Increased microbiome diversity at the time of infection is associated with improved growth rates of pigs after co-infection with porcine reproductive and respiratory syndrome virus (PRRSV) and porcine circovirus type 2 (PCV2)
Abstract
Porcine reproductive and respiratory syndrome virus (PRRSV) and porcine circovirus type 2 (PCV2) are two of the most important pathogens affecting the swine industry worldwide. Co-infections are common on a global scale, resulting in pork production losses through reducing weight gain and causing respiratory disease in growing pigs. Our initial work demonstrated that the fecal microbiome was associated with clinical outcome of pigs 70 days post-infection (dpi) with PRRSV and PCV2. However, it remained uncertain if microbiome characteristics could predispose response to viral infection. The purpose of this study was to determine if microbiome characteristics present at the time of virus exposure were associated with outcome after co-infection. Using the Lawrence Livermore Microbial Detection Array, we profiled the microbiome in feces prior to infection from pigs identified retrospectively as having high or low growth rates after co-infection. High growth rate pigs had less severe interstitial pneumonia, reduced virus replication, and a significant increase in average daily weight gain throughout the study. At the level of the fecal microbiome, high growth rate pigs had increased microbial diversity on both a family and species level. Shifts in the microbiome composition of high growth rate pigs included reduced Methanobacteriaceae species, increased Ruminococcaceae species,more »
- Authors:
-
- Kansas State Univ., Manhattan, KS (United States). Dept. of Diagnostic Medicine/Pathobiology and College of Veterinary Medicine
- Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States). Physical and Life Sciences Directorate
- Kansas State Univ., Manhattan, KS (United States). Dept. of Diagnostic Medicine/Pathobiology, College of Veterinary Medicine and Kansas State Veterinary Diagnostic Lab.
- Publication Date:
- Research Org.:
- Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)
- Sponsoring Org.:
- USDOE; USDA; Kansas State Univ., Manhattan, KS (United States). National Bio and Agro-Defense Facility (NBAF)
- OSTI Identifier:
- 1438602
- Alternate Identifier(s):
- OSTI ID: 1549709
- Report Number(s):
- LLNL-JRNL-736694
Journal ID: ISSN 0378-1135
- Grant/Contract Number:
- AC52-07NA27344; 2013-68004-20362; 14ERD081
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Veterinary Microbiology
- Additional Journal Information:
- Journal Volume: 208; Journal Issue: C; Journal ID: ISSN 0378-1135
- Publisher:
- Elsevier
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES; Microbiome; Swine; Porcine reproductive and respiratory syndrome virus; Porcine circovirus type 2; Weight gain; Microbial diversity
Citation Formats
Ober, Rebecca A., Thissen, James B., Jaing, Crystal J., Cino-Ozuna, Ada G., Rowland, Raymond R. R., and Niederwerder, Megan C. Increased microbiome diversity at the time of infection is associated with improved growth rates of pigs after co-infection with porcine reproductive and respiratory syndrome virus (PRRSV) and porcine circovirus type 2 (PCV2). United States: N. p., 2017.
Web. doi:10.1016/j.vetmic.2017.06.023.
Ober, Rebecca A., Thissen, James B., Jaing, Crystal J., Cino-Ozuna, Ada G., Rowland, Raymond R. R., & Niederwerder, Megan C. Increased microbiome diversity at the time of infection is associated with improved growth rates of pigs after co-infection with porcine reproductive and respiratory syndrome virus (PRRSV) and porcine circovirus type 2 (PCV2). United States. https://doi.org/10.1016/j.vetmic.2017.06.023
Ober, Rebecca A., Thissen, James B., Jaing, Crystal J., Cino-Ozuna, Ada G., Rowland, Raymond R. R., and Niederwerder, Megan C. Fri .
"Increased microbiome diversity at the time of infection is associated with improved growth rates of pigs after co-infection with porcine reproductive and respiratory syndrome virus (PRRSV) and porcine circovirus type 2 (PCV2)". United States. https://doi.org/10.1016/j.vetmic.2017.06.023. https://www.osti.gov/servlets/purl/1438602.
