Comprehensive Analysis Reveals Two Distinct Evolution Patterns of Salmonella Flagellin Gene Clusters

Liu, Yue; Zhang, Dao‐Feng; Zhou, Xiujuan; Xu, Li; Zhang, Lida; Shi, Xianming

doi:10.3389/fmicb.2017.02604

Cited by 12 publications

(14 citation statements)

References 53 publications

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“…Our analysis is in accordance to the data of Liu et al (2017) that the PCR systems based on the eight selected flagellin and flagellin related gene sequences can be applicable for the detection of Infantis serovar; however, some exceptions are possible. Accordingly, in case of 76 S. Infantis genomes, this analysis mainly corresponds to the results of "conventional" 1 http://enterobase.warwick.ac.uk/species/index/senterica serovar classification.…”

Section: Discussionsupporting

confidence: 89%

“…The serovar-marker flagellin gene fljB of S. Infantis was identified according to Kardos et al (2007). The flagellin genes fljA, fljB, fliA, fliB, fliC, fliD, fliS, and hin were identified based on sequences of the reference strain (Liu et al, 2017). For in silico prediction of the serovar and clonal identity of the strains, the web-based softwares SeqSero and MLST were used (Larsen et al, 2012;Zhang et al, 2015).…”

Section: Bioinformatics and Phylogenetic Analysismentioning

confidence: 99%

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Comparative Genome Analysis of Hungarian and Global Strains of Salmonella Infantis

et al. 2020

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Introduction: The emergence and spread of new strains of zoonotic bacteria, such as multidrug resistant (MDR) Salmonella Infantis, represent a growing health risk for humans in and outside Europe due to foodborne infections of poultry meat origin. Objectives: In order to understand genome relations of S. Infantis strains from Hungary and from different geographic regions, we performed a comprehensive genome analysis of nine Hungarian and 67 globally selected strains of S. Infantis and 26 Salmonella strains representing 13 non-Infantis serovars. Results: Analyses of whole-, and accessory genomes, showed that almost all S. Infantis strains were separated from the non-Infantis serovars. S. Infantis strains from Hungary formed subclusters based on their time of isolation. In whole genome sequence analysis, the Swiss strains of S. Infantis were closely related to each other and clustered together with subclusters of strains from Hungary, Japan, Italy, United States, and Israel. The accessory genome analysis revealed that the Swiss strains were distinct from most of the strains investigated, including the Hungarian ones. Analysis of the cloud genes offered the most detailed insight into the genetic distance and relationship of S. Infantis strains confirming that the Swiss and Hungarian strains belonged to different lineages. As expected, core genome analysis provided the least discriminatory power for analysis of S. Infantis. Genomic sequences of nine strains from Brazil, Israel, Mexico, Nigeria, and Senegal (deposited as S. Infantis) proved to be outliers from the S. Infantis clade. They were predicted to be Salmonella Rissen, Salmonella Ouakarm, Salmonella Kentucky, Salmonella Thompson, and Salmonella enterica subsp. diarizonae. Conclusion: Accessory genome of S. Infantis showed the highest diversity suggesting a faster evolution than that of the whole genomes contributing to the emergence of multiple genetic variants of S. Infantis worldwide. Accordingly, in spite of the comprehensive analysis of several genomic characteristics, no epidemiologic links between these S. Infantis strains from different countries could be established. It is also concluded that several strains originally designated as S. Infantis need in databanks reclassification.

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Section: Discussionsupporting

confidence: 89%

Section: Bioinformatics and Phylogenetic Analysismentioning

confidence: 99%

Comparative Genome Analysis of Hungarian and Global Strains of Salmonella Infantis

et al. 2020

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“…3b). The flagellin gene fliC encodes the Salmonella phase 1 antigen and, along with fliB (which encodes the phase 2 antigen), is considered a Salmonella serotype determinant gene (38). Flagellin genes contribute to ecological adaptation of Salmonella by allowing the cell to adjust their expression through phase variation when it encounters a new niche (39) and in the generation of new serotypes (40).…”

Section: Resultsmentioning

confidence: 99%

Distinct but Intertwined Evolutionary Histories of Multiple Salmonella enterica Subspecies

