Saturday, October 5, 2024

Metabolism of l-arabinose converges with virulence regulation to promote enteric pathogen fitness – Nature Communications

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  • Caballero-Flores, G., Pickard, J. M. & Núñez, G. Microbiota-mediated colonization resistance: mechanisms and regulation. Nat. Rev. Microbiol. 21, 347–360 (2023).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Baümler, A. J. & Sperandio, V. Interactions between the microbiota and pathogenic bacteria in the gut. Nature 535, 85–93 (2016).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Connolly, J. P. R., Brett Finlay, B. & Roe, A. J. From ingestion to colonization: the influence of the host environment on regulation of the LEE encoded type III secretion system in enterohaemorrhagic Escherichia coli. Front. Microbiol. 6, 568 (2015).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Turner, N. C. A., Connolly, J. P. R. & Roe, A. J. Control freaks—signals and cues governing the regulation of virulence in attaching and effacing pathogens. Biochem. Soc. Trans. 47, 229–238 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Wale, K. R., Cottam, C., Connolly, J. P. & Roe, A. J. Transcriptional and metabolic regulation of EHEC and Citrobacter rodentium pathogenesis. Curr. Opin. Microbiol. 63, 70–75 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Kaper, J. B., Nataro, J. P. & Mobley, H. L. Pathogenic Escherichia coli. Nat. Rev. Microbiol. 2, 123–140 (2004).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Croxen, M. A. & Finlay, B. B. Molecular mechanisms of Escherichia coli pathogenicity. Nat. Rev. Microbiol. 8, 26–38 (2010).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Moon, H. W., Whipp, S. C., Argenzio, R. A., Levine, M. M. & Giannella, R. A. Attaching and effacing activities of rabbit and human enteropathogenic Escherichia coli in pig and rabbit intestines. Infect. Immun. 41, 1340–1351 (1983).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kenny, B. et al. Enteropathogenic E. coli (EPEC) transfers its receptor for intimate adherence into mammalian cells. Cell 91, 511–520 (1997).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Jerse, A. E., Yu, J., Tall, B. D. & Kaper, J. B. A genetic locus of enteropathogenic Escherichia coli necessary for the production of attaching and effacing lesions on tissue culture cells. Proc. Natl Acad. Sci. USA 87, 7839–7843 (1990).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Mcdaniel, T. K., Jarvis, K. G., Donnenberg, M. S. & Kaper, J. B. A genetic locus of enterocyte effacement conserved among diverse enterobacterial pathogens. Proc. Natl Acad. Sci. USA 92, 1664–1668 (1995).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Deng, W. et al. Dissecting virulence: systematic and functional analyses of a pathogenicity island. Proc. Natl Acad. Sci. USA 101, 3597–3602 (2004).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Dean, P. & Kenny, B. The effector repertoire of enteropathogenic E. coli: ganging up on the host cell. Curr. Opin. Microbiol. 12, 101–109 (2009).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Tobe, T. et al. An extensive repetoire of type III secretion effectors in Escherichia coli O157 and the role of lambdoid phages in their dissemination. Proc. Natl Acad. Sci. USA 103, 14941–14946 (2006).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Perna, N. T. et al. Genome sequence of enterohaemorrhagic Escherichia coli O157:H7. Nature 409, 529–533 (2001).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Wong, A. R. C. et al. Enteropathogenic and enterohaemorrhagic Escherichia coli: Even more subversive elements. Mol. Microbiol. 80, 1420–1438 (2011).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Collins, J. W. et al. Citrobacter rodentium: Infection, inflammation and the microbiota. Nat. Rev. Microbiol. 12, 612–623 (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Mullineaux-Sanders, C. et al. Citrobacter rodentium–host–microbiota interactions: immunity, bioenergetics and metabolism. Nat. Rev. Microbiol. 17, 701–715 (2019).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Crepin, V. F., Collins, J. W., Habibzay, M. & Frankel, G. Citrobacter rodentium mouse model of bacterial infection. Nat. Protoc. 11, 1851–1876 (2016).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Kamada, N. et al. Regulated virulence controls the ability of a pathogen to compete with the gut microbiota. Science 336, 1325–1329 (2012).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Connolly, J. P. R. et al. Host-associated niche metabolism controls enteric infection through fine-tuning the regulation of type 3 secretion. Nat. Commun. 9, 4187 (2018).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Njoroge, J. W., Nguyen, Y., Curtis, M. M., Moreira, C. G. & Sperandio, V. Virulence meets metabolism: Cra and KdpE gene regulation in enterohemorrhagic Escherichia coli. MBio 3, e00280–00212 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Curtis, M. M. et al. The gut commensal bacteroides thetaiotaomicron exacerbates enteric infection through modification of the metabolic landscape. Cell Host Microbe 16, 759–769 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Menezes-Garcia, Z., Kumar, A., Zhu, W., Winter, S. E. & Sperandio, V. L-Arginine sensing regulates virulence gene expression and disease progression in enteric pathogens. Proc. Natl Acad. Sci. USA 117, 12387–12393 (2020).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Connolly, J. P. R. et al. The host metabolite D-serine contributes to bacterial niche specificity through gene selection. ISME J. 9, 1039–1051 (2015).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • O’Boyle, N., Connolly, J. P. R., Tucker, N. P. & Roe, A. J. Genomic plasticity of pathogenic Escherichia coli mediates D-serine tolerance via multiple adaptive mechanisms. Proc. Natl Acad. Sci. USA 117, 22484–22493 (2020).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Conway, T. & Cohen, P. S. Commensal and pathogenic Escherichia coli Metabolism in the gut. Microbiol. Spectr. 3, MBP-0006-2014 (2015).

