Unveiling the microbiome during post-partum uterine infection: a deep shotgun sequencing approach to characterize the dairy cow uterine microbiome

Abstract Background The goal of this study was to assess the microbial ecology and diversity present in the uterus of post-partum dairy cows with and without metritis from 24 commercial California dairy farms using shotgun metagenomics. A set subset of 95 intrauterine swab samples, taken from a larg...

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Main Authors: Carl Basbas, Adriana Garzon, Cory Schlesener, Machteld van Heule, Rodrigo Profeta, Bart C. Weimer, Noelia Silva-del-Rio, Barbara A. Byrne, Betsy Karle, Sharif S. Aly, Fabio S. Lima, Richard V. Pereira
Format: Article
Language:English
Published: BMC 2023-11-01
Series:Animal Microbiome
Subjects:
Online Access:https://doi.org/10.1186/s42523-023-00281-5
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author Carl Basbas
Adriana Garzon
Cory Schlesener
Machteld van Heule
Rodrigo Profeta
Bart C. Weimer
Noelia Silva-del-Rio
Barbara A. Byrne
Betsy Karle
Sharif S. Aly
Fabio S. Lima
Richard V. Pereira
author_facet Carl Basbas
Adriana Garzon
Cory Schlesener
Machteld van Heule
Rodrigo Profeta
Bart C. Weimer
Noelia Silva-del-Rio
Barbara A. Byrne
Betsy Karle
Sharif S. Aly
Fabio S. Lima
Richard V. Pereira
author_sort Carl Basbas
collection DOAJ
description Abstract Background The goal of this study was to assess the microbial ecology and diversity present in the uterus of post-partum dairy cows with and without metritis from 24 commercial California dairy farms using shotgun metagenomics. A set subset of 95 intrauterine swab samples, taken from a larger selection of 307 individual cow samples previously collected, were examined for α and β diversity and differential abundance associated with metritis. Cows within 21 days post-partum were categorized into one of three clinical groups during sample collection: control (CT, n = 32), defined as cows with either no vaginal discharge or a clear, non-purulent mucus vaginal discharge; metritis (MET, n = 33), defined as a cow with watery, red or brown colored, and fetid vaginal discharge; and purulent discharge cows (PUS, n = 31), defined as a non-fetid purulent or mucopurulent vaginal discharge. Results All three clinical groups (CT, MET, and PUS) were highly diverse, with the top 12 most abundant genera accounting for 10.3%, 8.8%, and 10.1% of mean relative abundance, respectively. The α diversity indices revealed a lower diversity from samples collected from MET and PUS when compared to CT cows. PERMANOVA statistical testing revealed a significant difference (P adjusted < 0.01) in the diversity of genera between CT and MET samples (R2 = 0.112, P = 0.003) and a non-significant difference between MET and PUS samples (R2 = 0.036, P = 0.046). ANCOM-BC analysis revealed that from the top 12 most abundant genera, seven genera were increased in the natural log fold change (LFC) of abundance in MET when compared to CT samples: Bacteroides, Clostridium, Fusobacterium, Phocaeicola, Porphyromonas, Prevotella, and Streptococcus. Two genera, Dietzia and Microbacterium, were decreased in natural LFC of abundance when comparing MET (regardless of treatment) and CT, while no changes in natural LFC of abundance were observed for Escherichia, Histophilus, and Trueperella. Conclusions The results presented here, are the current deepest shotgun metagenomic analyses conducted on the bovine uterine microbiome to date (mean of 256,425 genus-level reads per sample). Our findings support that uterine samples from cows without metritis (CT) had increased α-diversity but decreased β-diversity when compared to metritis or PUS cows, characteristic of dysbiosis. In summary, our findings highlight that MET cows have an increased abundance of Bacteroides, Porphyromonas, and Fusobacterium when compared to CT and PUS, and support the need for further studies to better understand their potential causal role in metritis pathogenesis.
