Escherichia coli limits Salmonella Typhimurium infections after diet shifts and fat-mediated microbiota perturbation in mice.
Animal Feed
Animals
Bile Acids and Salts
/ administration & dosage
Dietary Fats
/ administration & dosage
Escherichia coli
/ physiology
Female
Gastrointestinal Microbiome
Host-Pathogen Interactions
Male
Mice
Mice, Inbred C57BL
Microbial Interactions
Oleic Acids
/ administration & dosage
Salmonella typhimurium
/ physiology
Journal
Nature microbiology
ISSN: 2058-5276
Titre abrégé: Nat Microbiol
Pays: England
ID NLM: 101674869
Informations de publication
Date de publication:
12 2019
12 2019
Historique:
received:
22
08
2018
accepted:
23
08
2019
pubmed:
9
10
2019
medline:
8
7
2020
entrez:
9
10
2019
Statut:
ppublish
Résumé
The microbiota confers colonization resistance, which blocks Salmonella gut colonization
Identifiants
pubmed: 31591555
doi: 10.1038/s41564-019-0568-5
pii: 10.1038/s41564-019-0568-5
pmc: PMC6881180
mid: EMS84197
doi:
Substances chimiques
Bile Acids and Salts
0
Dietary Fats
0
Oleic Acids
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2164-2174Subventions
Organisme : Swiss National Science Foundation
ID : 173338
Pays : Switzerland
Organisme : Swiss National Science Foundation
ID : 153074
Pays : Switzerland
Organisme : Swiss National Science Foundation
ID : 158364
Pays : Switzerland
Organisme : Swiss National Science Foundation
ID : 136742
Pays : Switzerland
Organisme : Swiss National Science Foundation
ID : 167121
Pays : Switzerland
Références
Stecher, B., Berry, D. & Loy, A. Colonization resistance and microbial ecophysiology: using gnotobiotic mouse models and single-cell technology to explore the intestinal jungle. FEMS Microbiol. Rev. 37, 793–829 (2013).
pubmed: 23662775
David, L. A. et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature 505, 559–563 (2014).
Desai, M. S. et al. A dietary fiber-deprived gut microbiota degrades the colonic mucus barrier and enhances pathogen susceptibility. Cell 167, 1339–1353 (2016).
pubmed: 27863247
pmcid: 5131798
Barthel, M. et al. Pretreatment of mice with streptomycin provides a Salmonella enterica serovar Typhimurium colitis model that allows analysis of both pathogen and host. Infect. Immun. 71, 2839–2858 (2003).
pubmed: 12704158
pmcid: 153285
Brugiroux, S. et al. Genome-guided design of a defined mouse microbiota that confers colonization resistance against Salmonella enterica serovar Typhimurium. Nat. Microbiol. 2, 16215 (2016).
pubmed: 27869789
Stecher, B. et al. Gut inflammation can boost horizontal gene transfer between pathogenic and commensal Enterobacteriaceae. Proc. Natl Acad. Sci. USA 109, 1269–1274 (2012).
pubmed: 22232693
Arkan, M. C. et al. IKK-β links inflammation to obesity-induced insulin resistance. Nat. Med. 11, 191–198 (2005).
pubmed: 15685170
Kim, K. A., Gu, W., Lee, I. A., Joh, E. H. & Kim, D. H. High fat diet-induced gut microbiota exacerbates inflammation and obesity in mice via the TLR4 signaling pathway. PLoS ONE 7, e47713 (2012).
pubmed: 23091640
pmcid: 3473013
Moya-Perez, A., Neef, A. & Sanz, Y. Bifidobacterium pseudocatenulatum CECT 7765 reduces obesity-associated inflammation by restoring the lymphocyte-macrophage balance and gut microbiota structure in high-fat diet-fed mice. PLoS ONE 10, e0126976 (2015).
pubmed: 26161548
pmcid: 4498624
Hwang, D. H., Kim, J. A. & Lee, J. Y. Mechanisms for the activation of Toll-like receptor 2/4 by saturated fatty acids and inhibition by docosahexaenoic acid. Eur. J. Pharm. 785, 24–35 (2016).
Stecher, B., Maier, L. & Hardt, W. D. ‘Blooming’ in the gut: how dysbiosis might contribute to pathogen evolution. Nat. Rev. Microbiol. 11, 277–284 (2013).
pubmed: 23474681
Reddy, B. S., Mangat, S., Sheinfil, A., Weisburger, J. H. & Wynder, E. L. Effect of type and amount of dietary fat and 1,2-dimethylhydrazine on biliary bile acids, fecal bile acids and neutral sterols in rats. Cancer Res. 37, 2132–2137 (1977).
pubmed: 861940
Reddy, B. S. Diet and excretion of bile acids. Cancer Res. 41, 3766–3768 (1981).
pubmed: 6266664
Cummings, J. H. et al. Influence of diets high and low in animal fat on bowel habit, gastrointestinal transit time, fecal microflora, bile acid and fat excretion. J. Clin. Invest. 61, 953–963 (1978).
pubmed: 659584
pmcid: 372613
Begley, M., Gahan, C. G. & Hill, C. The interaction between bacteria and bile. FEMS Microbiol. Rev. 29, 625–651 (2005).
pubmed: 16102595
Islam, K. B. et al. Bile acid is a host factor that regulates the composition of the cecal microbiota in rats. Gastroenterology 141, 1773–1781 (2011).
pubmed: 21839040
Urdaneta, V. & Casadesus, J. Interactions between bacteria and bile salts in the gastrointestinal and hepatobiliary tracts. Front. Med. 4, 163 (2017).