@article{osti_1438602,
title = {Increased microbiome diversity at the time of infection is associated with improved growth rates of pigs after co-infection with porcine reproductive and respiratory syndrome virus (PRRSV) and porcine circovirus type 2 (PCV2)},
author = {Ober, Rebecca A. and Thissen, James B. and Jaing, Crystal J. and Cino-Ozuna, Ada G. and Rowland, Raymond R. R. and Niederwerder, Megan C.},
abstractNote = {Porcine reproductive and respiratory syndrome virus (PRRSV) and porcine circovirus type 2 (PCV2) are two of the most important pathogens affecting the swine industry worldwide. Co-infections are common on a global scale, resulting in pork production losses through reducing weight gain and causing respiratory disease in growing pigs. Our initial work demonstrated that the fecal microbiome was associated with clinical outcome of pigs 70 days post-infection (dpi) with PRRSV and PCV2. However, it remained uncertain if microbiome characteristics could predispose response to viral infection. The purpose of this study was to determine if microbiome characteristics present at the time of virus exposure were associated with outcome after co-infection. Using the Lawrence Livermore Microbial Detection Array, we profiled the microbiome in feces prior to infection from pigs identified retrospectively as having high or low growth rates after co-infection. High growth rate pigs had less severe interstitial pneumonia, reduced virus replication, and a significant increase in average daily weight gain throughout the study. At the level of the fecal microbiome, high growth rate pigs had increased microbial diversity on both a family and species level. Shifts in the microbiome composition of high growth rate pigs included reduced Methanobacteriaceae species, increased Ruminococcaceae species, and increased Streptococcaceae species when compared to low growth rate pigs. The results of the study indicate that both microbiome diversity and composition at the time of virus exposure may play a role in the subsequent response of pigs to PRRSV/PCV2 co-infection.},
doi = {10.1016/j.vetmic.2017.06.023},
journal = {Veterinary Microbiology},
number = C,
volume = 208,
place = {United States},
year = {Fri Aug 18 00:00:00 EDT 2017},
month = {Fri Aug 18 00:00:00 EDT 2017}
}
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Works referenced in this record:
Low gut microbiota diversity in early infancy precedes asthma at school age
journal, May 2014
- Abrahamsson, T. R.; Jakobsson, H. E.; Andersson, A. F.
- Clinical & Experimental Allergy, Vol. 44, Issue 6
Monitoring Bacterial Community of Human Gut Microbiota Reveals an Increase in Lactobacillus in Obese Patients and Methanogens in Anorexic Patients
journal, September 2009
- Armougom, Fabrice; Henry, Mireille; Vialettes, Bernard
- PLoS ONE, Vol. 4, Issue 9
Role of the Gut Microbiome in Obesity and Diabetes Mellitus
journal, October 2015
- Barlow, Gillian M.; Yu, Allen; Mathur, Ruchi
- Nutrition in Clinical Practice, Vol. 30, Issue 6
Characterization of Swine Infertility and Respiratory Syndrome (SIRS) Virus (Isolate ATCC VR-2332)
journal, April 1992
- Benfield, David A.; Nelson, Eric; Collins, James E.
- Journal of Veterinary Diagnostic Investigation, Vol. 4, Issue 2
Reduced diversity of the intestinal microbiota during infancy is associated with increased risk of allergic disease at school age
journal, September 2011
- Bisgaard, Hans; Li, Nan; Bonnelykke, Klaus
- Journal of Allergy and Clinical Immunology, Vol. 128, Issue 3
Evidence for a major QTL associated with host response to Porcine Reproductive and Respiratory Syndrome Virus challenge1
journal, June 2012
- Boddicker, N.; Waide, E. H.; Rowland, R. R. R.
