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Dysbiosis individualizes the fitness effect of antibiotic resistance in the mammalian gut

  • 1.

    Antimicrobial Resistance: Global Report on Surveillance (WHO, 2014).

  • 2.

    Gullberg, E. et al. Selection of resistant bacteria at very low antibiotic concentrations. PLoS Pathog. 7, e1002158 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 3.

    MacLean, R. C. & Vogwill, T. Limits to compensatory adaptation and the persistence of antibiotic resistance in pathogenic bacteria. Evol. Med. Publ. Health 1, 4–12 (2015).

    Google Scholar 

  • 4.

    Bhullar, K. et al. Antibiotic resistance is prevalent in an isolated cave microbiome. PLoS ONE 7, e34953 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 5.

    Forsberg, K. J. et al. The shared antibiotic resistome of soil bacteria and human pathogens. Science 337, 1107–1111 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 6.

    Hu, Y. et al. Metagenome-wide analysis of antibiotic resistance genes in a large cohort of human gut microbiota. Nat. Commun. 4, 2151 (2013).

    PubMed  Google Scholar 

  • 7.

    Andersson, D. I. & Hughes, D. Antibiotic resistance and its cost: is it possible to reverse resistance? Nat. Rev. Microbiol. 8, 260–271 (2010).

    CAS  PubMed  Google Scholar 

  • 8.

    Durão, P., Balbontín, R. & Gordo, I. Evolutionary mechanisms shaping the maintenance of antibiotic resistance. Trends Microbiol. 26, 677–691 (2018).

    PubMed  Google Scholar 

  • 9.

    Trindade, S. et al. Positive epistasis drives the acquisition of multidrug resistance. PLoS Genet 5, e1000578 (2009).

    PubMed  PubMed Central  Google Scholar 

  • 10.

    Miskinyte, M. & Gordo, I. Increased survival of antibiotic-resistant Escherichia coli inside macrophages. Antimicrob. Agents Chemother. 57, 189–195 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 11.

    Durão, P., Gülereşi, D., Proença, J. & Gordo, I. Enhanced survival of rifampin- and streptomycin-resistant Escherichia coli inside macrophages. Antimicrob. Agents Chemother. 60, 4324–4332 (2016).

    PubMed  PubMed Central  Google Scholar 

  • 12.

    Reynolds, M. G. Compensatory evolution in rifampin-resistant Escherichia coli. Genetics 156, 1471–1481 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 13.

    Enne, V. I., Bennett, P. M., Livermore, D. M. & Hall, L. M. C. Enhancement of host fitness by the sul2-coding plasmid p9123 in the absence of selective pressure. J. Antimicrob. Chemother. 53, 958–963 (2004).

    CAS  PubMed  Google Scholar 

  • 14.

    Gagneux, S. et al. The competitive cost of antibiotic resistance in Mycobacterium tuberculosis. Science 312, 1944–1946 (2006).

    CAS  PubMed  Google Scholar 

  • 15.

    Melnyk, A. H., Wong, A. & Kassen, R. The fitness costs of antibiotic resistance mutations. Evol. Appl. 8, 273–283 (2015).

    PubMed  Google Scholar 

  • 16.

    Seppälä, H. et al. The effect of changes in the consumption of macrolide antibiotics on erythromycin resistance in group A streptococci in Finland. N. Engl. J. Med. 337, 441–446 (1997).

    PubMed  Google Scholar 

  • 17.

    Enne, V. I., Livermore, D. M., Stephens, P. & Hall, L. M. Persistence of sulphonamide resistance in Escherichia coli in the UK despite national prescribing restriction. Lancet 357, 1325–1328 (2001).

    CAS  PubMed  Google Scholar 

  • 18.

    Bean, D. C., Livermore, D. M., Papa, I. & Hall, L. M. C. Resistance among Escherichia coli to sulphonamides and other antimicrobials now little used in man. J. Antimicrob. Chemother. 56, 962–964 (2005).

    CAS  PubMed  Google Scholar 

  • 19.

    Gottesman, B. S., Carmeli, Y., Shitrit, P. & Chowers, M. Impact of quinolone restriction on resistance patterns of Escherichia coli isolated from urine by culture in a community setting. Clin. Infect. Dis. 49, 869–875 (2009).

    CAS  PubMed  Google Scholar 

  • 20.

    Trindade, S., Sousa, A. & Gordo, I. Antibiotic resistance and stress in the light of Fisher’s model. Evolution 66, 3815–3824 (2012).

    PubMed  Google Scholar 

  • 21.

    Hall, A. R., Angst, D. C., Schiessl, K. T. & Ackermann, M. Costs of antibiotic resistance—separating trait effects and selective effects. Evol. Appl. 8, 261–272 (2015).

    PubMed  Google Scholar 

  • 22.

