Evol 42: 11. PubMed PMC

Callaway, T.R. , Anderson, R.C. , Edrington, T.S. , Genovese, K.J. , Harvey, R.B. , Poole, T.L. , and Nisbet, D.J. (2004) Recent pre‐harvest supplementation strategies to reduce carriage and shedding of zoonotic enteric bacterial pathogens in food animals. Anim Health Res Rev 5: 35–47. PubMed

Camacho, C. , Coulouris, G. , Avagyan, V. , Ma, N. , Papadopoulos, J. , Bealer, K. , and Madden, T.L. (2009) BLAST+: architecture and applications. BMC Bioinformatics 10: 421. PubMed PMC

Caporaso, J.G. , Kuczynski, J. , Stombaugh, J. , Bittinger, K. , Bushman, F.D. , Costello, E.K. , et al (2010) QIIME allows analysis of high‐throughput community sequencing data. Nat Methods 7: 335–336. PubMed PMC

Carina Audisio, M. , Oliver, G. , and Apella, M.C. (2000) Protective effect of Enterococcus faecium J96, a potential probiotic strain, on chicks infected with Salmonella Pullorum. J Food Prot 63: 1333–1337. PubMed

Carter, A. , Adams, M. , La Ragione, R.M. , and Woodward, M.J. (2017) Colonisation of poultry by Salmonella Enteritidis S1400 is reduced by combined administration of Lactobacillus salivarius 59 and Enterococcus faecium PXN‐33. Vet Microbiol 199: 100–107. PubMed

Chaussé, A.M. , Grépinet, O. , Bottreau, E. , Le Vern, Y. , Menanteau, P. , Trotereau, J. , et al (2011) Expression of Toll‐like receptor 4 and downstream effectors in selected cecal cell subpopulations of chicks resistant or susceptible to Salmonella carrier state. Infect Immun 79: 3445–3454. PubMed PMC

Deasy, B.M. , Rea, M.C. , Fitzgerald, G.F. , Cogan, T.M. , and Beresford, T.P. (2000) A rapid PCR based method to distinguish between Lactococcus and Enterococcus . Syst Appl Microbiol 23: 510–522. PubMed

Dibb‐Fuller, M.P. , Allen‐Vercoe, E. , Thorns, C.J. , and Woodward, M.J. (1999) Fimbriae‐ and flagella‐mediated association with and invasion of cultured epithelial cells by Salmonella enteritidis . Microbiol 145(Pt 5): 1023–1031. PubMed

Donaldson, G.P. , Lee, S.M. , and Mazmanian, S.K. (2016) Gut biogeography of the bacterial microbiota. Nat Rev Microbiol 14: 20–32. PubMed PMC

Duchet‐Suchaux, M. , Lechopier, P. , Marly, J. , Bernardet, P. , Delaunay, R. , and Pardon, P. (1995) Quantification of experimental Salmonella enteritidis carrier state in B13 leghorn chicks. Avian Dis 39: 796–802. PubMed

EFSA (2018) The European Union summary report on trends and sources of zoonoses, zoonotic agents and food‐borne outbreaks in 2017. EFSA Journal 16: e05500. PubMed PMC

El Aidy, S. , Van den Abbeele, P. , Van de Wiele, T. , Louis, P. , and Kleerebezem, M. (2013) Intestinal colonization: how key microbial players become established in this dynamic process: microbial metabolic activities and the interplay between the host and microbes. BioEssays 35: 913–923. PubMed

Escudie, F. , Auer, L. , Bernard, M. , Mariadassou, M. , Cauquil, L. , Vidal, K. , et al (2018) FROGS: find, rapidly, OTUs with galaxy solution. Bioinformatics 34: 1287–1294. PubMed

Gopinath, S. , Carden, S. , and Monack, D. (2012) Shedding light on Salmonella carriers. Trends Microbiol 20: 320–327. PubMed

Grépinet, O. , Rossignol, A. , Loux, V. , Chiapello, H. , Gendrault, A. , Gibrat, J.F. , et al (2012) Genome Sequence of the Invasive Salmonella enterica subsp. enterica Serotype Enteritidis Strain LA5. J Bacteriol 194: 2387–2388. PubMed PMC

Haiser, H.J. , and Turnbaugh, P.J. (2012) Is it time for a metagenomic basis of therapeutics? Science 336: 1253–1255. PubMed

Hanchi, H. , Mottawea, W. , Sebei, K. , and Hammami, R. (2018) The genus Enterococcus: between probiotic potential and safety concerns—an update. Front Microbiol 9: 1791. PubMed PMC

Iqbal, M. , Philbin, V.J. , Withanage, G.S. , Wigley, P. , Beal, R.K. , Goodchild, M.J. , et al (2005) Identification and functional characterization of chicken toll‐like receptor 5 reveals a fundamental role in the biology of infection with Salmonella enterica serovar Typhimurium. Infect Immun 73: 2344–2350. PubMed PMC