    Article 

    Google Scholar
     

  • Fabich, A. J. et al. Comparison of carbon nutrition for pathogenic and commensal Escherichia coli strains in the mouse intestine. Infect. Immun. 76, 1143–1152 (2008).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Crozier, L. et al. The role of l-arabinose metabolism for Escherichia coli o157:H7 in edible plants. Microbiology 167, 1–12 (2021).

    Article 

    Google Scholar
     

  • Mayer, C. & Boos, W. Hexose/pentose and hexitol/pentitol metabolism. EcoSal Plus https://doi.org/10.1128/ecosalplus.3.4.1 (2005).

  • John, M. et al. Use of in vivo-induced antigen technology for identification of Escherichia coli O157:H7 proteins expressed during human infection. Infect. Immun. 73, 2665–2679 (2005).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Segura, A. et al. Transcriptomic analysis reveals specific metabolic pathways of enterohemorrhagic Escherichia coli O157:H7 in bovine digestive contents. BMC Genom. 19, 766 (2018).

    Article 

    Google Scholar
     

  • Rice, A. J., Park, A. & Pinkett, H. W. Diversity in ABC transporters: type I, II and III importers. Crit. Rev. Biochem. Mol. Biol. 49, 426–437 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Drousiotis, K. et al. Characterization of the l-arabinofuranose-specific GafABCD ABC transporter essential for l-arabinose-dependent growth of the lignocellulose-degrading bacterium Shewanella sp. ANA-3. Microbiology 169, 3 (2023).

    Article 

    Google Scholar
     

  • Zschiedrich, C. P., Keidel, V. & Szurmant, H. Molecular mechanisms of two-component signal transduction. J. Mol. Biol. 428, 3752–3775 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Schleif, R. AraC protein, regulation of the l-arabinose operon in Escherichia coli, and the light switch mechanism of AraC action. FEMS Microbiol. Rev. 34, 779–796 (2010).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Mullineaux-Sanders, C. et al. Citrobacter rodentium relies on commensals for colonization of the colonic mucosa. Cell Rep. 21, 3381–3389 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Carlson-Banning, K. M. & Sperandio, V. Catabolite and oxygen regulation of enterohemorrhagic Escherichia coli virulence. MBio 7, e01852–16 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Freter, R., Brickner, H., Fekete, J., Vickerman, M. M. & Carey, K. E. Survival and implantation of Escherichia coli in the intestinal tract. Infect. Immun. 39, 686–703 (1983).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Yip, A. Y. G. et al. Antibiotics promote intestinal growth of carbapenem-resistant Enterobacteriaceae by enriching nutrients and depleting microbial metabolites. Nat. Commun. 14, 5094 (2023).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Liu, B. et al. Enterohaemorrhagic E. coli utilizes host- and microbiota-derived L-malate as a signaling molecule for intestinal colonization. Nat. Commun. 14, 7227 (2023).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Schutte, J. B., de Jong, J., van Weerden, E. J. & Tamminga, S. Nutritional implications of l -arabinose in pigs. Br. J. Nutr. 68, 195–207 (1992).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Schwalm, N. D., Townsend, G. E. & Groisman, E. A. Multiple signals govern utilization of a polysaccharide in the gut bacterium bacteroides thetaiotaomicron. MBio https://doi.org/10.1128/mbio.01342-16 (2016).

