Comparison of Carbon Nutrition for Pathogenic and Commensal Escherichia coli Strains in the Mouse Intestine
Open accessAbstract
The carbon sources that support the growth of pathogenic Escherichia coli O157:H7 in the mammalian intestine have not previously been investigated. In vivo, the pathogenic E. coli EDL933 grows primarily as single cells dispersed within the mucus layer that overlies the mouse cecal epithelium. We therefore compared the pathogenic strain and the commensal E. coli strain MG1655 modes of metabolism in vitro, using a mixture of the sugars known to be present in cecal mucus, and found that the two strains used the 13 sugars in a similar order and cometabolized as many as 9 sugars at a time. We conducted systematic mutation analyses of E. coli EDL933 and E. coli MG1655 by using lesions in the pathways used for catabolism of 13 mucus-derived sugars and five other compounds for which the corresponding bacterial gene system was induced in the transcriptome of cells grown on cecal mucus. Each of 18 catabolic mutants in both bacterial genetic backgrounds was fed to streptomycin-treated mice, together with the respective wild-type parent strain, and their colonization was monitored by fecal plate counts. None of the mutations corresponding to the five compounds not found in mucosal polysaccharides resulted in colonization defects. Based on the mutations that caused colonization defects, we determined that both E. coli EDL933 and E. coli MG1655 used arabinose, fucose, and N -acetylglucosamine in the intestine. In addition, E. coli EDL933 used galactose, hexuronates, mannose, and ribose, whereas E. coli MG1655 used gluconate and N -acetylneuraminic acid. The colonization defects of six catabolic lesions were found to be additive with E. coli EDL933 but not with E. coli MG1655. The data indicate that pathogenic E. coli EDL933 uses sugars that are not used by commensal E. coli MG1655 to colonize the mouse intestine. The results suggest a strategy whereby invading pathogens gain advantage by simultaneously consuming several sugars that may be available because they are not consumed by the commensal intestinal microbiota.
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Different species of Enterobacteriaceae have a different order of nutrient preference.
“Different species of Enterobacteriaceae have different nutrient utilization profiles in aerobic and anaerobic environments and also have a different order of nutrient preference [79, 128].”
From Role of the gut microbiota in nutrient competition and protection against intestinal pathogen colonization (2023) · cites this paper as [128]
Different species of Enterobacteriaceae have different nutrient utilization profiles in aerobic and anaerobic environments.
“Different species of Enterobacteriaceae have different nutrient utilization profiles in aerobic and anaerobic environments and also have a different order of nutrient preference [79, 128].”
From Role of the gut microbiota in nutrient competition and protection against intestinal pathogen colonization (2023) · cites this paper as [128]
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Cites
One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products.
Datsenko, K., & Wanner, B. (2000) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.120163297 · Cited by 15,902 · see citing works
Exploration, normalization, and summaries of high density oligonucleotide array probe level data
Irizarry, R. A. (2003) · Biostatistics · doi:10.1093/biostatistics/4.2.249 · Cited by 10,603 · see citing works
Escherichia coli and Salmonella :cellular and molecular biology
Neidhardt, F. C. (1996) · ASM Press eBooks · Cited by 8,230 · see citing works
The complete genome sequence of Escherichia coli K-12.
