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

Linz, Bodo; Ivanov, Yu. V.; Preston, Andrew; Brinkac, Lauren; Parkhill, Julian; Kim, Maria; Harris, Simon R.; Goodfield, Laura L.; Fry, Norman K.; Gorringe, Andrew; Nicholson, Tracy L.; Register, Karen B.; Losada, Liliana; Harvill, Eric T.

doi:10.1186/s12864-016-3112-5

Cited by 74 publications

(100 citation statements)

References 77 publications

(114 reference statements)

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…A neighborjoining phylogenetic reconstruction of these species, plus two distantly related Bordetella isolates (H567 and J329), rooted with outgroup Achromobacter xylosoxidans, clustered the classic bordetellae apart from the otherwise disparate species branches ( Fig. 1), consistent with previous studies (10). The number of single nucleotide polymorphisms (SNPs) observed in each species varied.…”

Section: Resultssupporting

confidence: 85%

“…There are Ͼ240 copies of IS481 in genomes of circulating B. pertussis strains, which has significantly impacted the evolution of this species (39). Likewise, the genomes of B. holmesii and B. parapertussis each harbor a collection of different IS elements that have contributed to their speciation through genome reduction (10,43,44), as well as mediated the rearrangements observed here. B. holmesii has evolved independently of the classic bordetellae, reiterating the influence of IS element colonization, not phylogenetic history, on genome structural fluidity in the genus.…”

Section: Discussionmentioning

confidence: 80%

“…Divergent lineages of B. parapertussis infect the respiratory tracts of sheep and humans (7)(8)(9). The remaining "nonclassic" species are phylogenetically more distant and have been recovered from varied hosts and pathologies, in particular, B. holmesii and B. hinzii from humans, which is reflected in their discrete virulence-associated-gene compositions (10).…”

mentioning

confidence: 99%

See 2 more Smart Citations

Conserved Patterns of Symmetric Inversion in the Genome Evolution of Bordetella Respiratory Pathogens

et al. 2019

View full text Add to dashboard Cite

Whooping cough (pertussis), primarily caused by Bordetella pertussis, has resurged in the United States, and circulating strains exhibit considerable chromosome structural fluidity in the form of rearrangement and deletion. The genus Bordetella includes additional pathogenic species infecting various animals, some even causing pertussis-like respiratory disease in humans; however, investigation of their genome evolution has been limited. We studied chromosome structure in complete genome sequences from 167 Bordetella species isolates, as well as 469 B. pertussis isolates, to gain a generalized understanding of rearrangement patterns among these related pathogens. Observed changes in gene order primarily resulted from large inversions and were only detected in species with genomes harboring multicopy insertion sequence (IS) elements, most notably B. holmesii and B. parapertussis. While genomes of B. pertussis contain >240 copies of IS481, IS elements appear less numerous in other species and yield less chromosome structural diversity through rearrangement. These data were further used to predict all possible rearrangements between IS element copies present in Bordetella genomes, revealing that only a subset is observed among circulating strains. Therefore, while it appears that rearrangement occurs less frequently in other species than in B. pertussis, these clinically relevant respiratory pathogens likely experience similar mutation of gene order. The resulting chromosome structural fluidity presents both challenges and opportunity for the study of Bordetella respiratory pathogens. IMPORTANCE Bordetella pertussis is the primary agent of whooping cough (pertussis). The Bordetella genus includes additional pathogens of animals and humans, including some that cause pertussis-like respiratory illness. The chromosome of B. pertussis has previously been shown to exhibit considerable structural rearrangement, but insufficient data have prevented comparable investigation in related species. In this study, we analyze chromosome structure variation in several Bordetella species to gain a generalized understanding of rearrangement patterns in this genus. Just as in B. pertussis, we observed inversions in other species that likely result from common mutational processes. We used these data to further predict additional, unobserved inversions, suggesting that specific genome structures may be preferred in each species.

show abstract

Section: Resultssupporting

confidence: 85%

Section: Discussionmentioning

confidence: 80%

mentioning

confidence: 99%

See 1 more Smart Citation

Conserved Patterns of Symmetric Inversion in the Genome Evolution of Bordetella Respiratory Pathogens

et al. 2019

View full text Add to dashboard Cite

show abstract

“…B. petrii was originally isolated from an anaerobic bioreactor culture enriched from river sediment (von Wintzingerode et al, 2001) and was subsequently isolated from many soil samples (Hamidou Soumana et al, 2017;Garrido-Sanz et al, 2018). Although several genomic features have changed throughout their independent evolution, including acquisition and loss of multiple virulence-associated genes (Linz et al, 2016(Linz et al, , 2019, these Bordetella species share many characteristics that make them successful animal pathogens.…”

