Hostname: page-component-8448b6f56d-tj2md Total loading time: 0 Render date: 2024-04-19T07:45:11.368Z Has data issue: false hasContentIssue false

Capacity of the bovine intestinal mucus and its components to support growth of Escherichia coli O157:H7

Published online by Cambridge University Press:  10 March 2014

C. C. Aperce
Affiliation:
Department of Animal Sciences and Industry, Kansas State University, Call Hall, Manhattan, KS 66506-1600, USA
J. M. Heidenreich
Affiliation:
Department of Animal Sciences and Industry, Kansas State University, Call Hall, Manhattan, KS 66506-1600, USA
J. S. Drouillard*
Affiliation:
Department of Animal Sciences and Industry, Kansas State University, Call Hall, Manhattan, KS 66506-1600, USA
*
E-mail: jdrouill@ksu.edu
Get access

Abstract

Colonization of the gastrointestinal tract of cattle by Shiga toxin-producing Escherichia coli increases the risk of contamination of food products at slaughter. Our study aimed to shed more light on the mechanisms used by E. coli O157:H7 to thrive and compete with other bacteria in the gastrointestinal tract of cattle. We evaluated, in vitro, bovine intestinal mucus and its constituents in terms of their capacity to support growth of E. coli O157:H7 in presence or absence of fecal inoculum, with and without various enzymes. Growth of E. coli O157:H7 and total anaerobic bacteria were proportionate to the amount of mucus added as substrate. Growth of E. coli O157:H7 was similar for small and large intestinal mucus as substrate, and was partially inhibited with addition of fecal inoculum to cultures, presumably due to competition from other organisms. Whole mucus stimulated growth to the greatest degree compared with other compounds evaluated, but the pathogen was capable of utilizing all substrates to some extent. Addition of enzymes to cultures failed to impact growth of E. coli O157:H7 except for neuraminidase, which resulted in greater growth of E. coli O157 when combined with sialic acid as substrate. In conclusion, E. coli O157 has capacity to utilize small or large intestinal mucus, and growth is greatest with whole mucus compared with individual mucus components. There are two possible explanations for these findings (i) multiple substrates are needed to optimize growth, or alternatively, (ii) a component of mucus not evaluated in this experiment is a key ingredient for optimal growth of E. coli O157:H7.