- Journal of Animal Science, Vol. 90, Issue 6
Pathogenesis of porcine reproductive and respiratory syndrome virus
journal, June 2012
- Chand, Ranjni J.; Trible, Benjamin R.; Rowland, Raymond RR
- Current Opinion in Virology, Vol. 2, Issue 3
Identification of two auto-cleavage products of nonstructural protein 1 (nsp1) in porcine reproductive and respiratory syndrome virus infected cells: nsp1 function as interferon antagonist
journal, March 2010
- Chen, Z.; Lawson, S.; Sun, Z.
- Virology, Vol. 398, Issue 1
House dust exposure mediates gut microbiome Lactobacillus enrichment and airway immune defense against allergens and virus infection
journal, December 2013
- Fujimura, K. E.; Demoor, T.; Rauch, M.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 2
A microbial detection array (MDA) for viral and bacterial detection
journal, January 2010
- Gardner, Shea N.; Jaing, Crystal J.; McLoughlin, Kevin S.
- BMC Genomics, Vol. 11, Issue 1
Development of a real-time PCR method for Firmicutes and Bacteroidetes in faeces and its application to quantify intestinal population of obese and lean pigs
journal, November 2008
- Guo, X.; Xia, X.; Tang, R.
- Letters in Applied Microbiology, Vol. 47, Issue 5
Modulation of innate immune signaling by nonstructural protein 1 (nsp1) in the family Arteriviridae
journal, December 2014
- Han, Mingyuan; Yoo, Dongwan
- Virus Research, Vol. 194
The microbiota in adaptive immune homeostasis and disease
journal, July 2016
- Honda, Kenya; Littman, Dan R.
- Nature, Vol. 535, Issue 7610
Microbiota regulates immune defense against respiratory tract influenza A virus infection
journal, March 2011
- Ichinohe, T.; Pang, I. K.; Kumamoto, Y.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 13
Application of a pathogen microarray for the analysis of viruses and bacteria in clinical diagnostic samples from pigs
journal, April 2015
- Jaing, Crystal J.; Thissen, James B.; Gardner, Shea N.
- Journal of Veterinary Diagnostic Investigation, Vol. 27, Issue 3
Estimates of animal methane emissions
journal, September 1996
- Johnson, Donald E.; Ward, Gerald M.
- Environmental Monitoring and Assessment, Vol. 42, Issue 1-2
Effects of the Antibiotics Growth Promoter Tylosin on Swine Gut Microbiota
journal, May 2016
- Kim, Jungman; Guevarra, Robin Becina; Nguyen, Son Giang
- Journal of Microbiology and Biotechnology, Vol. 26, Issue 5
Associations among Organochlorine Pesticides, Methanobacteriales, and Obesity in Korean Women
journal, November 2011
- Lee, Hae-Sook; Lee, Je-Chul; Lee, In-Kyu
- PLoS ONE, Vol. 6, Issue 11
Human gut microbes associated with obesity
journal, December 2006
- Ley, Ruth E.; Turnbaugh, Peter J.; Klein, Samuel
- Nature, Vol. 444, Issue 7122
In-feed antibiotic effects on the swine intestinal microbiome
journal, January 2012
- Looft, T.; Johnson, T. A.; Allen, H. K.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 5
Obesity-associated gut microbiota is enriched in Lactobacillus reuteri and depleted in Bifidobacterium animalis and Methanobrevibacter smithii
journal, August 2011
- Million, M.; Maraninchi, M.; Henry, M.
- International Journal of Obesity, Vol. 36, Issue 6
Correlation between body mass index and gut concentrations of Lactobacillus reuteri, Bifidobacterium animalis, Methanobrevibacter smithii and Escherichia coli
journal, March 2013
- Million, M.; Angelakis, E.; Maraninchi, M.
- International Journal of Obesity, Vol. 37, Issue 11
Gut Mucosal Barrier Dysfunction, Microbial Dysbiosis, and Their Role in HIV-1 Disease Progression
journal, September 2016
- Mudd, Joseph C.; Brenchley, Jason M.