    Durão, P., Trindade, S., Sousa, A. & Gordo, I. Multiple resistance at no cost: rifampicin and streptomycin a dangerous liaison in the spread of antibiotic resistance. Mol. Biol. Evol. 32, 2675–2680 (2015).

    PubMed  PubMed Central  Google Scholar 

  • 23.

    Rodríguez-Verdugo, A., Gaut, B. S. & Tenaillon, O. Evolution of Escherichia coli rifampicin resistance in an antibiotic-free environment during thermal stress. BMC Evol. Biol. 13, 50 (2013).

    PubMed  PubMed Central  Google Scholar 

  • 24.

    Silva, R. F. et al. Pervasive sign epistasis between conjugative plasmids and drug-resistance chromosomal mutations. PLoS Genet. 7, e1002181 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 25.

    Knopp, M. & Andersson, D. I. Predictable phenotypes of antibiotic resistance mutations. mBio 9, e00770-18 (2018).

    PubMed  PubMed Central  Google Scholar 

  • 26.

    Roux, D. et al. Fitness cost of antibiotic susceptibility during bacterial infection. Sci. Transl. Med. 7, 297ra114 (2015).

    PubMed  Google Scholar 

  • 27.

    Luo, N. et al. Enhanced in vivo fitness of fluoroquinolone-resistant Campylobacter jejuni in the absence of antibiotic selection pressure. Proc. Natl Acad. Sci. USA 102, 541–546 (2005).

    CAS  PubMed  Google Scholar 

  • 28.

    Koch, G. et al. Evolution of resistance to a last-resort antibiotic in Staphylococcus aureus via bacterial competition. Cell 158, 1060–1071 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 29.

    López-Rojas, R. et al. Impaired virulence and in vivo fitness of colistin-resistant Acinetobacter baumannii. J. Infect. Dis. 203, 545–548 (2011).

    PubMed  PubMed Central  Google Scholar 

  • 30.

    Björkholm, B. et al. Mutation frequency and biological cost of antibiotic resistance in Helicobacter pylori. Proc. Natl Acad. Sci. USA 98, 14607–14612 (2001).

    PubMed  Google Scholar 

  • 31.

    Warner, D. M., Folster, J. P., Shafer, W. M. & Jerse, A. E. Regulation of the MtrC-MtrD-MtrE efflux-pump system modulates the in vivo fitness of Neisseria gonorrhoeae. J. Infect. Dis. 196, 1804–1812 (2007).

    CAS  PubMed  Google Scholar 

  • 32.

    Björkman, J., Hughes, D. & Andersson, D. I. Virulence of antibiotic-resistant Salmonella typhimurium. Proc. Natl Acad. Sci. USA 95, 3949–3953 (1998).

    PubMed  Google Scholar 

  • 33.

    Gumpert, H. et al. Transfer and persistence of a multi-drug resistance plasmid in situ of the infant gut microbiota in the absence of antibiotic treatment. Front. Microbiol. 8, 1852 (2017).

    PubMed  PubMed Central  Google Scholar 

  • 34.

    Porse, A. et al. Genome dynamics of Escherichia coli during antibiotic treatment: transfer, loss, and persistence of genetic elements in situ of the infant gut. Front. Cell. Infect. Microbiol. 7, 126 (2017).

    PubMed  PubMed Central  Google Scholar 

  • 35.

    Barreto, Â. et al. Detection of antibiotic resistant E. coli and Enterococcus spp. in stool of healthy growing children in Portugal. J. Basic Microbiol. 49, 503–512 (2009).

    CAS  PubMed  Google Scholar 

  • 36.

    Hong, S. et al. Genetic characterization of atypical Shigella flexneri isolated in Korea. J. Microbiol. Biotechnol. 20, 1457–1462 (2010).

    CAS  PubMed  Google Scholar 

  • 37.

    Rahmani, F., Fooladi, A. A. I., Marashi, S. M. A. & Nourani, M. R. Drug resistance in Vibrio cholerae strains isolated from clinical specimens. Acta Microbiol. Immunol. Hung. 59, 77–84 (2012).

    CAS  PubMed  Google Scholar 

  • 38.

    Barroso-Batista, J. et al. The first steps of adaptation of Escherichia coli to the gut are dominated by soft sweeps. PLOS Genet. 10, e1004182 (2014).

    PubMed  PubMed Central  Google Scholar 

  • 39.

    Stebbins, R. B., Graessle, O. E. & Robinson, H. J. Studies on the absorption and excretion of streptomycin in animals. Proc. Soc. Exp. Biol. Med. 60, 68–73 (1945).

    CAS  PubMed  Google Scholar 

  • 40.

    Ng, K. M. et al. Recovery of the gut microbiota after antibiotics depends on host diet, community context, and environmental reservoirs. Cell Host Microbe 26, 650–665 (2019).

