Draft Genome Sequences of 53 Genetically Distinct Isolates of Bordetella bronchiseptica Representing 11 Terrestrial and Aquatic Hosts

Register, Karen B.; Ivanov, Yu. V.; Jacobs, Nathan T.; Meyer, Jessica A.; Goodfield, Laura L.; Muse, Sarah J.; Smallridge, William E.; Brinkac, Lauren; Kim, Maria; Sanka, Ravi; Harvill, Eric T.; Losada, Liliana

doi:10.1128/genomea.00152-15

Cited by 7 publications

(6 citation statements)

References 13 publications

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“…Recent efforts have generated numerous additional genome sequences from many Bordetella species, including B. bronchiseptica isolated from 11 different hosts [ 37 ] and B. pertussis outbreak strains [ 38 – 40 ]. Of particular interest are recently sequenced but only partially characterized genomes of non-classical Bordetella species, including sequences of B. holmesii [ 14 , 15 ], B. hinzii [ 41 , 42 ] and B. trematum [ 29 , 41 ].…”

Section: Introductionmentioning

confidence: 99%

Acquisition and loss of virulence-associated factors during genome evolution and speciation in three clades of Bordetella species

et al. 2016

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BackgroundThe genus Bordetella consists of nine species that include important respiratory pathogens such as the ‘classical’ species B. bronchiseptica, B. pertussis and B. parapertussis and six more distantly related and less extensively studied species. Here we analyze sequence diversity and gene content of 128 genome sequences from all nine species with focus on the evolution of virulence-associated factors.ResultsBoth genome-wide sequence-based and gene content-based phylogenetic trees divide the genus into three species clades. The phylogenies are congruent between species suggesting genus-wide co-evolution of sequence diversity and gene content, but less correlated within species, mainly because of strain-specific presence of many different prophages. We compared the genomes with focus on virulence-associated genes and identified multiple clade-specific, species-specific and strain-specific events of gene acquisition and gene loss, including genes encoding O-antigens, protein secretion systems and bacterial toxins. Gene loss was more frequent than gene gain throughout the evolution, and loss of hundreds of genes was associated with the origin of several species, including the recently evolved human-restricted B. pertussis and B. holmesii, B. parapertussis and the avian pathogen B. avium.ConclusionsAcquisition and loss of multiple genes drive the evolution and speciation in the genus Bordetella, including large scale gene loss associated with the origin of several species. Recent loss and functional inactivation of genes, including those encoding pertussis vaccine components and bacterial toxins, in individual strains emphasize ongoing evolution.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-3112-5) contains supplementary material, which is available to authorized users.

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Section: Introductionmentioning

confidence: 99%

Acquisition and loss of virulence-associated factors during genome evolution and speciation in three clades of Bordetella species

et al. 2016

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“…Thirty-four alleles were identified (Table 4). Although previously reported repeat region sequences derived from PCR amplicons for isolate 00-P-2730 comprise allele 1-4b1 / 2-6e1 (Diavatopoulos et al 2005), allele 1-4b1 / 2-6a2 is found in genome sequence data for this isolate (Register et al 2015b). Because other discrepant results have been reported by Diavatopoulos et al (2005), as noted by Register et al (2015a), here we opted to assign allele 1-4b1 / 2-6a2 to 00-P-2730.…”

Section: Pertactin Repeat Region Analysismentioning

confidence: 74%

“…STs for 61 isolates included in this study have been reported previously (Diavatopoulos et al;2005;Rath et al 2008;Register et al 2015a). Those for an additional 21 isolates were deduced from genome sequence data (Register et al 2015b; GenBank accession #NZ_JGWN01000000).…”

Section: Sequence-based Typingmentioning

confidence: 95%

“…An additional Arabic numeral is used to discriminate between different DNA sequence alleles with conservative substitutions that result in identical predicted amino acid sequences. Pertactin repeat region sequences from 86 isolates included in this study were previously reported (Register 2001;Parkhill et al 2003;Register 2004;Diavatopoulos et al 2005;Rath et al 2008;Register et al 2015a) or are available from genome sequence data (Register et al 2015b; GenBank accession #NZ_JGWN01000000).…”

Section: Sequence-based Typingmentioning

confidence: 99%

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Comparison of ribotyping and sequence-based typing for discriminating among isolates of Bordetella bronchiseptica