Jackson, C.R. , Fedorka‐Cray, P.J. , and Barrett, J.B. (2004) Use of a genus‐ and species‐specific multiplex PCR for identification of enterococci. J Clin Microbiol 42: 3558–3565. PubMed PMC

Kubasova, T. , Kollarcikova, M. , Crhanova, M. , Karasova, D. , Cejkova, D. , Sebkova, A. , et al (2019) Contact with adult hen affects development of caecal microbiota in newly hatched chicks. PLoS One 14: e0212446. PubMed PMC

Kumar, S. , Stecher, G. , and Tamura, K. (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33: 1870–1874. PubMed PMC

Lawley, T.D. , Bouley, D.M. , Hoy, Y.E. , Gerke, C. , Relman, D.A. , and Monack, D.M. (2008) Host transmission of Salmonella enterica serovar Typhimurium is controlled by virulence factors and indigenous intestinal microbiota. Infect Immun 76: 403–416. PubMed PMC

Lê, S. , Josse, J. , and Husson, F. (2008) FactoMineR: an R package for multivariate analysis. J Stat Softw 25: 1–18.

Lemon, K.P. , Armitage, G.C. , Relman, D.A. , and Fischbach, M.A. (2012) Microbiota‐targeted therapies: an ecological perspective. Sci Transl Med 4: 137rv135. PubMed PMC

Levine, U.Y. , Bearson, S.M. , and Stanton, T.B. (2012) Mitsuokella jalaludinii inhibits growth of Salmonella enterica serovar Typhimurium. Vet Microbiol 159: 115–122. PubMed

Litvak, Y. , Mon, K.K.Z. , Nguyen, H. , Chanthavixay, G. , Liou, M. , Velazquez, E.M. , et al (2019) Commensal Enterobacteriaceae protect against Salmonella colonization through oxygen competition. Cell Host Microbe 25: 128–139.e5. PubMed

Love, M.I. , Huber, W. , and Anders, S. (2014) Moderated estimation of fold change and dispersion for RNA‐seq data with DESeq2. Genome Biol 15: 550. PubMed PMC

Mahé, F. , Rognes, T. , Quince, C. , de Vargas, C. , and Dunthorn, M. (2014) Swarm: robust and fast clustering method for amplicon‐based studies. PeerJ 2: e593. PubMed PMC

Marshall, J. , and French, N. (2011) Modelling of Campylobacter Carriage and Transmission between and Within Animal Groups. Ministry of Agriculture and Forestry.

Matthews, L. , Low, J.C. , Gally, D.L. , Pearce, M.C. , Mellor, D.J. , Heesterbeek, J.A. , et al (2006) Heterogeneous shedding of Escherichia coli O157 in cattle and its implications for control. Proc Natl Acad Sci USA 103: 547–552. PubMed PMC

McMurdie, P.J. , and Holmes, S. (2013) phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8: e61217. PubMed PMC

Mead, G.C. (1989) Microbes of the avian cecum: types present and substrates utilized. J Exp Zool Suppl 3: 48–54. PubMed

Mead, G.C. , and Adams, B.W. (1975) Some observations on the caecal microflora of the chick during the first two weeks of life. Br Poult Sci 16: 169–176. PubMed

Menanteau, P. , Kempf, F. , Trotereau, J. , Virlogeux‐Payant, I. , Gitton, E. , Dalifard, J. , et al (2018) Role of systemic infection, cross contaminations and super‐shedders in Salmonella carrier state in chicken. Environ Microbiol 20: 3246–3260. PubMed

Naylor, S.W. , Low, J.C. , Besser, T.E. , Mahajan, A. , Gunn, G.J. , Pearce, M.C. , et al (2003) Lymphoid follicle‐dense mucosa at the terminal rectum is the principal site of colonization of enterohemorrhagic Escherichia coli O157:H7 in the bovine host. Infect Immun 71: 1505–1512. PubMed PMC

Oksanen, J. , Blanchet, F.G. , Kindt, R. , Legendre, P. , Minchin, P.R. , O'hara, R. , et al (2013) Package ‘vegan’. Community ecology package, version 2.

Parks, D.H. , Tyson, G.W. , Hugenholtz, P. , and Beiko, R.G. (2014) STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics 30: 3123–3124. PubMed PMC

Pinheiro, J. , Bates, D. , DebRoy, S. , and Sarkar, D. (2014) R Core Team (2014) nlme: linear and nonlinear mixed effects models. R package version 3.1‐117. URL http://CRANR‐projectorg/package=nlme

Quast, C. , Pruesse, E. , Yilmaz, P. , Gerken, J. , Schweer, T. , Yarza, P. , et al (2013) The SILVA ribosomal RNA gene database project: improved data processing and web‐based tools. Nucleic Acids Res 41: D590–D596. PubMed PMC

R Development Core Team (2015) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.

