Insights Into the Resistome of Bovine Clinical Mastitis Microbiome, a Key Factor in Disease Complication
Bovine clinical mastitis (CM) is one of the most prevalent diseases caused by a wide range of resident microbes. The emergence of antimicrobial resistance in CM bacteria is well-known, however, the genomic resistance composition (the resistome) at the microbiome-level is not well characterized. In t...
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doaj-767adc909fd3434181e0d02e28f6e7422020-11-25T03:31:22ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2020-06-011110.3389/fmicb.2020.00860520375Insights Into the Resistome of Bovine Clinical Mastitis Microbiome, a Key Factor in Disease ComplicationM. Nazmul Hoque0M. Nazmul Hoque1Arif Istiaq2Arif Istiaq3Rebecca A. Clement4Keylie M. Gibson5Otun Saha6Ovinu Kibria Islam7Ovinu Kibria Islam8Ruhshan Ahmed Abir9Munawar Sultana10AMAM Zonaed Siddiki11Keith A. Crandall12Keith A. Crandall13M. Anwar Hossain14Department of Microbiology, University of Dhaka, Dhaka, BangladeshDepartment of Gynecology, Obstetrics and Reproductive Health, Faculty of Veterinary Medicine and Animal Science, Bangabandhu Sheikh Mujibur Rahman Agricultural University, Gazipur, BangladeshDepartment of Microbiology, University of Dhaka, Dhaka, BangladeshDepartment of Developmental Neurobiology, Graduate School of Medical Sciences, Kumamoto University, Kumamoto, JapanComputational Biology Institute, Milken Institute School of Public Health, The George Washington University, Washington, DC, United StatesComputational Biology Institute, Milken Institute School of Public Health, The George Washington University, Washington, DC, United StatesDepartment of Microbiology, University of Dhaka, Dhaka, BangladeshDepartment of Microbiology, University of Dhaka, Dhaka, BangladeshDepartment of Microbiology, Jashore University of Science and Technology, Jashore, BangladeshBio-Bio-1, Bioinformatics Research Foundation, Dhaka, BangladeshDepartment of Microbiology, University of Dhaka, Dhaka, BangladeshDepartment of Pathology and Parasitology, Chittagong Veterinary and Animal Sciences University, Chittagong, BangladeshComputational Biology Institute, Milken Institute School of Public Health, The George Washington University, Washington, DC, United StatesDepartment of Biostatistics and Bioinformatics, Milken Institute School of Public Health, The George Washington University, Washington, DC, United StatesDepartment of Microbiology, University of Dhaka, Dhaka, BangladeshBovine clinical mastitis (CM) is one of the most prevalent diseases caused by a wide range of resident microbes. The emergence of antimicrobial resistance in CM bacteria is well-known, however, the genomic resistance composition (the resistome) at the microbiome-level is not well characterized. In this study, we applied whole metagenome sequencing (WMS) to characterize the resistome of the CM microbiome, focusing on antibiotics and metals resistance, biofilm formation (BF), and quorum sensing (QS) along with in vitro resistance assays of six selected pathogens isolated from the same CM samples. The WMS generated an average of 21.13 million reads (post-processing) from 25 CM samples that mapped to 519 bacterial strains, of which 30.06% were previously unreported. We found a significant (P = 0.001) association between the resistomes and microbiome composition with no association with cattle breed, despite significant differences in microbiome diversity among breeds. The in vitro investigation determined that 76.2% of six selected pathogens considered “biofilm formers” actually formed biofilms and were also highly resistant to tetracycline, doxycycline, nalidixic acid, ampicillin, and chloramphenicol and remained sensitive to metals (Cr, Co, Ni, Cu, Zn) at varying concentrations. We also found bacterial flagellar movement and chemotaxis, regulation and cell signaling, and oxidative stress to be significantly associated with the pathophysiology of CM. Thus, identifying CM microbiomes, and analyzing their resistomes and genomic potentials will help improve the optimization of therapeutic schemes involving antibiotics and/or metals usage in the prevention and control of bovine CM.https://www.frontiersin.org/article/10.3389/fmicb.2020.00860/fullwhole metagenome sequencingclinical mastitismicrobiomeresistomein vitro resistance assays |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
