Effect of maternal separation and transportation stress on the bovine upper respiratory tract microbiome and the immune response to resident opportunistic pathogens

Abstract Background The bovine upper respiratory tract (URT) microbiome includes opportunistic pathogens that cause respiratory disease and stress associated with maternal separation and transportation contributes to the severity of this respiratory disease. Stress is known to alter the gut microbio...

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Main Authors: Nilusha Malmuthuge, Angela Howell, Natasa Arsic, Tracy Prysliak, Jose Perez-Casal, Philip Griebel
Format: Article
Language:English
Published: BMC 2021-09-01
Series:Animal Microbiome
Subjects:
Online Access:https://doi.org/10.1186/s42523-021-00123-2
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spelling doaj-bcfb5cf3e6e141c7aa37d6b94c0d4b142021-09-26T11:37:56ZengBMCAnimal Microbiome2524-46712021-09-013111810.1186/s42523-021-00123-2Effect of maternal separation and transportation stress on the bovine upper respiratory tract microbiome and the immune response to resident opportunistic pathogensNilusha Malmuthuge0Angela Howell1Natasa Arsic2Tracy Prysliak3Jose Perez-Casal4Philip Griebel5Vaccine & Infectious Disease Organization – International Vaccine Centre (VIDO-InterVac), University of SaskatchewanVaccine & Infectious Disease Organization – International Vaccine Centre (VIDO-InterVac), University of SaskatchewanVaccine & Infectious Disease Organization – International Vaccine Centre (VIDO-InterVac), University of SaskatchewanVaccine & Infectious Disease Organization – International Vaccine Centre (VIDO-InterVac), University of SaskatchewanVaccine & Infectious Disease Organization – International Vaccine Centre (VIDO-InterVac), University of SaskatchewanVaccine & Infectious Disease Organization – International Vaccine Centre (VIDO-InterVac), University of SaskatchewanAbstract Background The bovine upper respiratory tract (URT) microbiome includes opportunistic pathogens that cause respiratory disease and stress associated with maternal separation and transportation contributes to the severity of this respiratory disease. Stress is known to alter the gut microbiome but little is known regarding the effect of stress on the URT microbiota. This study used six-month old suckling beef calves to investigate whether maternal separation (weaned), by itself or combined with transportation (weaned + transport), altered the URT microbiome and host immune responses to resident opportunistic pathogens. Results Taxonomic and functional composition of the URT microbiome in suckling and weaned beef calves did not change significantly when serially sampled over a one-month period. Subtle temporal changes in the URT microbiome composition were observed in weaned + transport calves. Total bacterial density was lower (p < 0.05) on day 4 post-weaning in both the weaned and weaned + transport groups when compared to suckling calves. In addition, significant (p < 0.05) temporal changes in the density of the opportunistic pathogens, M. haemolytica and P. multocida, were observed independent of treatment but these changes did not correlate with significantly increased (p < 0.05) serum antibody responses to both of these bacteria in the weaned and weaned + transport groups. Serum antibody responses to My. bovis, another opportunistic pathogen, remained unchanged in all treatment groups. Weaning, by itself and in combination with transportation, also had significant (p < 0.05) short- (2 to 8 days post-weaning) and long-term (28 days post-weaning) effects on the expression of adrenergic receptor genes in blood leukocytes when compared to age-matched suckling beef calves. Conclusions Maternal separation (weaning) and transportation has minor effects on the taxonomic and functional composition of the URT microbiome and temporal changes in the density of opportunistic pathogen residing in the URT did not correlate with significant changes in immune responses to these bacteria. Significant changes in adrenergic receptor expression in blood leukocytes following weaning, with or without transportation, suggests altered neuroimmune regulation should be further investigated as a mechanism by which stress can alter host-microbiome interactions for some opportunistic respiratory pathogens that reside in the URT.https://doi.org/10.1186/s42523-021-00123-2StressUpper respiratory tractMicrobiomeAdrenergic receptorsAntibody responseBovine