Park

Andam

2020

mSystems

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Salmonella is responsible for many nontyphoidal foodborne infections and enteric (typhoid) fever in humans. Of the two Salmonella species, Salmonella enterica is highly diverse and includes 10 known subspecies and approximately 2,600 serotypes. Understanding the evolutionary processes that generate the tremendous diversity in Salmonella is important in reducing and controlling the incidence of disease outbreaks and the emergence of virulent strains. In this study, we aim to elucidate the impact of homologous recombination in the diversification of S. enterica subspecies. Using a data set of previously published 926 Salmonella genomes representing the 10 S. enterica subspecies and Salmonella bongori, we calculated a genus-wide pan-genome composed of 84,041 genes and the S. enterica pan-genome of 81,371 genes. The size of the accessory genomes varies between 12,429 genes in S. enterica subsp. arizonae (subsp. IIIa) to 33,257 genes in S. enterica subsp. enterica (subsp. I). A total of 12,136 genes in the Salmonella pan-genome show evidence of recombination, representing 14.44% of the pan-genome. We identified genomic hot spots of recombination that include genes associated with flagellin and the synthesis of methionine and thiamine pyrophosphate, which are known to influence host adaptation and virulence. Last, we uncovered within-species heterogeneity in rates of recombination and preferential genetic exchange between certain donor and recipient strains. Frequent but biased recombination within a bacterial species may suggest that lineages vary in their response to environmental selection pressure. Certain lineages, such as the more uncommon non-enterica subspecies (non-S. enterica subsp. enterica), may also act as a major reservoir of genetic diversity for the wider population. IMPORTANCE S. enterica is a major foodborne pathogen, which can be transmitted via several distinct routes from animals and environmental sources to human hosts. Multiple subspecies and serotypes of S. enterica exhibit considerable differences in virulence, host specificity, and colonization. This study provides detailed insights into the dynamics of recombination and its contributions to S. enterica subspecies evolution. Widespread recombination within the species means that new adaptations arising in one lineage can be rapidly transferred to another lineage. We therefore predict that recombination has been an important factor in the emergence of several major disease-causing strains from diverse genomic backgrounds and their ability to adapt to disparate environments.

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“…coli, Pseudomonas aeruginosa, and Bacillus subtilis (11–13). In contrast, Salmonella species have two copies of flagellin genes (14), and Vibrio species have ∼5 or 6 flagellin genes. Six flagellin ORFs are found in Vibrio fischeri chromosomes as two clusters of flaABCDE and flaF (15), and five flagellin ORFs are in V.…”

Section: Introductionmentioning

confidence: 99%

Role of Flagellin-Homologous Proteins in Biofilm Formation by Pathogenic Vibrio Species

Jung

Lee

2019

mBio

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The pathogenic bacterium Vibrio vulnificus exhibits the ability to form biofilm, for which initiation is dependent upon swimming motility by virtue of a polar flagellum. The filament of its flagellum is composed of multiple flagellin subunits, FlaA, -B, -C, and -D. In V. vulnificus genomes, however, open reading frames (ORFs) annotated by FlaE and -F are also present. Although neither FlaE nor FlaF is involved in filament formation and cellular motility, they are well expressed and secreted to the extracellular milieu through the secretion apparatus for flagellar assembly. In the extrapolymeric matrix of V. vulnificus biofilm, significant levels of FlaEF were detected. Mutants defective in both flaE and flaF formed significantly decreased biofilms compared to the wild-type biofilm. Thus, the potential role of FlaEF during the biofilm-forming process was investigated by exogenous addition of recombinant FlaEF (rFlaEF) to the biofilm assays. The added rFlaE and rFlaF were predominantly incorporated into the biofilm matrix formed by the wild type. However, biofilms formed by a mutant defective in exopolysaccharide (EPS) biosynthesis were not affected by added FlaEF. These results raised a possibility that FlaEF specifically interact with EPS within the biofilm matrix. In vitro pulldown assays using His-tagged rFlaEF or rFlaC revealed the specific binding of EPS to rFlaEF but not to rFlaC. Taken together, our results demonstrate that V. vulnificus FlaEF, flagellin-homologous proteins (FHPs), are crucial for biofilm formation by directly interacting with the essential determinant for biofilm maturation, EPS. Further analyses performed with other pathogenic Vibrio species demonstrated both the presence of FHPs and their important role in biofilm formation. IMPORTANCE Flagellar filaments of the pathogenic Vibrio species, including V. vulnificus, V. parahaemolyticus, and V. cholerae, are composed of multiple flagellin subunits. In their genomes, however, there are higher numbers of the ORFs encoding flagellin-like proteins than the numbers of flagellin subunits required for filament assembly. Since these flagellin-homologous proteins (FHPs) are well expressed and excreted to environments via a flagellin transport channel, their extracellular role in the pathogenic Vibrio has been enigmatic. Their biological significance, which is not related with flagellar functions, has been revealed to be in maturation of biofilm structures. Among various components of the extracellular polymeric matrix produced in the V. vulnificus biofilms, the exopolysaccharides (EPS) are dominant constituents and crucial in maturation of biofilms. The enhancing role of the V. vulnificus FHPs in biofilm formation requires the presence of EPS, as indicated by highly specific interactions among two FHPs and three EPS.

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Comprehensive Analysis Reveals Two Distinct Evolution Patterns of Salmonella Flagellin Gene Clusters

Cited by 12 publications

References 53 publications

Comparative Genome Analysis of Hungarian and Global Strains of Salmonella Infantis

Comparative Genome Analysis of Hungarian and Global Strains of Salmonella Infantis

Distinct but Intertwined Evolutionary Histories of Multiple Salmonella enterica Subspecies

Role of Flagellin-Homologous Proteins in Biofilm Formation by Pathogenic Vibrio Species

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