Effects of Administration of Live or Inactivated Virulent Rhodococccus equi and Age on the Fecal Microbiome of Neonatal Foals

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Abstract

Background

Rhodococcus equi is an important pathogen of foals. Enteral administration of live, virulent R. equi during early life has been documented to protect against subsequent intrabronchial challenge with R. equi, indicating that enteral mucosal immunization may be protective. Evidence exists that mucosal immune responses develop against both live and inactivated micro-organisms. The extent to which live or inactivated R. equi might alter the intestinal microbiome of foals is unknown. This is an important question because the intestinal microbiome of neonates of other species is known to change over time and to influence host development. To our knowledge, changes in the intestinal microbiome of foals during early life have not been reported. Thus, the purpose of this study was to determine whether age (during the first month of life) or administration of either live virulent R. equi (at a dose reported to protect foals against subsequent intrabronchial challenge, viz., 1×10 ¹⁰ colony forming units [CFU]) or inactivated virulent R. equi (at higher doses, viz., 2×10 ¹⁰ and 1×10 ¹¹ [CFU]) altered the fecal microbiome of foals.

Methodology/Principal Findings

Fecal swab samples from 42 healthy foals after vaccination with low-dose inactivated R. equi (n = 9), high-dose inactivated R. equi (n = 10), live R. equi (n = 6), control with cholera toxin B (CTB, n = 9), and control without CTB (n = 8) were evaluated by 454-pyrosequencing of the 16S rRNA gene and by qPCR. No impact of treatment was observed among vaccinated foals; however, marked and significant differences in microbial communities and diversity were observed between foals at 30 days of age relative to 2 days of age.

Conclusions

The results suggest age-related changes in the fecal microbial population of healthy foals do occur, however, mucosal vaccination does not result in major changes of the fecal microbiome in foals.

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Most cited references 40

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Rhodococcus equi: an animal and human pathogen.

Natalie Prescott (1990)

Recent isolations of Rhodococcus equi from cavitatory pulmonary disease in patients with AIDS have aroused interest among medical microbiologists in this unusual organism. Earlier isolations from humans had also been in immunosuppressed patients following hemolymphatic tumors or renal transplantation. This organism has been recognized for many years as a cause of a serious pyogranulomatous pneumonia of young foals and is occasionally isolated from granulomatous lesions in several other species, in some cases following immunosuppression. The last decade has seen many advances in understanding of the epidemiology, pathogenesis, diagnosis, treatment, and immunity to infection in foals. The particular susceptibility of the foal is not understood but can be explained in part by a combination of heavy challenge through the respiratory route coinciding with declining maternally derived antibody in the absence of fully competent foal cellular immune mechanisms. R. equi is largely a soil organism but is widespread in the feces of herbivores. Its growth in soil is considerably improved by simple nutrients it obtains from herbivore manure. About one-third of human patients who have developed R. equi infections had contact in some way with herbivores or their manure. Others may have acquired infection from contact with soil or wild bird manure. R. equi is an intracellular parasite, which explains the typical pyogranulomatous nature of R. equi infections, the predisposition to infection in human patients with defective cell-mediated immune mechanisms, and the efficacy of antimicrobial drugs that penetrate phagocytic cells.

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The developing intestinal microbiome and its relationship to health and disease in the neonate.

R Murgas Torrazza, J Neu (2011)

The intestinal microbiota normally exists in a commensal and/or symbiotic relationship with the host. In the past few years, emerging technologies derived largely from the Human Genome Project have been applied to evaluating the intestinal microbiota and new discoveries using these techniques have prompted new initiatives such as the Human Microbiome Roadmap designed to evaluate the role of the intestinal microbiome in health and disease. In this review, we wish to focus on some new developments in this area and discuss some of the effects of medical manipulations such as antibiotics, probiotics, prebiotics and C-section versus vaginal delivery on the intestinal microbiota.

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Characterization of the fecal bacteria communities of forage-fed horses by pyrosequencing of 16S rRNA V4 gene amplicons.