MacConkey, A. T. Bile salt media and their advantages in some bacteriological examinations. J. Hyg. 8, 322–334 (1908).
pubmed: 20474363
Buckley, A. M. et al. The AcrAB-TolC efflux system of Salmonella enterica serovar Typhimurium plays a role in pathogenesis. Cell. Microbiol. 8, 847–856 (2006).
pubmed: 16611233
Nishino, K., Latifi, T. & Groisman, E. A. Virulence and drug resistance roles of multidrug efflux systems of Salmonella enterica serovar Typhimurium. Mol. Microbiol. 59, 126–141 (2006).
pubmed: 16359323
Devkota, S. et al. Dietary-fat-induced taurocholic acid promotes pathobiont expansion and colitis in Il10
pubmed: 22722865
pmcid: 3393783
Stecher, B. et al. Salmonella enterica serovar Typhimurium exploits inflammation to compete with the intestinal microbiota. PLoS Biol. 5, 2177–2189 (2007).
pubmed: 17760501
Winter, S. E. et al. Gut inflammation provides a respiratory electron acceptor for Salmonella. Nature 467, 426–429 (2010).
pubmed: 20864996
pmcid: 2946174
Winter, S. E. et al. Host-derived nitrate boosts growth of E. coli in the inflamed gut. Science 339, 708–711 (2013).
pubmed: 23393266
pmcid: 4004111
Raffatellu, M. et al. Lipocalin-2 resistance confers an advantage to Salmonella enterica serotype Typhimurium for growth and survival in the inflamed intestine. Cell Host Microbe 5, 476–486 (2009).
pubmed: 19454351
pmcid: 2768556
Litvak, Y., Byndloss, M. X. & Baumler, A. J. Colonocyte metabolism shapes the gut microbiota. Science 362, eaat9076 (2018).
pubmed: 30498100
pmcid: 6296223
Miki, T., Goto, R., Fujimoto, M., Okada, N. & Hardt, W. D. The bactericidal lectin RegIIIβ prolongs gut colonization and enteropathy in the streptomycin mouse model for Salmonella diarrhea. Cell Host Microbe 21, 195–207 (2017).
pubmed: 28111202
Miki, T., Holst, O. & Hardt, W. D. The bactericidal activity of the C-type lectin RegIIIβ against Gram-negative bacteria involves binding to lipid A. J. Biol. Chem. 287, 34844–34855 (2012).
pubmed: 22896700
pmcid: 3464586
Mukherjee, S. et al. Antibacterial membrane attack by a pore-forming intestinal C-type lectin. Nature 505, 103–107 (2014).
pubmed: 24256734
Lopez, C. A. et al. Phage-mediated acquisition of a type III secreted effector protein boosts growth of Salmonella by nitrate respiration. mBio 3, e00143-12 (2012).
pubmed: 22691391
pmcid: 3374392
Berg, R. D. The indigenous gastrointestinal microflora. Trends Microbiol. 4, 430–435 (1996).
pubmed: 8950812
Piddock, L. J. Multidrug-resistance efflux pumps—not just for resistance. Nat. Rev. Microbiol. 4, 629–636 (2006).
pubmed: 16845433
Wotzka, S. Y. et al. Microbiota stability in healthy individuals after single-dose lactulose challenge—a randomized controlled study. PLoS ONE 13, e0206214 (2018).
pubmed: 30359438
pmcid: 6201941
Litvak, Y. et al. Commensal Enterobacteriaceae protect against Salmonella colonization through oxygen competition. Cell Host Microbe 25, 128–139 (2019).
pubmed: 30629913
Sana, T. G. et al. Salmonella Typhimurium utilizes a T6SS-mediated antibacterial weapon to establish in the host gut. Proc. Natl Acad. Sci. USA 113, E5044–E5051 (2016).
pubmed: 27503894
Deriu, E. et al. Probiotic bacteria reduce Salmonella Typhimurium intestinal colonization by competing for iron. Cell Host Microbe 14, 26–37 (2013).
pubmed: 23870311
pmcid: 3752295
Nedialkova, L. P. et al. Temperate phages promote colicin-dependent fitness of Salmonella enterica serovar Typhimurium. Environ. Microbiol. 18, 1591–1603 (2016).
pubmed: 26439675
Conway, T. & Cohen, P. S. Commensal and pathogenic Escherichia coli metabolism in the gut. Microbiol. Spectr. 3, MBP-0006-2014 (2015).