  • Pereira, G. V. et al. Degradation of complex arabinoxylans by human colonic Bacteroidetes. Nat. Commun. 12, 459 (2021).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Martens, E. C. et al. Recognition and degradation of plant cell wall polysaccharides by two human gut symbionts. PLoS Biol. 9, e1001221 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Rogowski, A. et al. Glycan complexity dictates microbial resource allocation in the large intestine. Nat. Commun. 6, 7481 (2015).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Kyle, J. L., Parker, C. T., Goudeau, D. & Brandl, M. T. Transcriptome analysis of escherichia coli O157:H7 exposed to lysates of lettuce leaves. Appl. Environ. Microbiol. 76, 1375–1387 (2010).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Petty, N. K. et al. The Citrobacter rodentium genome sequence reveals convergent evolution with human pathogenic Escherichia coli. J. Bacteriol. 192, 525–538 (2010).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Harper, L. et al. Staphylococcus aureus responds to the central metabolite pyruvate to regulate virulence. MBio https://doi.org/10.1128/mbio.02272-17 (2018).

  • Jiang, L. et al. Salmonella Typhimurium reprograms macrophage metabolism via T3SS effector SopE2 to promote intracellular replication and virulence. Nat. Commun. 12, 879 (2021).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Wiebe, M. A. et al. Serine deamination is a new acid tolerance mechanism observed in uropathogenic Escherichia coli. MBio 13, e02963-22 (2022).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ruddle, S. J., Massis, L. M., Cutter, A. C. & Monack, D. M. Salmonella-liberated dietary L-arabinose promotes expansion in superspreaders. Cell Host Microbe 31, 405–417.e5 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Neumann, M. et al. Deprivation of dietary fiber in specific-pathogen-free mice promotes susceptibility to the intestinal mucosal pathogen Citrobacter rodentium. Gut Microbes 13, 1966263 (2021).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Desai, M. S. et al. A dietary fiber-deprived gut microbiota degrades the colonic mucus barrier and enhances pathogen susceptibility. Cell 167, 1339–1353.e21 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • An, J. et al. Western-style diet impedes colonization and clearance of Citrobacter rodentium. PLoS Pathog. 17, e1009497 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Jimenez, A. G., Ellermann, M., Abbott, W. & Sperandio, V. Diet-derived galacturonic acid regulates virulence and intestinal colonization in enterohaemorrhagic Escherichia coli and Citrobacter rodentium. Nat. Microbiol. 5, 368–378 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • 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).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25, 402–408 (2001).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Patro, R., Duggal, G., Love, M. I., Irizarry, R. A. & Kingsford, C. Salmon provides fast and bias-aware quantification of transcript expression. Nat. Methods 14, 417–419 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

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

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Szklarczyk, D. et al. The STRING database in 2021: customizable protein-protein networks, and functional characterization of user-uploaded gene/measurement sets. Nucleic Acids Res. 49, D605–D612 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ewels, P., Magnusson, M., Lundin, S. & Käller, M. MultiQC: summarize analysis results for multiple tools and samples in a single report. Bioinformatics 32, 3047–3048 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Wood, D. E. & Salzberg, S. L. Kraken: ultrafast metagenomic sequence classification using exact alignments. Genome Biol. 15, R46 (2014).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

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

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Huang, W., Li, L., Myers, J. R. & Marth, G. T. ART: a next-generation sequencing read simulator. Bioinformatics 28, 593–594 (2012).

    Article 
    PubMed 

    Google Scholar
     

  • Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754–1760 (2009).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Li, H. et al. The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • McKenna, A. et al. The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297–1303 (2010).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Depristo, M. A. et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat. Genet. 43, 491–501 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841–842 (2010).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Cingolani, P. et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly 6, 80–92 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Sarovich, D. S. & Price, E. P. SPANDx: a genomics pipeline for comparative analysis of large haploid whole genome re-sequencing datasets. BMC Res. Notes 7, 618 (2014).

  • Song, L., Florea, L. & Langmead, B. Lighter: fast and memory-efficient sequencing error correction without counting. Genome Biol. 15, 509 (2014).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Magoč, T. & Salzberg, S. L. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27, 2957–2963 (2011).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Bankevich, A. et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19, 455–477 (2012).

    Article 
    MathSciNet 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Walker, B. J. et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS ONE 9, e112963 (2014).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Gurevich, A., Saveliev, V., Vyahhi, N. & Tesler, G. QUAST: quality assessment tool for genome assemblies. Bioinformatics 29, 1072–1075 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Larsen, M. V. et al. Multilocus sequence typing of total-genome-sequenced bacteria. J. Clin. Microbiol. 50, 1355–1361 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Jumper, J. et al. Highly accurate protein structure prediction with AlphaFold. Nature 596, 583–589 (2021).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Evans, R. et al. Protein complex prediction with AlphaFold-Multimer. Preprint at bioRxiv https://doi.org/10.1101/2021.10.04.463034 (2022).

  • Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797 (2004).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35, 1547–1549 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

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