M. Nazmul Hoque M. Nazmul Hoque Arif Istiaq Arif Istiaq Rebecca A. Clement Keylie M. Gibson Otun Saha Ovinu Kibria Islam Ovinu Kibria Islam Ruhshan Ahmed Abir Munawar Sultana AMAM Zonaed Siddiki Keith A. Crandall Keith A. Crandall M. Anwar Hossain |
spellingShingle |
M. Nazmul Hoque M. Nazmul Hoque Arif Istiaq Arif Istiaq Rebecca A. Clement Keylie M. Gibson Otun Saha Ovinu Kibria Islam Ovinu Kibria Islam Ruhshan Ahmed Abir Munawar Sultana AMAM Zonaed Siddiki Keith A. Crandall Keith A. Crandall M. Anwar Hossain Insights Into the Resistome of Bovine Clinical Mastitis Microbiome, a Key Factor in Disease Complication Frontiers in Microbiology whole metagenome sequencing clinical mastitis microbiome resistome in vitro resistance assays |
author_facet |
M. Nazmul Hoque M. Nazmul Hoque Arif Istiaq Arif Istiaq Rebecca A. Clement Keylie M. Gibson Otun Saha Ovinu Kibria Islam Ovinu Kibria Islam Ruhshan Ahmed Abir Munawar Sultana AMAM Zonaed Siddiki Keith A. Crandall Keith A. Crandall M. Anwar Hossain |
author_sort |
M. Nazmul Hoque |
title |
Insights Into the Resistome of Bovine Clinical Mastitis Microbiome, a Key Factor in Disease Complication |
title_short |
Insights Into the Resistome of Bovine Clinical Mastitis Microbiome, a Key Factor in Disease Complication |
title_full |
Insights Into the Resistome of Bovine Clinical Mastitis Microbiome, a Key Factor in Disease Complication |
title_fullStr |
Insights Into the Resistome of Bovine Clinical Mastitis Microbiome, a Key Factor in Disease Complication |
title_full_unstemmed |
Insights Into the Resistome of Bovine Clinical Mastitis Microbiome, a Key Factor in Disease Complication |
title_sort |
insights into the resistome of bovine clinical mastitis microbiome, a key factor in disease complication |
publisher |
Frontiers Media S.A. |
series |
Frontiers in Microbiology |
issn |
1664-302X |
publishDate |
2020-06-01 |
description |
Bovine clinical mastitis (CM) is one of the most prevalent diseases caused by a wide range of resident microbes. The emergence of antimicrobial resistance in CM bacteria is well-known, however, the genomic resistance composition (the resistome) at the microbiome-level is not well characterized. In this study, we applied whole metagenome sequencing (WMS) to characterize the resistome of the CM microbiome, focusing on antibiotics and metals resistance, biofilm formation (BF), and quorum sensing (QS) along with in vitro resistance assays of six selected pathogens isolated from the same CM samples. The WMS generated an average of 21.13 million reads (post-processing) from 25 CM samples that mapped to 519 bacterial strains, of which 30.06% were previously unreported. We found a significant (P = 0.001) association between the resistomes and microbiome composition with no association with cattle breed, despite significant differences in microbiome diversity among breeds. The in vitro investigation determined that 76.2% of six selected pathogens considered “biofilm formers” actually formed biofilms and were also highly resistant to tetracycline, doxycycline, nalidixic acid, ampicillin, and chloramphenicol and remained sensitive to metals (Cr, Co, Ni, Cu, Zn) at varying concentrations. We also found bacterial flagellar movement and chemotaxis, regulation and cell signaling, and oxidative stress to be significantly associated with the pathophysiology of CM. Thus, identifying CM microbiomes, and analyzing their resistomes and genomic potentials will help improve the optimization of therapeutic schemes involving antibiotics and/or metals usage in the prevention and control of bovine CM. |
topic |
whole metagenome sequencing clinical mastitis microbiome resistome in vitro resistance assays |
url |
https://www.frontiersin.org/article/10.3389/fmicb.2020.00860/full |
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