Rapp, D. , Ross, C.M. , Pleydell, E.J. , and Muirhead, R.W. (2012) Differences in the fecal concentrations and genetic diversities of Campylobacter jejuni populations among individual cows in two dairy herds. Appl Environ Microbiol 78: 7564–7571. PubMed PMC

Rivera‐Chávez, F. , Zhang, L.F. , Faber, F. , Lopez, C.A. , Byndloss, M.X. , Olsan, E.E. , et al (2016) Depletion of butyrate‐producing Clostridia from the gut microbiota drives an aerobic luminal expansion of Salmonella . Cell Host Microbe 19: 443–454. PubMed PMC

Rognes, T. , Flouri, T. , Nichols, B. , Quince, C. , and Mahé, F. (2016) VSEARCH: a versatile open source tool for metagenomics. PeerJ 4: e2584. PubMed PMC

Sadeyen, J.R. , Trotereau, J. , Velge, P. , Marly, J. , Beaumont, C. , Barrow, P.A. , et al (2004) Salmonella carrier state in chicken: comparison of expression of immune response genes between susceptible and resistant animals. Microbes Infect 6: 1278–1286. PubMed

Sadeyen, J.R. , Trotereau, J. , Protais, J. , Beaumont, C. , Sellier, N. , Salvat, G. , et al (2006) Salmonella carrier‐state in hens: study of host resistance by a gene expression approach. Microbes Infect 8: 1308–1314. PubMed

Schellenberg and Maillard (1973) Techniques d’élevage de volailles axéniques. Journées Rech Avicoles Cunicoles INRA‐ITAVI‐ WPSA, Paris. pp. 283–285.

Slater, N. , Mitchell, R.M. , Whitlock, R.H. , Fyock, T. , Pradhan, A.K. , Knupfer, E. , et al (2016) Impact of the shedding level on transmission of persistent infections in Mycobacterium avium subspecies paratuberculosis (MAP). Vet Res 47: 38. PubMed PMC

Tamura, K. , and Nei, M. (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10: 512–526. PubMed

Theppangna, W. , Otsuki, K. , and Murase, T. (2006) Inhibitory effects of Enterococcus strains obtained from a probiotic product on in vitro growth of Salmonella enterica serovar enteritidis strain IFO3313. J Food Prot 69: 2258–2262. PubMed

Turner, L. , Ping, L. , Neubauer, M. , and Berg, H.C. (2016) Visualizing Flagella while tracking bacteria. Biophys J 111: 630–639. PubMed PMC

Van Cauteren, D. , Le Strat, Y. , Sommen, C. , Bruyand, M. , Tourdjman, M. , Da Silva, N.J. , et al (2017) Estimated annual numbers of foodborne pathogen‐associated illnesses, hospitalizations, and deaths, France, 2008–2013. Emerg Infect Dis 23: 1486–1492. PubMed PMC

Varmuzova, K. , Kubasova, T. , Davidova‐Gerzova, L. , Sisak, F. , Havlickova, H. , Sebkova, A. , et al (2016) Composition of Gut Microbiota Influences Resistance Of Newly Hatched Chickens to Salmonella Enteritidis infection. Front Microbiol 7: 957. PubMed PMC

Velge, P. , Cloeckaert, A. , and Barrow, P. (2005) Emergence of Salmonella epidemics: the problems related to Salmonella enterica serotype Enteritidis and multiple antibiotic resistance in other major serotypes. Vet Res 36: 267–288. PubMed

Videnska, P. , Faldynova, M. , Juricova, H. , Babak, V. , Sisak, F. , Havlickova, H. , and Rychlik, I. (2013) Chicken faecal microbiota and disturbances induced by single or repeated therapy with tetracycline and streptomycin. BMC Vet Res 9: 30. PubMed PMC

Videnska, P. , Sedlar, K. , Lukac, M. , Faldynova, M. , Gerzova, L. , Cejkova, D. , et al (2014) Succession and replacement of bacterial populations in the caecum of egg laying hens over their whole life. PLoS One 9: e115142. PubMed PMC

Wang, Q. , Garrity, G.M. , Tiedje, J.M. , and Cole, J.R. (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73: 5261–5267. PubMed PMC

Woolhouse, M.E. , Dye, C. , Etard, J.F. , Smith, T. , Charlwood, J.D. , Garnett, G.P. , et al (1997) Heterogeneities in the transmission of infectious agents: implications for the design of control programs. Proc Natl Acad Sci USA 94: 338–342. PubMed PMC

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