collection DOAJ
language English
format Article
sources DOAJ
author Nilusha Malmuthuge
Angela Howell
Natasa Arsic
Tracy Prysliak
Jose Perez-Casal
Philip Griebel
spellingShingle Nilusha Malmuthuge
Angela Howell
Natasa Arsic
Tracy Prysliak
Jose Perez-Casal
Philip Griebel
Effect of maternal separation and transportation stress on the bovine upper respiratory tract microbiome and the immune response to resident opportunistic pathogens
Animal Microbiome
Stress
Upper respiratory tract
Microbiome
Adrenergic receptors
Antibody response
Bovine
author_facet Nilusha Malmuthuge
Angela Howell
Natasa Arsic
Tracy Prysliak
Jose Perez-Casal
Philip Griebel
author_sort Nilusha Malmuthuge
title Effect of maternal separation and transportation stress on the bovine upper respiratory tract microbiome and the immune response to resident opportunistic pathogens
title_short Effect of maternal separation and transportation stress on the bovine upper respiratory tract microbiome and the immune response to resident opportunistic pathogens
title_full Effect of maternal separation and transportation stress on the bovine upper respiratory tract microbiome and the immune response to resident opportunistic pathogens
title_fullStr Effect of maternal separation and transportation stress on the bovine upper respiratory tract microbiome and the immune response to resident opportunistic pathogens
title_full_unstemmed Effect of maternal separation and transportation stress on the bovine upper respiratory tract microbiome and the immune response to resident opportunistic pathogens
title_sort effect of maternal separation and transportation stress on the bovine upper respiratory tract microbiome and the immune response to resident opportunistic pathogens
publisher BMC
series Animal Microbiome
issn 2524-4671
publishDate 2021-09-01
description Abstract Background The bovine upper respiratory tract (URT) microbiome includes opportunistic pathogens that cause respiratory disease and stress associated with maternal separation and transportation contributes to the severity of this respiratory disease. Stress is known to alter the gut microbiome but little is known regarding the effect of stress on the URT microbiota. This study used six-month old suckling beef calves to investigate whether maternal separation (weaned), by itself or combined with transportation (weaned + transport), altered the URT microbiome and host immune responses to resident opportunistic pathogens. Results Taxonomic and functional composition of the URT microbiome in suckling and weaned beef calves did not change significantly when serially sampled over a one-month period. Subtle temporal changes in the URT microbiome composition were observed in weaned + transport calves. Total bacterial density was lower (p < 0.05) on day 4 post-weaning in both the weaned and weaned + transport groups when compared to suckling calves. In addition, significant (p < 0.05) temporal changes in the density of the opportunistic pathogens, M. haemolytica and P. multocida, were observed independent of treatment but these changes did not correlate with significantly increased (p < 0.05) serum antibody responses to both of these bacteria in the weaned and weaned + transport groups. Serum antibody responses to My. bovis, another opportunistic pathogen, remained unchanged in all treatment groups. Weaning, by itself and in combination with transportation, also had significant (p < 0.05) short- (2 to 8 days post-weaning) and long-term (28 days post-weaning) effects on the expression of adrenergic receptor genes in blood leukocytes when compared to age-matched suckling beef calves. Conclusions Maternal separation (weaning) and transportation has minor effects on the taxonomic and functional composition of the URT microbiome and temporal changes in the density of opportunistic pathogen residing in the URT did not correlate with significant changes in immune responses to these bacteria. Significant changes in adrenergic receptor expression in blood leukocytes following weaning, with or without transportation, suggests altered neuroimmune regulation should be further investigated as a mechanism by which stress can alter host-microbiome interactions for some opportunistic respiratory pathogens that reside in the URT.
topic Stress
Upper respiratory tract
Microbiome
Adrenergic receptors
Antibody response
Bovine
url https://doi.org/10.1186/s42523-021-00123-2
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