Nicholson

Brunelle

2016

Journal of Microbiological Methods

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PvuII ribotyping and MLST are each highly discriminatory methods for genotyping Bordetella bronchiseptica, but a direct comparison between these approaches has not been undertaken. The goal of this study was to directly compare the discriminatory power of PvuII ribotyping and MLST, using a single set of geographically and genetically diverse strains, and to determine whether subtyping based on repeat region sequences of the pertactin gene (prn) provides additional resolution. One hundred twenty-two isolates were analyzed, representing 11 mammalian or avian hosts, sourced from the United States, Europe, Israel and Australia. Thirty-two ribotype patterns were identified; one isolate could not be typed. In comparison, all isolates were typeable by MLST and a total of 30 sequence types was identified. An analysis based on Simpson's Index of Diversity (SID) revealed that ribotyping and MLST are nearly equally discriminatory, with SIDs of 0.920 for ribotyping and 0.919 for MLST. Nonetheless, for ten ribotypes and eight MLST sequence types, the alternative method discriminates among isolates that otherwise type identically. Pairing prn repeat region typing with ribotyping yielded 54 genotypes and increased the SID to 0.954. Repeat region typing combined with MLST resulted in 47 genotypes and an SID of 0.944. Given the technical and practical advantages of MLST over ribotyping, and the nominal difference in their SIDs, we conclude MLST is the preferred primary typing tool. We recommend the combination of MLST and prn repeat region typing as a high-resolution, objective and standardized approach valuable for investigating the population structure and epidemiology of B. bronchiseptica.

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“…B. pertussis is a strictly human pathogen, but B. parapertussis consists of two lineages, one infecting humans and the other infecting sheep (Mattoo and Cherry, 2005). In contrast to these examples of adaptation to a single host, B. bronchiseptica colonizes a variety of animals and even humans (Register et al, 2015), resulting in a broad array of respiratory diseases, from asymptomatic colonization to lethal pneumonia (Goodnow, 1980). Phylogenetic analyses (Musser et al, 1986; Diavatopoulos et al, 2005) and genome comparisons (Parkhill et al, 2003) have revealed that B. pertussis and B. parapertussis represent human-adapted forms of B. bronchiseptica that have evolved independently from a B. bronchiseptica -like ancestor.…”

Section: Introductionmentioning

confidence: 99%

Environmental Origin of the Genus Bordetella

2017

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Members of the genus Bordetella include human and animal pathogens that cause a variety of respiratory infections, including whooping cough in humans. Despite the long known ability to switch between a within-animal and an extra-host lifestyle under laboratory growth conditions, no extra-host niches of pathogenic Bordetella species have been defined. To better understand the distribution of Bordetella species in the environment, we probed the NCBI nucleotide database with the 16S ribosomal RNA (16S rRNA) gene sequences from pathogenic Bordetella species. Bacteria of the genus Bordetella were frequently found in soil, water, sediment, and plants. Phylogenetic analyses of their 16S rRNA gene sequences showed that Bordetella recovered from environmental samples are evolutionarily ancestral to animal-associated species. Sequences from environmental samples had a significantly higher genetic diversity, were located closer to the root of the phylogenetic tree and were present in all 10 identified sequence clades, while only four sequence clades possessed animal-associated species. The pathogenic bordetellae appear to have evolved from ancestors in soil and/or water. We show that, despite being animal-adapted pathogens, Bordetella bronchiseptica, and Bordetella hinzii have preserved the ability to grow and proliferate in soil. Our data implicate soil as a probable environmental origin of Bordetella species, including the animal-pathogenic lineages. Soil may further constitute an environmental niche, allowing for persistence and dissemination of the bacterial pathogens. Spread of pathogenic bordetellae from an environmental reservoir such as soil may potentially explain their wide distribution as well as frequent disease outbreaks that start without an obvious infectious source.

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Draft Genome Sequences of 53 Genetically Distinct Isolates of Bordetella bronchiseptica Representing 11 Terrestrial and Aquatic Hosts

Cited by 7 publications

References 13 publications

Acquisition and loss of virulence-associated factors during genome evolution and speciation in three clades of Bordetella species

Acquisition and loss of virulence-associated factors during genome evolution and speciation in three clades of Bordetella species

Comparison of ribotyping and sequence-based typing for discriminating among isolates of Bordetella bronchiseptica

Environmental Origin of the Genus Bordetella

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