Baucheron, S. et al. AcrAB-TolC directs efflux-mediated multidrug resistance in Salmonella enterica serovar Typhimurium DT104. Antimicrob. Agents Chemother. 48, 3729–3735 (2004).
pubmed: 15388427
pmcid: 521921
Eaves, D. J., Ricci, V. & Piddock, L. J. Expression of acrB, acrF, acrD, marA and soxS in Salmonella enterica serovar Typhimurium: role in multiple antibiotic resistance. Antimicrob. Agents Chemother. 48, 1145–1150 (2004).
pubmed: 15047514
pmcid: 375282
Urdaneta, V. & Casadesus, J. Adaptation of Salmonella enterica to bile: essential role of AcrAB-mediated efflux. Environ. Microbiol. 20, 1405–1418 (2018).
pubmed: 29349886
Theriot, C. M. et al. Antibiotic-induced shifts in the mouse gut microbiome and metabolome increase susceptibility to Clostridium difficile infection. Nat. Commun. 5, 3114 (2014).
pubmed: 24445449
pmcid: 3950275
Rozwandowicz, M. et al. Plasmids carrying antimicrobial resistance genes in Enterobacteriaceae. J. Antimicrob. Chemother. 73, 1121–1137 (2018).
pubmed: 29370371
Hoiseth, S. K. & Stocker, B. A. Aromatic-dependent Salmonella Typhimurium are non-virulent and effective as live vaccines. Nature 291, 238–239 (1981).
pubmed: 7015147
Datsenko, K. A. & Wanner, B. L. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl Acad. Sci. USA 97, 6640–6645 (2000).
Grant, A. J. et al. Modelling within-host spatiotemporal dynamics of invasive bacterial disease. PLoS Biol. 6, e74 (2008).
pubmed: 18399718
pmcid: 2288627
Gil, D. & Bouche, J. P. ColE1-type vectors with fully repressible replication. Gene 105, 17–22 (1991).
pubmed: 1937005
Kaiser, P. et al. Cecum lymph node dendritic cells harbor slow-growing bacteria phenotypically tolerant to antibiotic treatment. PLoS Biol. 12, e1001793 (2014).
pubmed: 24558351
pmcid: 3928039
Moor, K. et al. High-avidity IgA protects the intestine by enchaining growing bacteria. Nature 544, 498–502 (2017).
pubmed: 28405025
Sturm, A. et al. The cost of virulence: retarded growth of Salmonella Typhimurium cells expressing type III secretion system 1. PLoS Pathog. 7, e1002143 (2011).
pubmed: 21829349
pmcid: 3145796
Li, H. et al. The outer mucus layer hosts a distinct intestinal microbial niche. Nat. Commun. 6, 8292 (2015).
pubmed: 26392213
pmcid: 4595636
Apprill, A., McNally, S., Parsons, R. & Weber, L. Minor revision to V4 region SSU rRNA 806R gene primer greatly increases detection of SAR11 bacterioplankton. Aquatic Microbial Ecol. 75, 129–137 (2015).
Parada, A. E., Needham, D. M. & Fuhrman, J. A. Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ. Microbiol. 18, 1403–1414 (2016).
pubmed: 26271760
Dey, N. et al. Regulators of gut motility revealed by a gnotobiotic model of diet–microbiome interactions related to travel. Cell 163, 95–107 (2015).
pubmed: 26406373
pmcid: 4583712
Fuhrer, T., Heer, D., Begemann, B. & Zamboni, N. High-throughput, accurate mass metabolome profiling of cellular extracts by flow injection-time-of-flight mass spectrometry. Anal. Chem. 83, 7074–7080 (2011).
pubmed: 21830798
Kanehisa, M. & Goto, S. KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res. 28, 27–30 (2000).
pubmed: 10592173
pmcid: 102409
Yin, S. et al. Factors affecting separation and detection of bile acids by liquid chromatography coupled with mass spectrometry in negative mode. Anal. Bioanal. Chem. 409, 5533–5545 (2017).
pubmed: 28689325
pmcid: 6554201
Wiegand, I., Hilpert, K. & Hancock, R. E. Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances. Nat. Protoc. 3, 163–175 (2008).
pubmed: 18274517
Lambert, R. J. & Pearson, J. Susceptibility testing: accurate and reproducible minimum inhibitory concentration (MIC) and non-inhibitory concentration (NIC) values. J. Appl. Microbiol. 88, 784–790 (2000).
pubmed: 10792538
Cremer, J., Arnoldini, M. & Hwa, T. Effect of water flow and chemical environment on microbiota growth and composition in the human colon. Proc. Natl Acad. Sci. USA 114, 6438–6443 (2017).
pubmed: 28588144
Vandeputte, D. et al. Quantitative microbiome profiling links gut community variation to microbial load. Nature 551, 507–511 (2017).
pubmed: 29143816
Soetaert, K., Petzoldt, T. & Setzer, R. W. Solving differential equations in R: Package deSolve. J. Stat. Softw. 33, 1–25 (2010).
R Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2014); https://www.R-project.org/
Letunic, I. & Bork, P. Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res. 44, W242–W245 (2016).
pubmed: 27095192
pmcid: 4987883