Type
Full Paper
Copyright
© The Animal Consortium 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Atuma, C, Strugala, V, Allen, A and Holm, L 2001. The adherent gastrointestinal mucus gel layer: thickness and physical state in vivo . American Journal of Physiology-Gastrointestinal and Liver Physiology 280, 922929.Google Scholar
Bertin, Y, Chaucheyras-Durand, F, Robbe-Masselot, C, Durand, A, de la Foye, A, Harel, J, Cohen, PS, Conway, T, Forano, E and Martin, C 2013. Carbohydrate utilization by enterohaemorrhagic Escherichia coli O157:H7 in bovine intestinal content. Environmental Microbiology 15, 610622.Google Scholar
Chang, DE, Smalley, DJ, Tucker, DL, Leatham, MP, Norris, WE, Stevenson, SJ, Anderson, AB, Grissom, JE, Laux, DC, Cohen, PS and Conway, T 2004. Carbon nutrition of Escherichia coli in the mouse intestine. Proceedings of the National Academy of Sciences of the United States of America 101, 74277432.Google Scholar
Conway, T, Krogfelt, KA and Cohen, PS 2006. Escherichia coli at the intestinal mucosal surface. In Virulence mechanisms of bacterial pathogens (ed. KA Brogden, FC Minion, N Cornick, TB Stanton, Q Zhang, LK Nolan and MJ Wannemuehler), pp. 175196. ASM Press, Washington, DC.Google Scholar
Corfield, AP, Wagner, SA, Clamp, JR, Kriaris, MS and Hoskins, LC 1992. Mucin degradation in the human colon – production of sialidase, sialate O-acetylesterase, N-acetylneuraminate lyase, arylesterase, and glycosulfatase activities by strains of fecal bacteria. Infection and Immunity 60, 39713978.Google Scholar
Deplancke, B and Gaskins, HR 2001. Microbial modulation of innate defense: goblet cells and the intestinal mucus layer. American Journal of Clinical Nutrition 73, 1131S1141S.Google Scholar
Fabich, AJ, Jones, SA, Chowdhury, FZ, Cernosek, A, Anderson, A, Smalley, D, McHargue, JW, Hightower, GA, Smith, JT, Autieri, SM, Leatham, MP, Lins, JJ, Allen, RL, Laux, DC, Cohen, PS and Conway, T 2008. Comparison of carbon nutrition for pathogenic and commensal Escherichia coli strains in the mouse intestine. Infection and Immunity 76, 11431152.Google Scholar
Fox, JT, Drouillard, JS, Shi, X and Nagaraja, TG 2009. Effects of mucin and its carbohydrate constituents on Escherichia coli O157 growth in batch culture fermentations with ruminal or fecal microbial inoculum. Journal of Animal Science 87, 13041313.Google Scholar
Freitas, M, Axelsson, LG, Cayuela, C, Midtvedt, T and Trugnan, G 2002. Microbial-host interactions specifically control the glycosylation pattern in intestinal mouse mucosa. Histochemistry and Cell Biology 118, 149161.CrossRefGoogle ScholarPubMed
Freter, R 1988. Mechanisms of bacterial colonization of the mucosal surfaces of the gut. In Virulence mechanisms of bacterial pathogens (ed. JA Roth), pp. 4560. American Society of Microbiology, Washington, DC.Google Scholar
Hoskins, LC, Agustines, M, McKee, WB, Boulding, ET, Kriaris, M and Niedermeyer, G 1985. Mucin degradation in human-colon ecosystems – isolation and properties of fecal strains that degrade ABH blood-group antigens and oligosaccharides from mucin glycoproteins. Journal of Clinical Investigation 75, 944953.Google Scholar
Ihssen, J and Egli, T 2005. Global physiological analysis of carbon- and energy-limited growing Escherichia coli confirms a high degree of catabolic flexibility and preparedness for mixed substrate utilization. Environmental Microbiology 7, 15681581.Google Scholar
Jacob, ME, Fox, JT, Drouillard, JS, Renter, DG and Nagaraja, TG 2009. Evaluation of feeding dried distiller's grains with solubles and dry-rolled corn on the fecal prevalence of Escherichia coli O157:H7 and Salmonella spp. in cattle. Foodborne Pathogens and Disease 6, 145153.Google Scholar
Jacob, ME, Parsons, GL, Shelor, MK, Fox, JT, Drouillard, JS, Thomson, DU, Renter, DG and Nagaraja, TG 2008. Feeding supplemental dried distiller's grains increases faecal shedding of Escherichia coli O157 in experimentally inoculated calves. Zoonoses and Public Health 55, 125132.Google Scholar
Jones, SA, Jorgensen, M, Chowdhury, FZ, Rodgers, R, Hartline, J, Leatham, MP, Struve, C, Krogfelt, KA, Cohen, PS and Conway, T 2008. Glycogen and maltose utilization by Escherichia coli O157: H7 in the mouse intestine. Infection and Immunity 76, 25312540.Google Scholar
Malhotra, R and Singh, B 2006. Ethanol-induced changes in glycolipids of Saccharomyces cerevisiae . Applied Biochemistry and Biotechnology 128, 205213.Google Scholar
Mayer, C and Boos, W 2005. Hexose/pentose and hexitol/pentitol metabolism. In Escherichia coli and Salmonella: cellular and molecular biology (ed. R Curtis III and FC Neidhardt). ASM Press, Washington, DC.Google Scholar
McDougall, EI 1948. Studies on ruminant saliva, I. The composition and output of sheep’s saliva. Biochemical Journal 43, 99109.Google Scholar
Miranda, RL, Conway, T, Leatham, MP, Chang, DE, Norris, WE, Allen, JH, Stevenson, SJ, Laux, DC and Cohen, PS 2004. Glycolytic and gluconeogenic growth of Escherichia coli O157:H7 (EDL933) and E. coli K-12 (MG1655) in the mouse intestine. Infection and Immunity 72, 16661676.Google Scholar
Moller, AK, Leatham, MP, Conway, T, Nuijten, PJM, de Haan, LAM, Krogfelt, KA, Cohen, PS 2003. An Escherichia coli MG1655 lipopolysaccharide deep-rough core mutant grows and survives in mouse cecal mucus but fails to colonize the mouse large intestine. Infection and Immunity 71, 21422152.Google Scholar
Montagne, L, Toullec, R and Lalles, JP 2000. Calf intestinal mucin: isolation, partial characterization, and measurement in ileal digesta with an enzyme-linked immunoabsorbent assay. Journal of Dairy Science 83, 507517.Google Scholar
Naylor, SW, Low, JC, Besser, TE, Mahajan, A, Gunn, GJ, Pearce, MC, McKendrick, IJ, Smith, DGE and Gally, DL 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. Infection and Immunity 71, 15051512.Google Scholar
Robbe, C, Capon, C, Coddeville, B and Michalski, JC 2004. Structural diversity and specific distribution of O-glycans in normal human mucins along the intestinal tract. Biochemical Journal 384, 307316.Google Scholar
Sargeant, JM, Sanderson, MW, Smith, RA and Griffin, DD 2003. Escherichia coli O157 in feedlot cattle feces and water in four major feeder-cattle states in the USA. Preventive Veterinary Medicine 61, 127135.Google Scholar
Schamberger, GP, Phillips, RL, Jacobs, JL and Diez-Gonzalez, F 2004. Reduction of Escherichia coli O157:H7 populations in cattle by addition of colicin E7-producing E. coli to feed. Applied and Environmental Microbiology 70, 60536060.Google Scholar
Snider, TA, Fabich, AJ, Conway, T and Clinkenbeard, KD 2009. E. coli O157:H7 catabolism of intestinal mucin-derived carbohydrates and colonization. Veterinary Microbiology 136, 150154.Google Scholar
Tkalcic, S, Zhao, T, Harmon, BG, Doyle, MP, Brown, CA and Zhao, P 2003. Fecal shedding of enterohemorrhagic Escherichia coli in weaned calves following treatment with probiotic Escherichia coli . Journal of Food Protection 66, 11841189.Google Scholar
Undersander, D, Mertens, DR and Thiex, N 1993. Forage analysis procedures. National forage testing association, Omaha, Nebraska.Google Scholar