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Genomic epidemiology and global diversity of the emerging bacterial pathogen Elizabethkingia anophelis.

ABSTRACT: Elizabethkingia anophelis is an emerging pathogen involved in human infections and outbreaks in distinct world regions. We investigated the phylogenetic relationships and pathogenesis-associated genomic features of two neonatal meningitis isolates isolated 5 years apart from one hospital in Central African Republic and compared them with Elizabethkingia from other regions and sources. Average nucleotide identity firmly confirmed that E. anophelis, E. meningoseptica and E. miricola represent demarcated genomic species. A core genome multilocus sequence typing scheme, broadly applicable to Elizabethkingia species, was developed and made publicly available (http://bigsdb.pasteur.fr/elizabethkingia). Phylogenetic analysis revealed distinct E. anophelis sublineages and demonstrated high genetic relatedness between the African isolates, compatible with persistence of the strain in the hospital environment. CRISPR spacer variation between the African isolates was mirrored by the presence of a large mobile genetic element. The pan-genome of E. anophelis comprised 6,880 gene families, underlining genomic heterogeneity of this species. African isolates carried unique resistance genes acquired by horizontal transfer. We demonstrated the presence of extensive variation of the capsular polysaccharide synthesis gene cluster in E. anophelis. Our results demonstrate the dynamic evolution of this emerging pathogen and the power of genomic approaches for Elizabethkingia identification, population biology and epidemiology.

SUBMITTER: Breurec S

PROVIDER: S-EPMC4961963 | biostudies-literature | 2016 Jul

REPOSITORIES: biostudies-literature

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Genomic epidemiology and global diversity of the emerging bacterial pathogen Elizabethkingia anophelis.

Breurec Sebastien S Criscuolo Alexis A Diancourt Laure L Rendueles Olaya O Vandenbogaert Mathias M Passet Virginie V Caro Valérie V Rocha Eduardo P C EP Touchon Marie M Brisse Sylvain S

Scientific reports 20160727

Elizabethkingia anophelis is an emerging pathogen involved in human infections and outbreaks in distinct world regions. We investigated the phylogenetic relationships and pathogenesis-associated genomic features of two neonatal meningitis isolates isolated 5 years apart from one hospital in Central African Republic and compared them with Elizabethkingia from other regions and sources. Average nucleotide identity firmly confirmed that E. anophelis, E. meningoseptica and E. miricola represent dema ...[more]

PMID: 27461509

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Project description:The incidence of Elizabethkingia anophelis bacteremia increased significantly in a tertiary hospital, Changhua Christian Hospital (CCH) since 2013. The infection density was 1.3 and 8.1 cases per 100,000 patient-days between 2005 and 2012 and 2013 and 2020, respectively (P < 0.05). During an outbreak investigation, a specific lineage of E. anophelis strains was identified by the pulsed-field gel electrophoresis analysis. To evaluate the evolution of the specific E. anophelis lineage, whole-genome sequencing was performed, and unique genomic features (GRs) were determined by comparative genomic analysis. The specific E. anophelis lineage was novel compared to worldwide strains ever reported by cg-MLST phylogenic and whole-genome comparative analysis. Multiplex PCR using primers designed from unique GRs were performed for prevalence screening among isolates from the CCH and nationwide isolates from the Taiwan surveillance of Antimicrobial Resistance (TSAR) Program. The proportion of the specific E. anophelis lineage increased from 7.9% (3/38) during 2005-2012 to 89.2% (223/250) during 2013-2020 (P < 0.05). Although E. anophelis usually confers resistance to multiple antibiotics with limited therapeutic options, the E. anophelis strains in the specific lineage had higher ciprofloxacin resistance (100% [226/226] versus 27.4% [17/62], P < 0.05) and was associated with a higher 14-day mortality rates (33.2% [37/226] versus 16.1% [10/62], P < 0.05) than other strains at CCH. A similarly increasing trend was also found in the national TSAR program during 2002-2018 (p for trend <0.05). We concluded that a novel lineage of E. anophelis strains has emerged dominantly in Taiwan. The genomic features are important for further investigations of epidemiology, resistance, virulence, and appropriate treatment. IMPORTANCE Elizabethkingia anophelis is an emerging multidrug resistant pathogen caused several global outbreaks recently. E. anophelis was frequently misidentified as E. meningoseptica in the past by conventional culture methods; therefore, the prevalence was often underestimated. Through revised identification, an increasing trend of E. anophelis infection was noted in a tertiary hospital and a dominant lineage of strains was recognized by genotyping. To our best knowledge, the dominant lineage of E. anophelis is novel in comparison to other worldwide strains by whole-genome comparative analysis and several unique genomic regions were found. The whole-genome sequencing data also demonstrated multiple putative virulence factors and genes associated with multidrug resistance. In our study, we identified a specially evolved E. anophelis in Taiwan with increasing nationwide dominance. This study will assist in further epidemiology surveillance and developing corresponsive infection control policies to restrain it potential of global dissemination.

Project description:Elizabethkingia anophelis bacteria encounter fluxes of iron in the midgut of mosquitoes, where they live as symbionts. They also establish bacteremia with severe clinical manifestations in humans, and live in water service lines in hospitals. In this study, we investigated the global gene expression responses of E. anophelis to iron fluxes in the midgut of female Anopheles stephensi mosquitoes fed sucrose or blood, and in iron-poor or iron-rich culture conditions. Of 3,686 transcripts revealed by RNAseq technology, 218 were upregulated while 112 were down-regulated under iron-poor conditions. Most of these differentially expressed genes were enriched in functional groups assigned within “biological process,” “cell component” and “molecular function” categories. E. anophelis possessed 4 iron/heme acquisition systems. Hemolysin gene expression was significantly repressed when cells were grown under iron-rich or high temperature (37℃) conditions. Furthermore, hemolysin gene expression was down-regulated after a blood meal, indicating that E. anophelis cells responded to excess iron and its associated physiological stress by limiting iron loading. By contrast, genes encoding respiratory chain proteins were up-regulated under iron-rich conditions, allowing these iron-containing proteins to chelate intracellular free iron. In vivo studies showed that growth of E. anophelis cells increased 3-fold in blood-fed mosquitoes over those in sucrose-fed ones. Deletion of aerobactin synthesis genes led to impaired cell growth in both iron-rich and iron-poor media. Mutants showed more susceptibility to H2O2 toxicity and less biofilm formation than did wild-type cells. Mosquitoes with E. anophelis experimentally colonized in their guts produced more eggs than did those treated with erythromycin or left unmanipulated, as controls. Results reveal that E. anophelis bacteria respond to varying iron concentration in the mosquito gut, harvest iron while fending off iron-associated stress, contribute to lysis of red blood cells, and positively influence mosquito host fecundity.

Dataset Information

Genomic epidemiology and global diversity of the emerging bacterial pathogen Elizabethkingia anophelis.

Publications

Genomic epidemiology and global diversity of the emerging bacterial pathogen Elizabethkingia anophelis.

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