Blattner, F., Plunkett, G., Bloch, C., Perna, N., Burland, V., Riley, M., Collado-Vides, J., Glasner, J. D., Rode, C., Mayhew, G., et al. (1997) · Science · doi:10.1126/science.277.5331.1453 · Cited by 7,996 · see citing works
Kaper, J. B., Nataro, J. P., & Mobley, H. L. T. (2004) · Nature Reviews Microbiology · doi:10.1038/nrmicro818 · Cited by 5,583 · see citing works
Culture Medium for Enterobacteria
Neidhardt, F. C., Bloch, P. L., & Smith, D. F. (1974) · Journal of Bacteriology · doi:10.1128/jb.119.3.736-747.1974 · Cited by 2,977 · see citing works
Genome sequence of enterohaemorrhagic Escherichia coli O157:H7
Perna, N. T., Plunkett, G., Burland, V., Mau, B., Glasner, J. D., Rose, D. J., Mayhew, G. F., Evans, P. S., Gregor, J., Kirkpatrick, H. A., et al. (2001) · Nature · doi:10.1038/35054089 · Cited by 2,035 · see citing works
Structural and sequence-based classification of glycoside hydrolases
Henrissat, B., & Davies, G. J. (1997) · Current Opinion in Structural Biology · doi:10.1016/s0959-440x(97)80072-3 · Cited by 1,668 · see citing works
Wolfe, A. J. (2005) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.69.1.12-50.2005 · Cited by 1,233 · see citing works
Kovárová, K., & Egli, T. W. (1998) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.62.3.646-666.1998 · Cited by 737 · see citing works
Rossi, M., Corradini, C., Amaretti, A., Nicolini, M., Pompei, A., Zanoni, S., & Matteuzzi, D. (2005) · Applied and Environmental Microbiology · doi:10.1128/aem.71.10.6150-6158.2005 · Cited by 546 · see citing works
Probiotics : the scientific basis
Fuller, R. (1992) · Cited by 544 · see citing works
Genetics of lipopolysaccharide biosynthesis in enteric bacteria
Schnaitman, C. A., & Klena, J. D. (1993) · Microbiological Reviews · doi:10.1128/mr.57.3.655-682.1993 · Cited by 523 · see citing works
Carbon nutrition of Escherichia coli in the mouse intestine
Chang, D., Smalley, D. J., Tucker, D. L., Leatham, M. P., Norris, W. E., Stevenson, S. J., Anderson, A. B., Grissom, J. E., Laux, D. C., Cohen, P. S., et al. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0307888101 · Cited by 513 · see citing works
Self-citationFermentation in the human large intestine and the available substrates
Cummings, J. H., & Englyst, H. N. (1987) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/45.5.1243 · Cited by 490 · see citing works
Human intestinal microflora in health and disease
(1985) · Food and Chemical Toxicology · doi:10.1016/0278-6915(85)90079-1 · Cited by 429 · see citing works
Virulence Mechanisms of Bacterial Pathogens
Kudva, I. T. (2016) · ASM Press eBooks · doi:10.1128/9781555819286 · Cited by 408 · see citing works
Tweeddale, H. J., McRobb, L. S., & Ferenci, T. (1998) · Journal of Bacteriology · doi:10.1128/jb.180.19.5109-5116.1998 · Cited by 393 · see citing works
Falony, G., Vlachou, A., Verbrugghe, K., & Vuyst, L. D. (2006) · Applied and Environmental Microbiology · doi:10.1128/aem.01296-06 · Cited by 362 · see citing works
Hoskins, L. C., Agustines, M., McKee, W. B., Boulding, E. T., Kriaris, M. S., & Niedermeyer, G. (1985) · Journal of Clinical Investigation · doi:10.1172/jci111795 · Cited by 322 · see citing works
What’s for Dinner?: Entner-Doudoroff Metabolism in Escherichia coli
Peekhaus, N. T., & Conway, T. (1998) · Journal of Bacteriology · doi:10.1128/jb.180.14.3495-3502.1998 · Cited by 289 · see citing works
Self-citationMucin Degradation in Human Colon Ecosystems
Hoskins, L. C., & Boulding, E. T. (1981) · Journal of Clinical Investigation · doi:10.1172/jci110009 · Cited by 277 · see citing works
Englyst, K. N., & Englyst, H. N. (2005) · British Journal Of Nutrition · doi:10.1079/bjn20051457 · Cited by 230 · see citing works
Respiration of <i>Escherichia coli</i> in the Mouse Intestine
Jones, S. A., Chowdhury, F. Z., Fabich, A. J., Anderson, A., Schreiner, D. M., House, A. L., Autieri, S. M., Leatham, M. P., Lins, J. J., Jorgensen, M., et al. (2007) · Infection and Immunity · doi:10.1128/iai.00484-07 · Cited by 223 · see citing works
Self-citationGlobal Transcriptional Programs Reveal a Carbon Source Foraging Strategy by Escherichia coli
Liu, M., Durfee, T., Cabrera, J. E., Zhao, K., Jin, D. J., & Blattner, F. R. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m414050200 · Cited by 209 · see citing works
