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Persistence of Brucella abortus lineages revealed by genomic characterization and phylodynamic analysis.

ABSTRACT: Brucellosis, caused by Brucella abortus, is a major disease of cattle and humans worldwide distributed. Eradication and control of the disease has been difficult in Central and South America, Central Asia, the Mediterranean and the Middle East. Epidemiological strategies combined with phylogenetic methods provide the high-resolution power needed to study relationships between surveillance data and pathogen population dynamics, using genetic diversity and spatiotemporal distributions. This information is crucial for prevention and control of disease spreading at a local and worldwide level. In Costa Rica (CR), the disease was first reported at the beginning of the 20th century and has not been controlled despite many efforts. We characterized 188 B. abortus isolates from CR recovered from cattle, humans and water buffalo, from 2003 to 2018, and whole genome sequencing (WGS) was performed in 95 of them. They were also assessed based on geographic origin, date of introduction, and phylogenetic associations in a worldwide and national context. Our results show circulation of five B. abortus lineages (I to V) in CR, phylogenetically related to isolates from the United States, United Kingdom, and South America. Lineage I was dominant and probably introduced at the end of the 19th century. Lineage II, represented by a single isolate from a water buffalo, clustered with a Colombian sample, and was likely introduced after 1845. Lineages III and IV were likely introduced during the early 2000s. Fourteen isolates from humans were found within the same lineage (lineage I) regardless of their geographic origin within the country. The main CR lineages, introduced more than 100 years ago, are widely spread throughout the country, in contrast to new introductions that seemed to be more geographically restricted. Following the brucellosis prevalence and the farming practices of several middle- and low-income countries, similar scenarios could be found in other regions worldwide.

SUBMITTER: Suarez-Esquivel M

PROVIDER: S-EPMC7182279 | biostudies-literature | 2020 Apr

REPOSITORIES: biostudies-literature

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Persistence of Brucella abortus lineages revealed by genomic characterization and phylodynamic analysis.

Suárez-Esquivel Marcela M Hernández-Mora Gabriela G Ruiz-Villalobos Nazareth N Barquero-Calvo Elías E Chacón-Díaz Carlos C Ladner Jason T JT Oviedo-Sánchez Gerardo G Foster Jeffrey T JT Rojas-Campos Norman N Chaves-Olarte Esteban E Thomson Nicholas R NR Moreno Edgardo E Guzmán-Verri Caterina C

PLoS neglected tropical diseases 20200414 4

Brucellosis, caused by Brucella abortus, is a major disease of cattle and humans worldwide distributed. Eradication and control of the disease has been difficult in Central and South America, Central Asia, the Mediterranean and the Middle East. Epidemiological strategies combined with phylogenetic methods provide the high-resolution power needed to study relationships between surveillance data and pathogen population dynamics, using genetic diversity and spatiotemporal distributions. This inform ...[more]

PMID: 32287327

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Project description:IntroductionBrucellosis, a serious public health issue affecting animals and humans, is neglected in West Africa (WA).MethodsIn the present study, bio-typing, multi-locus sequence typing (MLST), multiple-locus variable-number tandem repeat analysis (MLVA), and whole genome sequencing single-nucleotide polymorphism (WGS-SNP) analysis were used to characterize the Brucella abortus (B. abortus) strains from WA.ResultsAll of the 309 strains analyzed in this study were extracted and downloaded from the international MLVA bank and were from 10 hosts (cattle, humans, ovine, buffalo, dromedaries, horse, sheep, zebu, dog, and cat) distributed in 17 countries in WA. Based on the bio-typing, three biovars, dominated by B. abortus bv.3, were observed and reported across seven decades (1958-2019). With MLST, 129 B. abortus strains from the present study were sorted into 14 STs, with ST34 as the predicted founder. These 14 STs clustered into the global MLST data into three clone complexes (C I-C III) with the majority of strains clustering in C I, while C II forms an independent branch, and C III harbors three STs shared by different continents. These data revealed that most cases were caused by strains from native lineages. According to the MLVA-11 comparison, 309 strains were divided into 22 MLVA-11 genotypes, 15 of which were unique to WA and the remaining seven had a global distribution. MLVA-16 analysis showed that there were no epidemiological links among these strains. Based on the MLVA data, B. abortus strains from WA have high genetic diversity, and predominated genotypes were descended from a native lineage. While the MLVA-16 globally highlights that the dominant native and few introduced lineages (from Brazil, the USA, South Korea, Argentina, India, Italy, Portugal, the UK, Costa Rica, and China) co-driving the B. abortus ongoing prevalence in WA. The high-resolution SNP analysis implied the existence of introduced B. abortus lineages, which may be reasonably explained by the movement and trade of dominant hosts (cattle) and/or their products.DiscussionOur results indicated that B. abortus strains in WA consist of native and introduced strains that necessitate control such as vaccination, testing, slaughtering, and movement control by the relevant country authorities to reduce brucellosis in livestock.

Project description:As the causative agent of cattle brucellosis, Brucella abortus commonly exhibits smooth phenotype (by virtue of colony morphology) that is characteristically sensitive to specific Brucella phages, playing until recently a major role in taxonomical classification of the Brucella species by the phage typing approach. We previously reported the discrepancy between traditional phenotypic typing and MLVA results of a smooth phage-resistant (SPR) strain Bab8416 isolated from a 45-year-old custodial worker with brucellosis in a cattle farm. Here, we performed whole genome sequencing and further obtained a complete genome sequence of strain Bab8416 by a combination of multiple NGS technologies and routine PCR sequencing. The detailed genetic differences between B. abortus SPR Bab8416 and large smooth phage-sensitive (SPS) strains were investigated in a comprehensively comparative genomic study. The large indels between B. abortus SPS strains and Bab8416 showed possible divergence between two evolutionary branches at a far phylogenetic node. Compared to B. abortus SPS strain 9-941 (Bab9-941), the specific re-arrangement event in Bab8416 displaying a closer linear relationship with B. melitensis 16M than other B. abortus strains resulted in the truncation of c-di-GMP synthesis, and 3 c-di-GMP-metabolizing genes, were present in Bab8416 and B. melitensis 16M, but absent in Bab9-941 and other B. abortus strains, indicating potential SPR-associated key determinants and novel molecular mechanisms. Moreover, despite almost completely intact smooth LPS related genes, only one mutated OmpA family protein of Bab8416, functionally related to flagellar and efflux pump, was newly identified. Several point mutations were identified to be Bab8416 specific while a majority of them were verified to be B. abortus ST2 characteristic. In conclusion, our study therefore identifies new SPR-associated factors that could play a role in refining and updating Brucella taxonomic schemes and provides resources for further detailed analysis of mechanism for Brucella phage resistance.

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Persistence of Brucella abortus lineages revealed by genomic characterization and phylodynamic analysis.

Publications

Persistence of Brucella abortus lineages revealed by genomic characterization and phylodynamic analysis.

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