Brittany Shepherd, William S. Swecker, Roderick V. Jensen … (2011)

The diversity of the equine fecal bacterial community was evaluated using pyrosequencing of 16S rRNA gene amplicons. Fecal samples were obtained from horses fed cool-season grass hay. Fecal bacteria were characterized by amplifying the V4 region of bacterial 16S rRNA gene. Of 5898 mean unique sequences, a mean of 1510 operational taxonomic units were identified in the four fecal samples. Equine fecal bacterial richness was higher than that reported in humans, but lower than that reported in either cattle feces or soil. Bacterial classified sequences were assigned to 16 phyla, of which 10 were present in all samples. The largest number of reads belonged to Firmicutes (43.7% of total bacterial sequences), Verrucomicrobia (4.1%), Proteobacteria (3.8%), and Bacteroidetes (3.7%). The less abundant Actinobacteria, Cyanobacteria, and TM7 phyla presented here have not been previously described in the gut contents or feces of horses. Unclassified sequences represented 38.1% of total bacterial sequences; therefore, the equine fecal microbiome diversity is likely greater than that described. This is the first study to characterize the fecal bacterial community in horses by the use of 16S rRNA gene amplicon pyrosequencing, expanding our knowledge of the fecal microbiota of forage-fed horses. © 2011 Federation of European Microbiological Societies. Published by Blackwell Publishing Ltd. All rights reserved.

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Author and article information

Contributors

Xiaofeng Ren: Role: Editor

Journal

Journal ID (nlm-ta): PLoS One

Journal ID (iso-abbrev): PLoS ONE

Journal ID (publisher-id): plos

Journal ID (pmc): plosone

Title: PLoS ONE

Publisher: Public Library of Science (San Francisco, USA )

ISSN (Electronic): 1932-6203

Publication date Collection: 2013

Publication date (Electronic): 13 June 2013

Volume: 8

Issue: 6

Electronic Location Identifier: e66640

Affiliations

[1 ]Equine Infectious Diseases Laboratory, Department of Large Animal Clinical Sciences, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, Texas, United States of America

[2 ]Gastrointestinal Laboratory, Small Animal Clinical Sciences, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, Texas, United States of America

[3 ]Molecular Research DNA Laboratory, Shallowater, Texas, United States of America

[4 ]National Center for Electron Beam Research and Department of Poultry Science, Texas A&M University, College Station, Texas, United States of America

Northeast Agricultural University, China

Author notes

* E-mail: ncohen@ 123456cvm.tamu.edu

Competing Interests: The authors declare that they had partial support for this work through an unrestricted gift from Boehringer-Ingelheim to our laboratory and a scholarship from Fort Dodge Animal Health/Pfizer Animal Health for Dr. Angela Bordin. This industry funding does not relate to or involve any patents, products in development, marketed products, or any other private or proprietary interests. The authors do not have any consultancy agreements with these companies, and none of this work pertains to products in development or produced by these companies. This funding does not alter the authors' adherence to all the PLOS ONE policies on sharing data and materials.

Conceived and designed the experiments: AIB JSS NDC. Performed the experiments: AIB MEM KBW SED NDC. Analyzed the data: JSS AIB NDC. Contributed reagents/materials/analysis tools: JMS JSS SED SP NDC. Wrote the paper: AIB JSS MEM JMS NDC.

Article

Publisher ID: PONE-D-13-08225

DOI: 10.1371/journal.pone.0066640

PMC ID: 3681940

PubMed ID: 23785508

SO-VID: a42db224-16fa-462c-8dc5-c79028ab4726

License:

This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

History

Date received : 22 February 2013

Date accepted : 8 May 2013

Page count

Pages: 17

Funding

This work was supported by the Link Equine Research Endowment at Texas A&M University with additional support provided by the Gastrointestinal Laboratory at Texas A&M University and Boehringer-Ingelheim Vetmedica. Dr. Bordin was supported by a fellowship from Fort Dodge Animal Health/Pfizer Animal Health. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Effects of Administration of Live or Inactivated Virulent Rhodococccus equi and Age on the Fecal Microbiome of Neonatal Foals

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Abstract

Background

Methodology/Principal Findings

Conclusions

Related collections

PLOS Climate

Most cited references 40

Rhodococcus equi: an animal and human pathogen.

The developing intestinal microbiome and its relationship to health and disease in the neonate.

Characterization of the fecal bacteria communities of forage-fed horses by pyrosequencing of 16S rRNA V4 gene amplicons.

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Journal

Affiliations

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History

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