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spelling doaj.art-2b766c4592554de4b6c5f39180add0dc2023-11-26T14:20:35ZengBMCAnimal Microbiome2524-46712023-11-015111810.1186/s42523-023-00281-5Unveiling the microbiome during post-partum uterine infection: a deep shotgun sequencing approach to characterize the dairy cow uterine microbiomeCarl Basbas0Adriana Garzon1Cory Schlesener2Machteld van Heule3Rodrigo Profeta4Bart C. Weimer5Noelia Silva-del-Rio6Barbara A. Byrne7Betsy Karle8Sharif S. Aly9Fabio S. Lima10Richard V. Pereira11Department of Population Health & Reproduction, School of Veterinary Medicine, University of CaliforniaDepartment of Population Health & Reproduction, School of Veterinary Medicine, University of CaliforniaDepartment of Population Health & Reproduction, School of Veterinary Medicine, University of CaliforniaDepartment of Population Health & Reproduction, School of Veterinary Medicine, University of CaliforniaDepartment of Population Health & Reproduction, School of Veterinary Medicine, University of CaliforniaDepartment of Population Health & Reproduction, School of Veterinary Medicine, University of CaliforniaDepartment of Population Health & Reproduction, School of Veterinary Medicine, University of CaliforniaDepartment of Pathology, Microbiology & Immunology, School of Veterinary Medicine, University of CaliforniaCooperative Extension, Division of Agriculture and Natural Resources, University of CaliforniaDepartment of Population Health & Reproduction, School of Veterinary Medicine, University of CaliforniaDepartment of Population Health & Reproduction, School of Veterinary Medicine, University of CaliforniaDepartment of Population Health & Reproduction, School of Veterinary Medicine, University of CaliforniaAbstract Background The goal of this study was to assess the microbial ecology and diversity present in the uterus of post-partum dairy cows with and without metritis from 24 commercial California dairy farms using shotgun metagenomics. A set subset of 95 intrauterine swab samples, taken from a larger selection of 307 individual cow samples previously collected, were examined for α and β diversity and differential abundance associated with metritis. Cows within 21 days post-partum were categorized into one of three clinical groups during sample collection: control (CT, n = 32), defined as cows with either no vaginal discharge or a clear, non-purulent mucus vaginal discharge; metritis (MET, n = 33), defined as a cow with watery, red or brown colored, and fetid vaginal discharge; and purulent discharge cows (PUS, n = 31), defined as a non-fetid purulent or mucopurulent vaginal discharge. Results All three clinical groups (CT, MET, and PUS) were highly diverse, with the top 12 most abundant genera accounting for 10.3%, 8.8%, and 10.1% of mean relative abundance, respectively. The α diversity indices revealed a lower diversity from samples collected from MET and PUS when compared to CT cows. PERMANOVA statistical testing revealed a significant difference (P adjusted < 0.01) in the diversity of genera between CT and MET samples (R2 = 0.112, P = 0.003) and a non-significant difference between MET and PUS samples (R2 = 0.036, P = 0.046). ANCOM-BC analysis revealed that from the top 12 most abundant genera, seven genera were increased in the natural log fold change (LFC) of abundance in MET when compared to CT samples: Bacteroides, Clostridium, Fusobacterium, Phocaeicola, Porphyromonas, Prevotella, and Streptococcus. Two genera, Dietzia and Microbacterium, were decreased in natural LFC of abundance when comparing MET (regardless of treatment) and CT, while no changes in natural LFC of abundance were observed for Escherichia, Histophilus, and Trueperella. Conclusions The results presented here, are the current deepest shotgun metagenomic analyses conducted on the bovine uterine microbiome to date (mean of 256,425 genus-level reads per sample). Our findings support that uterine samples from cows without metritis (CT) had increased α-diversity but decreased β-diversity when compared to metritis or PUS cows, characteristic of dysbiosis. In summary, our findings highlight that MET cows have an increased abundance of Bacteroides, Porphyromonas, and Fusobacterium when compared to CT and PUS, and support the need for further studies to better understand their potential causal role in metritis pathogenesis.https://doi.org/10.1186/s42523-023-00281-5Uterine microbiomeMicrobiotaMetritisDiversity
spellingShingle Carl Basbas
Adriana Garzon
Cory Schlesener
Machteld van Heule
Rodrigo Profeta
Bart C. Weimer
Noelia Silva-del-Rio
Barbara A. Byrne
Betsy Karle
Sharif S. Aly
Fabio S. Lima
Richard V. Pereira
Unveiling the microbiome during post-partum uterine infection: a deep shotgun sequencing approach to characterize the dairy cow uterine microbiome
Animal Microbiome
Uterine microbiome
Microbiota
Metritis
Diversity
title Unveiling the microbiome during post-partum uterine infection: a deep shotgun sequencing approach to characterize the dairy cow uterine microbiome
title_full Unveiling the microbiome during post-partum uterine infection: a deep shotgun sequencing approach to characterize the dairy cow uterine microbiome
title_fullStr Unveiling the microbiome during post-partum uterine infection: a deep shotgun sequencing approach to characterize the dairy cow uterine microbiome
title_full_unstemmed Unveiling the microbiome during post-partum uterine infection: a deep shotgun sequencing approach to characterize the dairy cow uterine microbiome
title_short Unveiling the microbiome during post-partum uterine infection: a deep shotgun sequencing approach to characterize the dairy cow uterine microbiome
title_sort unveiling the microbiome during post partum uterine infection a deep shotgun sequencing approach to characterize the dairy cow uterine microbiome
topic Uterine microbiome
Microbiota
Metritis
Diversity
url https://doi.org/10.1186/s42523-023-00281-5
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