Section: Introductionmentioning

confidence: 99%

Conservation of Ancient Genetic Pathways for Intracellular Persistence Among Animal Pathogenic Bordetellae

et al. 2019

Self Cite

View full text Add to dashboard Cite

Animal and human pathogens of the genus Bordetella are not commonly considered to be intracellular pathogens, although members of the closely related classical bordetellae are known to enter and persist within macrophages in vitro and have anecdotally been reported to be intracellular in clinical samples. B. bronchiseptica, the species closest to the ancestral lineage of the classical bordetellae, infects a wide range of mammals but is known to have an alternate life cycle, persisting, replicating and disseminating with amoeba. These observations give rise to the hypothesis that the ability for intracellular survival has an ancestral origin and is common among animalpathogenic and environmental Bordetella species. Here we analyzed the survival of B. bronchiseptica and defined its transcriptional response to internalization by murine macrophage-like cell line RAW 264.7. Although the majority of the bacteria were killed and digested by the macrophages, a consistent fraction survived and persisted inside the phagocytes. Internalization prompted the activation of a prominent stress response characterized by upregulation of genes involved in DNA repair, oxidative stress response, pH homeostasis, chaperone functions, and activation of specific metabolic pathways. Cross species genome comparisons revealed that most of these upregulated genes are highly conserved among both the classical and non-classical Bordetella species. The diverse Bordetella species also shared the ability to survive inside RAW 264.7 cells, with the single exception being the bird pathogen B. avium, which has lost several of those genes. Knockout mutations in genes expressed intracellularly resulted in decreased persistence inside the phagocytic cells, emphasizing the importance of these genes in this environment. These data show that the ability to persist inside macrophage-like RAW 264.7 cells is shared among nearly all Bordetella species, suggesting that resisting phagocytes may be an ancient mechanism that precedes speciation in the genus and may have facilitated the adaptation of Bordetella species from environmental bacteria to mammalian respiratory pathogens.

show abstract

“…The genus Bordetella consists of nine species that could infect a variety of hosts, including humans, birds and rodents . B. pertussis , the agent of whooping cough in humans, together with B. parapertussis and B. bronchiseptica , are commonly classified as “classical” Bordetella . The other six species ( Bordetella holmesii , Bordetella trematum , Bordetella avium , Bordetella petrii , Bordetella hinzii and Bordetella pseudohinzii ) are classified as “non‐classical” Bordetella …”

Section: Introductionmentioning

confidence: 99%

Isolation and characterization of Bordetella pseudohinzii in mice in China

Huang

Luo

et al. 2019

Anim Models and Exp Med

View full text Add to dashboard Cite

We report on the first detection and isolation of B. pseudohinzii (Bordetella pseudohinzii) in laboratory mice in China. Forty‐one B. pseudohinzii strains were isolated from 3094 mice in 33 different laboratory animal facilities in southern China. The isolates were identified through culture and genome sequenceing. Phylogenetic analysis based on the sequences of 16S rRNA and OmpA genes demonstrated that these strains were on the same clade as other B. pseudohinzii strains isolated from mice. Experimental infected mice presented an asymptomatic infection. B. pseudohinzii replicated in both the respiratory tract and the digestive tract. Most importantly B. pseudohinzii shed via feces and infected a group of sentinel mice in a separate cage via cage padding contaminated with B. pseudohinzii‐positive feces, indicating that B. pseudohinzii could transmit efficiently among mice and contaminate environmental facilities. Our study highlights the importance of routine monitoring of the pathogen in laboratory mice and provides vital insights into the transmission of Brodetellae in rodents and human.

show abstract

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

Cited by 74 publications

References 77 publications

Conserved Patterns of Symmetric Inversion in the Genome Evolution of Bordetella Respiratory Pathogens

Conserved Patterns of Symmetric Inversion in the Genome Evolution of Bordetella Respiratory Pathogens

Conservation of Ancient Genetic Pathways for Intracellular Persistence Among Animal Pathogenic Bordetellae

Isolation and characterization of Bordetella pseudohinzii in mice in China

Contact Info

Product

Resources

About