- Journal of Infectious Diseases, Vol. 214, Issue suppl 2
Vaccination with a Porcine Reproductive and Respiratory Syndrome (PRRS) Modified Live Virus Vaccine Followed by Challenge with PRRS Virus and Porcine Circovirus Type 2 (PCV2) Protects against PRRS but Enhances PCV2 Replication and Pathogenesis Compared to Results for Nonvaccinated Cochallenged Controls
journal, October 2015
- Niederwerder, Megan C.; Bawa, Bhupinder; Serão, Nick V. L.
- Clinical and Vaccine Immunology, Vol. 22, Issue 12
Microbiome associations in pigs with the best and worst clinical outcomes following co-infection with porcine reproductive and respiratory syndrome virus (PRRSV) and porcine circovirus type 2 (PCV2)
journal, May 2016
- Niederwerder, Megan C.; Jaing, Crystal J.; Thissen, James B.
- Veterinary Microbiology, Vol. 188
Current State of Knowledge on Porcine Circovirus Type 2-Associated Lesions
journal, June 2012
- Opriessnig, T.; Langohr, I.
- Veterinary Pathology, Vol. 50, Issue 1
The effect of high-fat diet on the composition of the gut microbiota in cloned and non-cloned pigs of lean and obese phenotype
journal, September 2013
- Pedersen, Rebecca; Andersen, Anders Daniel; Hermann-Bank, Marie Louise
- Gut Microbes, Vol. 4, Issue 5
Changes in the gut microbiota of cloned and non-cloned control pigs during development of obesity: gut microbiota during development of obesity in cloned pigs
journal, January 2013
- Pedersen, Rebecca; Andersen, Anders Daniel; Mølbak, Lars
- BMC Microbiology, Vol. 13, Issue 1
The Microbial Detection Array for Detection of Emerging Viruses in Clinical Samples - A Useful Panmicrobial Diagnostic Tool
journal, June 2014
- Rosenstierne, Maiken W.; McLoughlin, Kevin S.; Olesen, Majken Lindholm
- PLoS ONE, Vol. 9, Issue 6
Modulation of Systemic Immune Responses through Commensal Gastrointestinal Microbiota
journal, January 2013
- Schachtschneider, Kyle M.; Yeoman, Carl J.; Isaacson, Richard E.
- PLoS ONE, Vol. 8, Issue 1
Disease tolerance mediated by microbiome E. coli involves inflammasome and IGF-1 signaling
journal, October 2015
- Schieber, A. M. P.; Lee, Y. M.; Chang, M. W.
- Science, Vol. 350, Issue 6260
The gut microbiota plays a protective role in the host defence against pneumococcal pneumonia
journal, October 2015
- Schuijt, Tim J.; Lankelma, Jacqueline M.; Scicluna, Brendon P.
- Gut, Vol. 65, Issue 4
Microbiota and SCFA in Lean and Overweight Healthy Subjects
journal, January 2010
- Schwiertz, Andreas; Taras, David; Schäfer, Klaus
- Obesity, Vol. 18, Issue 1
Porcine circovirus type 2 (PCV2) infections: Clinical signs, pathology and laboratory diagnosis
journal, March 2012
- Segalés, Joaquim
- Virus Research, Vol. 164, Issue 1-2
Bacteria within the Gastrointestinal Tract Microbiota Correlated with Improved Growth and Feed Conversion: Challenges Presented for the Identification of Performance Enhancing Probiotic Bacteria
journal, February 2016
- Stanley, Dragana; Hughes, Robert J.; Geier, Mark S.
- Frontiers in Microbiology, Vol. 7
Antibody responses following vaccination versus infection in a porcine circovirus-type 2 (PCV2) disease model show distinct differences in virus neutralization and epitope recognition
journal, June 2012
- Trible, Benjamin R.; Ramirez, Alejandro; Suddith, Andrew
- Vaccine, Vol. 30, Issue 27
Lung-gut cross-talk: evidence, mechanisms and implications for the mucosal inflammatory diseases
journal, March 2016
- Tulic, M. K.; Piche, T.; Verhasselt, V.