    CAS  PubMed  Google Scholar 

  • 41.

    Robertson, S. J. et al. Comparison of co-housing and littermate methods for microbiota standardization in mouse models. Cell Rep. 27, 1910–1919 (2019).

    CAS  PubMed  Google Scholar 

  • 42.

    Barroso-Batista, J., Demengeot, J. & Gordo, I. Adaptive immunity increases the pace and predictability of evolutionary change in commensal gut bacteria. Nat. Commun. 6, 8945 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 43.

    Coyte, K. Z., Schluter, J. & Foster, K. R. The ecology of the microbiome: networks, competition, and stability. Science 350, 663–666 (2015).

    CAS  PubMed  Google Scholar 

  • 44.

    Posfai, A., Taillefumier, T. & Wingreen, N. S. Metabolic trade-offs promote diversity in a model ecosystem. Phys. Rev. Lett. 118, 028103 (2017).

    PubMed  PubMed Central  Google Scholar 

  • 45.

    Ley, R. E. et al. Obesity alters gut microbial ecology. Proc. Natl Acad. Sci. USA 102, 11070–11075 (2005).

    CAS  PubMed  Google Scholar 

  • 46.

    Ubeda, C. et al. Familial transmission rather than defective innate immunity shapes the distinct intestinal microbiota of TLR-deficient mice. J. Exp. Med. 209, 1445–1456 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 47.

    Brandis, G., Wrande, M., Liljas, L. & Hughes, D. Fitness-compensatory mutations in rifampicin-resistant RNA polymerase. Mol. Microbiol. 85, 142–151 (2012).

    CAS  PubMed  Google Scholar 

  • 48.

    Maisnier-Patin, S., Berg, O. G., Liljas, L. & Andersson, D. I. Compensatory adaptation to the deleterious effect of antibiotic resistance in Salmonella typhimurium. Mol. Microbiol. 46, 355–366 (2002).

    CAS  PubMed  Google Scholar 

  • 49.

    Moura de Sousa, J., Balbontín, R., Durão, P. & Gordo, I. Multidrug-resistant bacteria compensate for the epistasis between resistances. PLoS Biol. 15, e2001741 (2017).

    PubMed  PubMed Central  Google Scholar 

  • 50.

    Lourenço, M. et al. A mutational hotspot and strong selection contribute to the order of mutations selected for during Escherichia coli adaptation to the gut. PLOS Genet. 12, e1006420 (2016).

    PubMed  PubMed Central  Google Scholar 

  • 51.

    Frazão, N., Sousa, A., Lässig, M. & Gordo, I. Horizontal gene transfer overrides mutation in Escherichia coli colonizing the mammalian gut. Proc. Natl Acad. Sci. USA 116, 17906–17915 (2019).

    PubMed  Google Scholar 

  • 52.

    Ghalayini, M. et al. Evolution of a dominant natural isolate of Escherichia coli in the human gut over the course of a year suggests a neutral evolution with reduced effective population size. Appl. Environ. Microbiol. 84, e02377-17 (2018).

    PubMed  PubMed Central  Google Scholar 

  • 53.

    Jakobsson, H. E. et al. Short-term antibiotic treatment has differing long-term impacts on the human throat and gut microbiome. PLoS ONE 5, e9836 (2010).

    PubMed  PubMed Central  Google Scholar 

  • 54.

    Jernberg, C., Löfmark, S., Edlund, C. & Jansson, J. K. Long-term ecological impacts of antibiotic administration on the human intestinal microbiota. ISME J. 1, 56–66 (2007).

    CAS  PubMed  Google Scholar 

  • 55.

    Qi, Q., Preston, G. M. & MacLean, R. C. Linking system-wide impacts of RNA polymerase mutations to the fitness cost of rifampin resistance in Pseudomonas aeruginosa. mBio 5, e01562–14 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 56.

    Barnard, A. M. L., Simpson, N. J. L., Lilley, K. S. & Salmond, G. P. C. Mutations in rpsL that confer streptomycin resistance show pleiotropic effects on virulence and the production of a carbapenem antibiotic in Erwinia carotovora. Microbiology 156, 1030–1039 (2010).

    CAS  PubMed  Google Scholar 

  • 57.

    Robinson, L. J., Cameron, A. D. S. & Stavrinides, J. Spontaneous and on point: do spontaneous mutations used for laboratory experiments cause pleiotropic effects that might confound bacterial infection and evolution assays? FEMS Microbiol. Lett. 362, fnv177 (2015).

  • 58.

    Ruusala, T., Andersson, D., Ehrenberg, M. & Kurland, C. G. Hyper-accurate ribosomes inhibit growth. EMBO J. 3, 2575–2580 (1984).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 59.

    Libby, R. T., Nelson, J. L., Calvo, J. M. & Gallant, J. A. Transcriptional proofreading in Escherichia coli. EMBO J. 8, 3153–3158 (1989).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 60.

