Comparative Genomic Analyses of Lactococcus garvieae Isolated from Bovine Mastitis in China

ABSTRACT Lactococcus garvieae is an emerging zoonotic pathogen, but there are few reports regarding bovine mastitis. The prevalence of L. garvieae represents an increasing disease threat and global public health risk. Thirty-nine L. garvieae isolates were obtained from 2,899 bovine clinical mastitis...

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Main Authors: Yushan Lin, Jinge Han, Herman W. Barkema, Yue Wang, Jian Gao, John P. Kastelic, Bo Han, Shunyi Qin, Zhaoju Deng
Format: Article
Language:English
Published: American Society for Microbiology 2023-06-01
Series:Microbiology Spectrum
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/spectrum.02995-22
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author Yushan Lin
Jinge Han
Herman W. Barkema
Yue Wang
Jian Gao
John P. Kastelic
Bo Han
Shunyi Qin
Zhaoju Deng
author_facet Yushan Lin
Jinge Han
Herman W. Barkema
Yue Wang
Jian Gao
John P. Kastelic
Bo Han
Shunyi Qin
Zhaoju Deng
author_sort Yushan Lin
collection DOAJ
description ABSTRACT Lactococcus garvieae is an emerging zoonotic pathogen, but there are few reports regarding bovine mastitis. The prevalence of L. garvieae represents an increasing disease threat and global public health risk. Thirty-nine L. garvieae isolates were obtained from 2,899 bovine clinical mastitis milk samples in 6 provinces of China from 2017 to 2021. Five clonal complexes were determined from 32 multilocus sequence types (MLSTs) of L. garvieae: sequence type 46 (ST46) was the predominant sequence type, and 13 novel MLSTs were identified. All isolates were resistant to chloramphenicol and clindamycin, but susceptible to penicillin, ampicillin, amoxicillin-clavulanic acid, imipenem, ceftiofur, enrofloxacin, and marbofloxacin. Based on genomic analyses, L. garvieae had 6,310 genes, including 1,015 core, 3,641 accessory, and 1,654 unique genes. All isolates had virulence genes coding for collagenase, fibronectin-binding protein, glyceraldehyde-3-phosphate dehydrogenase, superoxide dismutase, and NADH oxidase. Most isolates had lsaD and mdtA antimicrobial resistance (AMR) genes. Based on COG (Clusters of Orthologous Genes database) results, the functions of defense, transcription and replication, and recombination and repair were enhanced in unique genes, whereas functions of translation, ribosomal structure, and biogenesis were enhanced in core genes. The KEGG functional categories enriched in unique genes included human disease and membrane transport, whereas COG functional categories enriched in core genes included energy metabolism, nucleotide metabolism, and translation. No gene was significantly associated with host specificity. In addition, analysis of core genome single nucleotide polymorphisms (SNPs) implied potential host adaptation of some isolates in several sequence types. In conclusion, this study characterized L. garvieae isolated from mastitis and detected potential adaptations of L. garvieae to various hosts. IMPORTANCE This study provides important genomic insights into a bovine mastitis pathogen, Lactococcus garvieae. Comprehensive genomic analyses of L. garvieae from dairy farms have not been reported. This study is a detailed and comprehensive report of novel features of isolates of L. garvieae, an important but poorly characterized bacterium, recovered in the past 5 years in 6 Chinese provinces. We documented diverse genetic features, including predominant sequence type ST46 and 13 novel MLSTs. Lactococcus garvieae had 6,310 genes, including 1,015 core, 3,641 accessory, and 1,654 unique genes. All isolates had virulence genes coding for collagenase, fibronectin-binding protein, glyceraldehyde-3-phosphate dehydrogenase, superoxide dismutase, and NADH oxidase and resistance to chloramphenicol and clindamycin. Most isolates had lsaD and mdtA antimicrobial resistance genes. However, no gene was significantly associated with host specificity. This is the first report that characterized L. garvieae isolates from bovine mastitis and revealed potential host adaptations of L. garvieae to various hosts.