- Clinical & Experimental Allergy, Vol. 46, Issue 4
An obesity-associated gut microbiome with increased capacity for energy harvest
journal, December 2006
- Turnbaugh, Peter J.; Ley, Ruth E.; Mahowald, Michael A.
- Nature, Vol. 444, Issue 7122
Microbial perspective on fiber utilization by swine.
journal, January 1997
- Varel, V. H.; Yen, J. T.
- Journal of Animal Science, Vol. 75, Issue 10
Influence of dietary fiber on xylanolytic and cellulolytic bacteria of adult pigs.
journal, January 1987
- Varel, V. H.; Robinson, I. M.; Jung, H. J.
- Applied and Environmental Microbiology, Vol. 53, Issue 1
Activity of Fiber-Degrading Microorganisms in the Pig Large Intestine
journal, August 1987
- Varel, V. H.
- Journal of Animal Science, Vol. 65, Issue 2
Human gut microbiota in obesity and after gastric bypass
journal, January 2009
- Zhang, H.; DiBaise, J. K.; Zuccolo, A.
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 7
Works referencing / citing this record:
Antimicrobial removal on piglets promotes health and higher bacterial diversity in the nasal microbiota
journal, April 2019
- Correa-Fiz, Florencia; Gonçalves dos Santos, José Maurício; Illas, Francesc
- Scientific Reports, Vol. 9, Issue 1
Comparative analysis of the fecal microbiota from different species of domesticated and wild suids
journal, September 2019
- Correa-Fiz, Florencia; Blanco-Fuertes, Miguel; Navas, Maria J.
- Scientific Reports, Vol. 9, Issue 1
Impacts of environmental complexity on respiratory and gut microbiome community structure and diversity in growing pigs
journal, September 2019
- Megahed, Ameer; Zeineldin, Mohamed; Evans, Kaleigh
- Scientific Reports, Vol. 9, Issue 1
Axiom Microbiome Array, the next generation microarray for high-throughput pathogen and microbiome analysis
journal, February 2019
- Thissen, James B.; Be, Nicholas A.; McLoughlin, Kevin
- PLOS ONE, Vol. 14, Issue 2
Antimicrobial removal on piglets promotes health and higher bacterial diversity in the nasal microbiota
journal, April 2019
- Correa-Fiz, Florencia; Gonçalves dos Santos, José Maurício; Illas, Francesc
- Scientific Reports, Vol. 9, Issue 1
Comparative analysis of the fecal microbiota from different species of domesticated and wild suids
journal, September 2019
- Correa-Fiz, Florencia; Blanco-Fuertes, Miguel; Navas, Maria J.
- Scientific Reports, Vol. 9, Issue 1
Impacts of environmental complexity on respiratory and gut microbiome community structure and diversity in growing pigs
journal, September 2019
- Megahed, Ameer; Zeineldin, Mohamed; Evans, Kaleigh
- Scientific Reports, Vol. 9, Issue 1
Axiom Microbiome Array, the next generation microarray for high-throughput pathogen and microbiome analysis
journal, February 2019
- Thissen, James B.; Be, Nicholas A.; McLoughlin, Kevin
- PLOS ONE, Vol. 14, Issue 2
Fecal Microbiota Transplantation Is Associated With Reduced Morbidity and Mortality in Porcine Circovirus Associated Disease
journal, July 2018
- Niederwerder, Megan C.; Constance, Laura A.; Rowland, Raymond R. R.
- Frontiers in Microbiology, Vol. 9
Change of Gut Microbiota in PRRSV-Resistant Pigs and PRRSV-Susceptible Pigs from Tongcheng Pigs and Large White Pigs Crossed Population upon PRRSV Infection
journal, June 2022
- Wang, Tengfei; Guan, Kaifeng; Su, Qiuju
- Animals, Vol. 12, Issue 12