Conserved Patterns of Symmetric Inversion in the Genome Evolution of Bordetella Respiratory Pathogens - PubMed (original) (raw)

. 2019 Nov 19;4(6):e00702-19.

doi: 10.1128/mSystems.00702-19.

Yanhui Peng 2, Dhwani Batra 3, Mark Burroughs 3, Jamie K Davis 3, Kristen Knipe 3, Vladimir N Loparev 3, Taccara Johnson 2, Phalasy Juieng 3, Lori A Rowe 3, Mili Sheth 3, Kevin Tang 3, Yvette Unoarumhi 3, Margaret M Williams 2, M Lucia Tondella 2

Affiliations

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

Michael R Weigand et al. mSystems. 2019.

Abstract

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 IS_481_, 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.

Keywords: Bordetella; evolution; genomics; insertion sequence; pertussis; rearrangement; whooping cough.

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Figures

FIG 1

FIG 1

Phylogeny of the genus Bordetella. Neighbor-joining tree of named and provisional Bordetella species with available complete-genome sequences based on pairwise mash distances and rooted with Achromobacter xylosoxidans. Species sequenced at the CDC are listed in red. Triangles indicate collapsed nodes.

FIG 2

FIG 2

Genome rearrangements in Bordetella species. (A) Eleven unique chromosome structures that included six symmetric inversions were observed among B. holmesii isolate genomes. (B) Two predominant structures were observed in B. parapertussis. (C, D) Phylogenetic placement of structures observed in B. holmesii (C) and B. parapertussis (D) isolates was reconstructed using maximum parsimony from 1,496 and 677 core SNPs, respectively.

FIG 3

FIG 3

Genome rearrangement in B. pertussis. (A) Observed inversions were either symmetric, encompassing either replication origin (purple) or terminus (light blue), or asymmetric (blue). (B) Single inversions observed in pairwise alignments varied in size and were predominantly symmetric. (C) Undirected network constructed from single inversions or insertion/deletions observed between 71 unique chromosome structures. Node diameter and edge line type indicate cluster size and rearrangement, respectively, according to the key. Nodes with the highest degrees of centrality (Fig. S5A) and their connections at the network core are highlighted (green). Shaded arrows indicate directionality inferred from the SNP phylogeny (Fig. S7), including divergence toward the predominant cluster BP-01 (pink), as described in the text.

FIG 4

FIG 4

Symmetric inversion balance and prediction. (A) Density of relative replichore size balance observed in each of the 107 unique B. pertussis genome structures. (B) Histogram of breakpoint balance observed in symmetric inversions encompassing the replication origin (purple) or terminus (light blue). The combined densities of observed (solid line) and predicted (dotted line) symmetric inversions were scaled to 10. (C) Linear regression of right and left breakpoint distances observed in B. pertussis (circle) and B. holmesii (triangle) nearest to the replication origin (purple) or terminus (light blue). Open symbols represent duplicated points inverted for model calculation. Blue line indicates linear fit, and shading represents the 95% confidence interval. Dotted red lines denote boundaries of the model’s 95% prediction interval, and gray points correspond to all predicted inversions between copies of IS elements in B. pertussis J549.

FIG 5

FIG 5

Inversion potential of Bordetella species genomes based on IS element content. Chromosome maps of B. pertussis J549 (A), B. holmesii C690 (B), and B. parapertussis B271 (C). Tracks of red lines indicate the locations of IS elements in either the forward or reverse orientation (above or below center, respectively). Connecting lines link breakpoints of observed symmetric (black), observed asymmetric (blue), and predicted symmetric (gray) inversions. Additional tracks in panel A denote all breakpoints observed in pairwise alignments between J549 and genomes of the ptxP1-ptxP2 (orange) or ptxP3 (green) clades.

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