Phosphoenolpyruvate:carbohydrate phosphotransferase systems
Postma, P. W., Lengeler, J. W., Jacobson, G. R., et al. (1996) · UvA-DARE (University of Amsterdam) · Cited by 190 · see citing works
Microarray expression profiling: capturing a genome‐wide portrait of the transcriptome
Conway, T., Gary, K., & Schoolnik (2003) · Molecular Microbiology · doi:10.1046/j.1365-2958.2003.03338.x · Cited by 181 · see citing works
Self-citationKinetics of the simultaneous utilization of sugar mixtures by Escherichia coli in continuous culture
Lendenmann, U., Snozzi, M., & Egli, T. W. (1996) · Applied and Environmental Microbiology · doi:10.1128/aem.62.5.1493-1499.1996 · Cited by 151 · see citing works
Mechanisms That Control the Microflora in the Large Intestine
Freter, R. (1983) · Elsevier eBooks · doi:10.1016/b978-0-12-341280-5.50008-2 · Cited by 148 · see citing works
Miranda, R. L., Conway, T., Leatham, M. P., Chang, D., Norris, W. E., Allen, J. H., Stevenson, S. J., Laux, D. C., & Cohen, P. S. (2004) · Infection and Immunity · doi:10.1128/iai.72.3.1666-1676.2004 · Cited by 133 · see citing works
Self-citationNutritional features and ecology of predominant anaerobic bacteria of the intestinal tract
Bryant, M. P. (1974) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/27.11.1313 · Cited by 124 · see citing works
Perry, M. B., MacLean, L. L., & Griffith, D. W. (1986) · Biochemistry and Cell Biology · doi:10.1139/o86-004 · Cited by 119 · see citing works
Factors affecting the microecology of the gut
Freter, R. (1992) · Springer eBooks · doi:10.1007/978-94-011-2364-8_6 · Cited by 119 · see citing works
Fraenkel, D. G. (1968) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)93160-1 · Cited by 113 · see citing works
Degradation of polysaccharides by intestinal bacterial enzymes
Salyers, A. A., Palmer, J. F., & Wilkins, T. D. (1978) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/31.10.s128 · Cited by 107 · see citing works
Schwaiger, H., Oefner, P. J., Huber, C. G., et al. (1994) · Electrophoresis · doi:10.1002/elps.11501501138 · Cited by 100 · see citing works
Ihssen, J., & Egli, T. W. (2005) · Environmental Microbiology · doi:10.1111/j.1462-2920.2005.00846.x · Cited by 99 · see citing works
Møller, A. K., Leatham, M. P., Conway, T., Nuijten, P. J. M., Haan, L. A. M., Krogfelt, K. A., & Cohen, P. S. (2003) · Infection and Immunity · doi:10.1128/iai.71.4.2142-2152.2003 · Cited by 95 · see citing works
Self-citationLeatham, M. P., Stevenson, S. J., Gauger, E. J., Krogfelt, K. A., Lins, J. J., Haddock, T. L., Autieri, S. M., Conway, T., & Cohen, P. S. (2005) · Infection and Immunity · doi:10.1128/iai.73.12.8039-8049.2005 · Cited by 93 · see citing works
Self-citationThe Life of Commensal Escherichia coli in the Mammalian Intestine
Conway, T., Krogfelt, K. A., & Cohen, P. S. (2004) · EcoSal Plus · doi:10.1128/ecosalplus.8.3.1.2 · Cited by 93 · see citing works
Self-citationColonization of Mucosal Surfaces
(2005) · ASM Press eBooks · doi:10.1128/9781555817619 · Cited by 87 · see citing works
Measurements of Fitness and Competition in CommensalEscherichia coliandE. coliO157:H7 Strains
Durso, L. M., Smith, D. R., & Hutkins, R. W. (2004) · Applied and Environmental Microbiology · doi:10.1128/aem.70.11.6466-6472.2004 · Cited by 83 · see citing works
Böck, A., & Neidhardt, F. C. (1966) · Journal of Bacteriology · doi:10.1128/jb.92.2.470-476.1966 · Cited by 66 · see citing works
Ho, T. D., & Waldor, M. K. (2006) · Infection and Immunity · doi:10.1128/iai.01342-06 · Cited by 60 · see citing works
Autieri, S. M., Lins, J. J., Leatham, M. P., Laux, D. C., Conway, T., & Cohen, P. S. (2007) · Infection and Immunity · doi:10.1128/iai.00822-07 · Cited by 54 · see citing works
Self-citationStroeher, U. H., Karageorgos, L., Brown, M. H., et al. (1995) · Gene · doi:10.1016/0378-1119(95)00589-0 · Cited by 49 · see citing works
Determination of colonization resistance of the digestive tract by biotyping of Enterobacteriaceae
Apperloo-Renkema, H. Z., van der Waaij, B. D., & van der Waaij, D. (1990) · Epidemiology and Infection · doi:10.1017/s0950268800047944 · Cited by 48 · see citing works
Hexose/Pentose and Hexitol/Pentitol Metabolism
Mayer, C., & Boos, W. (2005) · EcoSal Plus · doi:10.1128/ecosalplus.3.4.1 · Cited by 37 · see citing works