    Blank, A., Gallant, J. A., Burgess, R. R. & Loeb, L. A. An RNA polymerase mutant with reduced accuracy of chain elongation. Biochemistry 25, 5920–5928 (1986).

    CAS  PubMed  Google Scholar 

  • 61.

    Strathern, J. N., Jin, D. J., Court, D. L. & Kashlev, M. Isolation and characterization of transcription fidelity mutants. Biochim. Biophys. Acta 1819, 694–699 (2012).

  • 62.

    Li, J. et al. Antibiotic treatment drives the diversification of the human gut resistome. Genom. Proteom. Bioinform. 17, 39–51 (2019).

    CAS  Google Scholar 

  • 63.

    Sousa, A. et al. Recurrent reverse evolution maintains polymorphism after strong bottlenecks in commensal gut bacteria. Mol. Biol. Evol. 34, 2879–2892 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 64.

    Muinck, E. Jde et al. Context-dependent competition in a model gut bacterial community. PLoS ONE 8, e67210 (2013).

    PubMed  PubMed Central  Google Scholar 

  • 65.

    Barroso-Batista, J. et al. Specific eco-evolutionary contexts in the mouse gut reveal Escherichia coli metabolic versatility. Curr. Biol. 30, 1049–1062.e7 (2020).

    CAS  PubMed  Google Scholar 

  • 66.

    Tramontano, M. et al. Nutritional preferences of human gut bacteria reveal their metabolic idiosyncrasies. Nat. Microbiol. 3, 514–522 (2018).

    CAS  PubMed  Google Scholar 

  • 67.

    Görke, B. & Stülke, J. Carbon catabolite repression in bacteria: many ways to make the most out of nutrients. Nat. Rev. Microbiol. 6, 613–624 (2008).

    PubMed  Google Scholar 

  • 68.

    Kovárová-Kovar, K. & Egli, T. Growth kinetics of suspended microbial cells: from single-substrate-controlled growth to mixed-substrate kinetics. Microbiol. Mol. Biol. Rev. 62, 646–666 (1998).

    PubMed  PubMed Central  Google Scholar 

  • 69.

    Chang, D.-E. et al. Carbon nutrition of Escherichia coli in the mouse intestine. Proc. Natl Acad. Sci. USA 101, 7427–7432 (2004).

    CAS  PubMed  Google Scholar 

  • 70.

    Belenguer, A. et al. Two routes of metabolic cross-feeding between Bifidobacterium adolescentis and butyrate-producing anaerobes from the human gut. Appl. Environ. Microbiol. 72, 3593–3599 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 71.

    Samuel, B. S. & Gordon, J. I. A humanized gnotobiotic mouse model of host-archaeal-bacterial mutualism. Proc. Natl Acad. Sci. USA. 103, 10011–10016 (2006).

    CAS  PubMed  Google Scholar 

  • 72.

    Goldford, J. E. et al. Emergent simplicity in microbial community assembly. Science 361, 469–474 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 73.

    Filippo, C. D. et al. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc. Natl Acad. Sci. USA 107, 14691–14696 (2010).

    PubMed  Google Scholar 

  • 74.

    Franzosa, E. A. et al. Identifying personal microbiomes using metagenomic codes. Proc. Natl Acad. Sci. USA 112, E2930–E2938 (2015).

    CAS  PubMed  Google Scholar 

  • 75.

    Thompson, J. A., Oliveira, R. A., Djukovic, A., Ubeda, C. & Xavier, K. B. Manipulation of the quorum sensing signal AI-2 affects the antibiotic-treated gut microbiota. Cell Rep. 10, 1861–1871 (2015).

    CAS  PubMed  Google Scholar 

  • 76.

    Caporaso, J. G. et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335–336 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 77.

    Callahan, B. J. et al. DADA2: high-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581–583 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 78.

    Mandal, S. et al. Analysis of composition of microbiomes: a novel method for studying microbial composition. Microb. Ecol. Health Dis. 26, 27663 (2015).

    PubMed  Google Scholar 

  • 79.

    Lozupone, C. & Knight, R. UniFrac: a new phylogenetic method for comparing microbial communities. Appl. Environ. Microbiol. 71, 8228–8235 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 80.

    DeSantis, T. Z. et al. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microbiol. 72, 5069–5072 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 81.

    Soetaert, K., Petzoldt, T. & Setzer, R. W. Solving differential equations in R: package deSolve. J. Stat. Softw. 33, 1–25 (2010).

    Google Scholar 

  • 82.

    Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer-Verlag, 2016); https://ggplot2.tidyverse.org

  • 83.

    Oksanen, J. et al. vegan: Community Ecology Package. R package version 2.5-6 (2019); https://CRAN.R-project.org/package=vegan


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