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Molecular Characteristics of Burkholderia pseudomallei Collected From Humans in Hainan, China.

ABSTRACT: Melioidosis is a common infectious disease in Southeast Asia and Northern Australia. In Hainan, several cases have been reported, but no systematic study has yet been done on the molecular epidemiology profiles of the organism. An investigation of the molecular epidemiology links and population structure of Burkholderia pseudomallei would help to better understand the clonally of the isolates and differences among them. In this study, multilocus variable-number tandem repeat analysis (MLVA), and multilocus sequence typing (MLST) were applied to examine the epidemiological relatedness and population structure of 166 B. pseudomallei isolates obtained during 2002-2014 in Hainan, China. Both the MLVA_4 and MLST approaches had high discriminatory power for this population, with diversity indices of 0.9899 and 0.9457, respectively. However, the MLVA_4 assay showed a higher discriminatory power than the MLST approach, and a variable-number tandem repeat (VNTR3 933) found by the MLVA approach was the most useful in discriminating strains from this province. A total of 166 strains yielded 99 MLVA_4 genotypes, of which 34 genotypes were shared by 101 isolates, for a clustering rate of 60.8% (101/166), which suggested that some cases may have a common source. Additionally, 65 isolates showed distinct genotypes, indicating that more than 39.2% (65/166) of melioidosis cases in Hainan had epidemiologically unrelated or sporadic characteristics. The 166 isolates were resolved into 48 STs, of which five STs (ST55, -70, -46, -50, and -58) were here found to be predominant. Phylogenetic analysis of 116 isolates conducted using the eBURST v3 segregated the 48 STs into eight groups with ST50 as predicted founder, and 21 STs were found to be singletons, which suggest that the strains in the Hainan region represent a high diversity of ST clones, indicating that many B. pseudomallei clone groups are endemic to this region. Moreover, ST50 had 5 SLV, 7 DLV, 6 TLV, and 29 satellite STs and formed a radial expansion pattern, suggesting that the melioidosis epidemic in this study was mainly caused by the clonal expansion of ST 50. Phylogenetic analysis on global scale suggests that China's isolates are closely related to isolates from Southeast Asia, particularly from Thailand and Malaysia.

SUBMITTER: Zhu X

PROVIDER: S-EPMC7223694 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Molecular Characteristics of <i>Burkholderia pseudomallei</i> Collected From Humans in Hainan, China.

Zhu Xiong X Chen Hai H Li Sha S Wang Li-Cheng LC Wu Duo-Rong DR Wang Xu-Ming XM Chen Ru-Shou RS Li Zhen-Jun ZJ Liu Zhi-Guo ZG

Frontiers in microbiology 20200507

Melioidosis is a common infectious disease in Southeast Asia and Northern Australia. In Hainan, several cases have been reported, but no systematic study has yet been done on the molecular epidemiology profiles of the organism. An investigation of the molecular epidemiology links and population structure of <i>Burkholderia pseudomallei</i> would help to better understand the clonally of the isolates and differences among them. In this study, multilocus variable-number tandem repeat analysis (MLV ...[more]

PMID: 32457710

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Project description:Brucellosis has been reported in several regions of Hainan Province, but the extent of the disease has not been fully elucidated. Conventional biotyping methods, multiple locus variable number tandem repeats analysis (MLVA), and single-nucleotide polymorphisms (SNPs) from draft genome sequencing were employed to characterize the strains. There were four biovars (Brucella melitensis bv. 1, 2, and 3 and Brucella suis bv. 3) detected, which showed that the biovar diversity of Brucella in Hainan is higher than in other areas of China. Both B. melitensis bv. 3 and B. suis bv. 3 were dominant species and showed epidemiology patterns that were compatible with both southern and northern China. Eight of MLVA-11 genotypes were known (31, 111, 116, 120, 136, 291, 297, and 345), and the remaining seven were novel (HN11-1 to HN11-7); these data showed that Brucella strains in this study had multiple geographic origins and exhibited characteristics of origin and evolution of co-existing imported and Hainan specific lineage. A total of 41 strains were found, belonging to 37 unique genotypes that each represented a single strain, which suggests that these strains were not directly related epidemiologically and indicates that the epidemic characteristics of human brucellosis in Hainan was dominated by sporadic strains. The high HGDI values were observed in MLVA-8, MLVA-11, and MLVA-16 among two species, suggesting considerable genetic diversity among these species. MST is characterized based on MLVA-16 that was found both throughout China and on a global level and showed that strains of this study had significant genetic differences with strains from many parts of the globe and seemingly represent a unique genetic lineage. Whole-genome SNP analysis showed that four B. melitensis were closely related to strains from China's northern provinces, and the source of infection was partly of human brucellosis in this province that may have been from these regions. The B. suis were closely related to strains from the United States, and further investigation of the transportation of animals, such as pigs, is needed to elucidate the origins of these strains.

Project description:Burkholderia pseudomallei is a Gram-negative soil-dwelling bacillus that causes melioidosis, a frequently fatal infectious disease, in tropical and subtropical regions. Previous studies have identified the overall genetic and evolutionary characteristics of B. pseudomallei on a global scale, including its origin and transmission routes. However, beyond its known hyperendemicity foci in northern Australia and Southeast Asia, the distribution and genetic characteristics of B. pseudomallei in most tropical regions remain poorly understood, including in southern China. Here, we sequenced the genomes of 122 B. pseudomallei strains collected from Hainan, an island in southern China, in 2002-2018, to investigate the population structure, relationships with global strains, local epidemiology, and virulence and antimicrobial-resistance factors. A phylogenetic analysis and hierarchical clustering divided the Hainan strains into nine phylogenic groups (PGs), 80 % of which were concentrated within five major groups (group 1: corresponding to minor sequence types [STs], 12.3 %; group 3: ST46 and ST50, 31.1 %; group 9: ST58, 13.1 %; group 11: ST55, 8.2 %; group 15: mainly ST658, 15.6%). A phylogenetic analysis that included global strains suggested that B. pseudomallei in Hainan originated from Southeast Asian countries, transmitted in multiple historical importation events. We also identified several mutual transmission events between Hainan and Southeast Asian countries in recent years, including three importation events from Thailand and Singapore to Hainan and three exportation events from Hainan to Singapore, Malaysia, and Taiwan island. A statistical analysis of the temporal distribution showed that the Hainan strains of groups 3, 9, and 15 have dominated the disease epidemic locally in the last 5 years. The spatial distribution of the Hainan strains demonstrated that some PGs are distributed in different cities on Hainan island, and by combining phylogenic and geographic distribution information, we detected 21 between-city transmission events, indicating its frequent local transmission. The detection of virulence factor genes showed that 56 % of the Hainan strains in group 1 encode a B. pseudomallei-specific adherence factor, boaB, confirming the specific pathogenic characteristics of the Hainan strains in group 1. An analysis of the antimicrobial-resistance potential of B. pseudomallei showed that various kinds of alterations were identified in clinically relevant antibiotic resistance factors, such as AmrR, PenA and PBP3, etc. Our results clarify the population structure, local epidemiology, and pathogenic characteristics of B. pseudomallei in Hainan, providing further insight into its regional and global transmission networks and improving our knowledge of its global phylogeography.

Dataset Information

Molecular Characteristics of Burkholderia pseudomallei Collected From Humans in Hainan, China.

Publications

Molecular Characteristics of <i>Burkholderia pseudomallei</i> Collected From Humans in Hainan, China.

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