Lendenmann, U., Snozzi, M., & Egli, T. W. (2000) · Canadian Journal of Microbiology · doi:10.1139/cjm-46-1-72 · Cited by 35 · see citing works
Pultz, N. J., Hoskins, L. C., & Donskey, C. J. (2006) · Microbial Drug Resistance · doi:10.1089/mdr.2006.12.63 · Cited by 31 · see citing works
Role of the Mucus Layer in Bacterial Colonization of the Intestine
Laux, D. C., Cohen, P. S., & Conway, T. (2014) · ASM Press eBooks · doi:10.1128/9781555817619.ch15 · Cited by 30 · see citing works
Self-citationFlores, S., Flores, N., Anda, R. D., González, A., Escalante, A., Sigala, J., Gosset, G., & Bolívar, F. G. (2005) · Microbial Physiology · doi:10.1159/000090348 · Cited by 23 · see citing works
Wren, J. D., & Conway, T. (2006) · OMICS A Journal of Integrative Biology · doi:10.1089/omi.2006.10.15 · Cited by 17 · see citing works
Self-citationEscherichia coliat the Intestinal Mucosal Surface
Conway, T., & Cohen, P. S. (2007) · doi:10.1128/9781555815851.ch12 · Cited by 14 · see citing works
Self-citationZhao, G., Liu, J., Liu, X., et al. (2007) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2007.08.184 · Cited by 14 · see citing works
Flagged first, then by citations
Research works printed but not linked: 3
- [2]Autieri, S. M., J. J. Lins, M. P. Leatham, D. C. Laux, T. Conway, and P. S. Cohen. 2007. l-Fucose stimulates utilization of d-ribose by Escherichia coli MG1655 ΔfucAO and E. coli Nissle 1917 ΔfucAO mutants in the mouse intestine and in M9 minimal medium. Infect. Immun. 755465-5475. [DOI] [PMC free article] [PubMed] [Google Scholar]
- [12]Durso, L. M., D. Smith, and R. W. Hutkins. 2004. Measurements of fitness and competition in commensal Escherichia coli and E. coli O157:H7 strains. Appl. Environ Microbiol. 706466-6472. [DOI] [PMC free article] [PubMed] [Google Scholar]
- [21]Hentges, D. J., J. U. Que, S. W. Casey, and A. J. Stein. 1984. The influence of streptomycin on colonization in mice. Microecol. Theor. 1453-62. [Google Scholar]
Cited by
Sorted by citations
Role of the gut microbiota in immunity and inflammatory disease
Kamada, N., Seo, S.-U., Chen, G. Y., & Núñez, G. (2013) · Nature reviews. Immunology · doi:10.1038/nri3430 · Cited by 2,256 · see citing works
Control of pathogens and pathobionts by the gut microbiota
Kamada, N., Chen, G. Y., Inohara, N., & Núñez, G. (2013) · Nature Immunology · doi:10.1038/ni.2608 · Cited by 1,625 · see citing works
Interactions between the microbiota and pathogenic bacteria in the gut
Bäumler, A. J., & Sperandio, V. (2016) · Nature · doi:10.1038/nature18849 · Cited by 1,420 · see citing works
Microbiota-liberated host sugars facilitate post-antibiotic expansion of enteric pathogens
Ng, K. M., Ferreyra, J. A., Higginbottom, S. K., Lynch, J. B., Kashyap, P. C., Gopinath, S., Naidu, N., Choudhury, B., Weimer, B. C., Monack, D. M., et al. (2013) · Nature · doi:10.1038/nature12503 · Cited by 1,035 · see citing works
Mechanisms and consequences of intestinal dysbiosis
Weiss, G. A., & Hennet, T. (2017) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-017-2509-x · Cited by 775 · see citing works
The intestinal microbiota: Antibiotics, colonization resistance, and enteric pathogens
Kim, S., Covington, A., & Pamer, E. G. (2017) · Immunological Reviews · doi:10.1111/imr.12563 · Cited by 741 · see citing works
Gut Microbiota and Colonization Resistance against Bacterial Enteric Infection
Ducarmon, Q. R., Zwittink, R. D., Hornung, B. V. H., van Schaik, W., Young, V. B., & Kuijper, E. J. (2019) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00007-19 · Cited by 566 · see citing works
The outer mucus layer hosts a distinct intestinal microbial niche
Li, H., Limenitakis, J. P., Fuhrer, T., Geuking, M. B., Lawson, M. A., Wyss, M., Brugiroux, S., Keller, I., Macpherson, J. A., Rupp, S., et al. (2015) · Nature Communications · doi:10.1038/ncomms9292 · Cited by 511 · see citing works
Fucose sensing regulates bacterial intestinal colonization
Pacheco, A. R., Curtis, M. M., Ritchie, J. M., Munera, D., Waldor, M. K., Moreira, C. G., & Sperandio, V. (2012) · Nature · doi:10.1038/nature11623 · Cited by 499 · see citing works
Maltby, R., Leatham-Jensen, M. P., Gibson, T., Cohen, P. S., & Conway, T. (2013) · PLoS ONE · doi:10.1371/journal.pone.0053957 · Cited by 285 · see citing works
“hexuronates, mannose, N-acetylglucosamine, ribose, and sucrose for colonization [25].”
