Novel reusable animal model for comparative evaluation of in vivo growth and protein-expression of Escherichia coli O157 strains in the bovine rumen

Previously, we had demonstrated that Escherichia coli O157:H7 (O157) strain 86-24 expresses proteins involved in survival rather than virulence in vitro in rumen fluid from dairy cattle limit fed a maintenance diet. Here, we verified if this observation would be true for different O157 strains grown...

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Veröffentlicht in:PloS one 2022-05, Vol.17 (5), p.e0268645-e0268645
Hauptverfasser: Kudva, Indira T, Trachsel, Julian, Biernbaum, Erika N, Casey, Thomas
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Trachsel, Julian
Biernbaum, Erika N
Casey, Thomas
description Previously, we had demonstrated that Escherichia coli O157:H7 (O157) strain 86-24 expresses proteins involved in survival rather than virulence in vitro in rumen fluid from dairy cattle limit fed a maintenance diet. Here, we verified if this observation would be true for different O157 strains grown in vitro in rumen fluid from, and in vivo in the rumen of, animals on contrasting maintenance (high fiber) and lactation (high energy-protein) diets usually limit fed to dairy cattle. For the in vivo studies, an economical, novel, reusable and non-terminal rumen-fistulated animal model permitting simultaneous evaluation of multiple bacterial strains in the bovine rumen was developed. All experiments were conducted in duplicate using different animals to account for host-related variations. The O157 strains included, 86-24, EDL933 and the super shed SS-17. E. coli NalR (#5735), derived from a bovine intestinal commensal E. coli, was included as a control. As expected, diet influenced ruminal pH and volatile fatty acid (VFA) composition. The pH ranged from 6.2-7.0 and total VFA concentrations from 109-141 μM/ml, in animals fed the maintenance diet. In comparison, animals fed the lactation diet had a ruminal pH ranging between 5.18-6.0, and total VFA of 125-219 μM/ml. Strain dependent differences in O157 recovery from the rumen fluid of cattle fed either diet was observed, both in vitro and in vivo, with O157 strains 86-24 and EDL933 demonstrating similar survival patterns. Analysis of the O157 proteomes expressed in the rumen fluid/rumen verified previous observations of adaptive responses. Any difference in the adaptive response was mainly influenced by the animal's diet and growth conditions (in vitro and in vivo) and not the O157 strain. These new insights into the O157 responses could help formulate modalities to control O157 across strains in cattle at all stages of husbandry.
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Here, we verified if this observation would be true for different O157 strains grown in vitro in rumen fluid from, and in vivo in the rumen of, animals on contrasting maintenance (high fiber) and lactation (high energy-protein) diets usually limit fed to dairy cattle. For the in vivo studies, an economical, novel, reusable and non-terminal rumen-fistulated animal model permitting simultaneous evaluation of multiple bacterial strains in the bovine rumen was developed. All experiments were conducted in duplicate using different animals to account for host-related variations. The O157 strains included, 86-24, EDL933 and the super shed SS-17. E. coli NalR (#5735), derived from a bovine intestinal commensal E. coli, was included as a control. As expected, diet influenced ruminal pH and volatile fatty acid (VFA) composition. The pH ranged from 6.2-7.0 and total VFA concentrations from 109-141 μM/ml, in animals fed the maintenance diet. In comparison, animals fed the lactation diet had a ruminal pH ranging between 5.18-6.0, and total VFA of 125-219 μM/ml. Strain dependent differences in O157 recovery from the rumen fluid of cattle fed either diet was observed, both in vitro and in vivo, with O157 strains 86-24 and EDL933 demonstrating similar survival patterns. Analysis of the O157 proteomes expressed in the rumen fluid/rumen verified previous observations of adaptive responses. Any difference in the adaptive response was mainly influenced by the animal's diet and growth conditions (in vitro and in vivo) and not the O157 strain. These new insights into the O157 responses could help formulate modalities to control O157 across strains in cattle at all stages of husbandry.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>35617366</pmid><doi>10.1371/journal.pone.0268645</doi><tpages>e0268645</tpages><orcidid>https://orcid.org/0000-0001-6750-7867</orcidid><orcidid>https://orcid.org/0000-0003-2357-7737</orcidid><orcidid>https://orcid.org/0000000323577737</orcidid><orcidid>https://orcid.org/0000000167507867</orcidid><oa>free_for_read</oa></addata></record>
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identifier ISSN: 1932-6203
ispartof PloS one, 2022-05, Vol.17 (5), p.e0268645-e0268645
issn 1932-6203
1932-6203
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source MEDLINE; DOAJ Directory of Open Access Journals; Public Library of Science (PLoS) Journals Open Access; EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry
subjects Analysis
Animal experimentation
Animal husbandry
Animal lactation
Animal models
Animals
artificial membranes
Bacteria
BASIC BIOLOGICAL SCIENCES
Biology and Life Sciences
Cattle
cell membranes
Chemical composition
cytoplasm
Dairy cattle
Diet
Diet - veterinary
E coli
Economic models
Epidemics
Escherichia coli
Escherichia coli O157 - physiology
Evaluation
Experiments
Fatty acids
Fatty Acids, Volatile - analysis
Feces
Feces - microbiology
Feeds
Female
Food contamination & poisoning
Genetic aspects
Growth conditions
Hemodialysis
High protein diet
Identification and classification
In vivo methods and tests
Lactation
Maintenance
Medicine and Health Sciences
membrane metabolism
Models, Animal
nuclear membrane
outer membrane proteins
pH effects
Physical Sciences
Probiotics
Properties
protein expression
Proteins
Proteomes
Research and Analysis Methods
Rumen
Rumen - microbiology
Strains (organisms)
Survival
Virulence
title Novel reusable animal model for comparative evaluation of in vivo growth and protein-expression of Escherichia coli O157 strains in the bovine rumen
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