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spelling doaj.art-4cdebb4dcf9e4c69b9d48baf3a6e257d2023-06-15T13:18:32ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972023-06-0111310.1128/spectrum.02995-22Comparative Genomic Analyses of Lactococcus garvieae Isolated from Bovine Mastitis in ChinaYushan Lin0Jinge Han1Herman W. Barkema2Yue Wang3Jian Gao4John P. Kastelic5Bo Han6Shunyi Qin7Zhaoju Deng8Department of Clinical Veterinary Medicine, College of Veterinary Medicine, China Agricultural University, Beijing, People’s Republic of ChinaCollege of Animal Science and Veterinary Medicine, Tianjin Agricultural University, Tianjin, People’s Republic of ChinaFaculty of Veterinary Medicine, University of Calgary, Calgary, Alberta, CanadaDepartment of Clinical Veterinary Medicine, College of Veterinary Medicine, China Agricultural University, Beijing, People’s Republic of ChinaDepartment of Clinical Veterinary Medicine, College of Veterinary Medicine, China Agricultural University, Beijing, People’s Republic of ChinaFaculty of Veterinary Medicine, University of Calgary, Calgary, Alberta, CanadaDepartment of Clinical Veterinary Medicine, College of Veterinary Medicine, China Agricultural University, Beijing, People’s Republic of ChinaCollege of Animal Science and Veterinary Medicine, Tianjin Agricultural University, Tianjin, People’s Republic of ChinaDepartment of Clinical Veterinary Medicine, College of Veterinary Medicine, China Agricultural University, Beijing, People’s Republic of ChinaABSTRACT Lactococcus garvieae is an emerging zoonotic pathogen, but there are few reports regarding bovine mastitis. The prevalence of L. garvieae represents an increasing disease threat and global public health risk. Thirty-nine L. garvieae isolates were obtained from 2,899 bovine clinical mastitis milk samples in 6 provinces of China from 2017 to 2021. Five clonal complexes were determined from 32 multilocus sequence types (MLSTs) of L. garvieae: sequence type 46 (ST46) was the predominant sequence type, and 13 novel MLSTs were identified. All isolates were resistant to chloramphenicol and clindamycin, but susceptible to penicillin, ampicillin, amoxicillin-clavulanic acid, imipenem, ceftiofur, enrofloxacin, and marbofloxacin. Based on genomic analyses, L. garvieae had 6,310 genes, including 1,015 core, 3,641 accessory, and 1,654 unique genes. All isolates had virulence genes coding for collagenase, fibronectin-binding protein, glyceraldehyde-3-phosphate dehydrogenase, superoxide dismutase, and NADH oxidase. Most isolates had lsaD and mdtA antimicrobial resistance (AMR) genes. Based on COG (Clusters of Orthologous Genes database) results, the functions of defense, transcription and replication, and recombination and repair were enhanced in unique genes, whereas functions of translation, ribosomal structure, and biogenesis were enhanced in core genes. The KEGG functional categories enriched in unique genes included human disease and membrane transport, whereas COG functional categories enriched in core genes included energy metabolism, nucleotide metabolism, and translation. No gene was significantly associated with host specificity. In addition, analysis of core genome single nucleotide polymorphisms (SNPs) implied potential host adaptation of some isolates in several sequence types. In conclusion, this study characterized L. garvieae isolated from mastitis and detected potential adaptations of L. garvieae to various hosts. IMPORTANCE This study provides important genomic insights into a bovine mastitis pathogen, Lactococcus garvieae. Comprehensive genomic analyses of L. garvieae from dairy farms have not been reported. This study is a detailed and comprehensive report of novel features of isolates of L. garvieae, an important but poorly characterized bacterium, recovered in the past 5 years in 6 Chinese provinces. We documented diverse genetic features, including predominant sequence type ST46 and 13 novel MLSTs. Lactococcus garvieae had 6,310 genes, including 1,015 core, 3,641 accessory, and 1,654 unique genes. All isolates had virulence genes coding for collagenase, fibronectin-binding protein, glyceraldehyde-3-phosphate dehydrogenase, superoxide dismutase, and NADH oxidase and resistance to chloramphenicol and clindamycin. Most isolates had lsaD and mdtA antimicrobial resistance genes. However, no gene was significantly associated with host specificity. This is the first report that characterized L. garvieae isolates from bovine mastitis and revealed potential host adaptations of L. garvieae to various hosts.https://journals.asm.org/doi/10.1128/spectrum.02995-22bovine mastitisLactococcus garvieaepopulation structurevirulence genesantimicrobial resistancehost adaptation
spellingShingle Yushan Lin
Jinge Han
Herman W. Barkema
Yue Wang
Jian Gao
John P. Kastelic
Bo Han
Shunyi Qin
Zhaoju Deng
Comparative Genomic Analyses of Lactococcus garvieae Isolated from Bovine Mastitis in China
Microbiology Spectrum
bovine mastitis
Lactococcus garvieae
population structure
virulence genes
antimicrobial resistance
host adaptation
title Comparative Genomic Analyses of Lactococcus garvieae Isolated from Bovine Mastitis in China
title_full Comparative Genomic Analyses of Lactococcus garvieae Isolated from Bovine Mastitis in China
title_fullStr Comparative Genomic Analyses of Lactococcus garvieae Isolated from Bovine Mastitis in China
title_full_unstemmed Comparative Genomic Analyses of Lactococcus garvieae Isolated from Bovine Mastitis in China
title_short Comparative Genomic Analyses of Lactococcus garvieae Isolated from Bovine Mastitis in China
title_sort comparative genomic analyses of lactococcus garvieae isolated from bovine mastitis in china
topic bovine mastitis
Lactococcus garvieae
population structure
virulence genes
antimicrobial resistance
host adaptation
url https://journals.asm.org/doi/10.1128/spectrum.02995-22
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