InfluentialSelf-citationZhang, C., Derrien, M., Levenez, F., Brazeilles, R., Ballal, S. A., Kim, J., Degivry, M.-C., Quéré, G., Garault, P., van Hylckama Vlieg, J. E. T., et al. (2016) · The ISME Journal · doi:10.1038/ismej.2016.13 · Cited by 264 · see citing works
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Unified Theory of Bacterial Sialometabolism: How and Why Bacteria Metabolize Host Sialic Acids
Vimr, E. R. (2013) · ISRN Microbiology · doi:10.1155/2013/816713 · Cited by 105 · see citing works
Horrocks, V., King, O. G., Yip, A. Y. G., Marques, I. M., & McDonald, J. A. K. (2023) · Microbiology · doi:10.1099/mic.0.001377 · Cited by 104 · see citing works
Rapid growth and metabolism of uropathogenic Escherichia coli in relation to urine composition
Reitzer, L., & Zimmern, P. (2019) · Clinical Microbiology Reviews · doi:10.1128/cmr.00101-19 · Cited by 85 · see citing works
Ostrem Loss, E., Thompson, J., Cheung, P. L. K., Qian, Y., & Venturelli, O. S. (2023) · Nature Ecology & Evolution · doi:10.1038/s41559-022-01930-9 · Cited by 38 · see citing works
The Interplay between the Microbiota and Enterohemorrhagic <i>Escherichia coli</i>
Pifer, R., & Sperandio, V. (2014) · Microbiology Spectrum · doi:10.1128/microbiolspec.ehec-0015-2013 · Cited by 32 · see citing works
Burin, R., & Shah, D. H. (2021) · Pathogens · doi:10.3390/pathogens10040469 · Cited by 5 · see citing works
- Authors
- Fabich, A. J., Jones, S. A., Chowdhury, F. Z., Cernosek, A., Anderson, A., Smalley, D., McHargue, J. W., Hightower, G. A., Smith, J. T., Autieri, S. M., Leatham, M. P., Lins, J. J., Allen, R. L., Laux, D. C., Cohen, P. S., & Conway, T.
- Affiliations
- University of Oklahoma (US)
- Southeastern Oklahoma State University (US)
- University of Rhode Island (US)
- Corresponding author
- Conway, Tyrrell
- Venue
- Infection and Immunity
- Publisher
- American Society for Microbiology
- Published
- 2008-03
- Volume
- 76
- Issue
- 3
- Pages
- 1143-1152
- ISSN
- 0019-9567 (ISSN-L)
- 1098-5522
- PMC
- PMC2258830
- OpenAlex
- W2096666146
- Cited by
- 380
- References
- 55
- Citations by year
- 2026: 15 · 2025: 18 · 2024: 25 · 2023: 18 · 2022: 28 · 2021: 25 · 2020: 31 · 2019: 29 · 2018: 24 · 2017: 21 · 2016: 21 · 2015: 30 · 2014: 21 · 2013: 21 · 2012: 9
- FWCI
- 9.07
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Infection and Immunity (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Journal of Media Literacy Education (submittedVersion, cc-by)
- Funders
- National Institutes of Health
- National Institute of Allergy and Infectious Diseases (R56AI048945, R01AI048945, AI48945)
- National Center for Research Resources (P20RR016478)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Escherichia coli research studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Keywords
- Escherichia coli O157:H7, commensal Escherichia coli, carbon source utilization, bacterial colonization, arabinose, fucose, N-acetylglucosamine, N-acetylneuraminic acid, mouse intestine, virulence
- MeSH terms
- Animals, Escherichia coli, Escherichia coli Infections, Feces, Intestines, Male, Colony Count, Microbial, Gene Deletion, Oligonucleotide Array Sequence Analysis, Gene Expression Profiling, Carbohydrate Metabolism, Mice, Metabolic Networks and Pathways
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