Bodo Linz1, Yury V Ivanov2, Andrew Preston3, Lauren Brinkac4, Julian Parkhill5, Maria Kim4, Simon R Harris5, Laura L Goodfield2, Norman K Fry6, Andrew R Gorringe7, Tracy L Nicholson8, Karen B Register8, Liliana Losada4, Eric T Harvill9,10,11. 1. Department of Veterinary and Biomedical Sciences, Pennsylvania State University, University Park, PA 16802, USA. bxl29@psu.edu. 2. Department of Veterinary and Biomedical Sciences, Pennsylvania State University, University Park, PA 16802, USA. 3. The Millner Centre for Evolution and Department of Biology and Biochemistry, University of Bath, Bath, UK. 4. J. Craig Venter Institute, Rockville, MD, USA. 5. Pathogen Genomics, The Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge, UK. 6. Public Health England, Respiratory and Vaccine Preventable Bacteria Reference Unit, London, UK. 7. Public Health England, Porton Down, Salisbury, UK. 8. USDA, Agricultural Research Service, National Animal Disease Center, Ames, IA, USA. 9. Department of Veterinary and Biomedical Sciences, Pennsylvania State University, University Park, PA 16802, USA. Harvill@uga.edu. 10. Singapore Centre on Environmental Life Sciences Engineering, Lee Kong Chian School of Medicine, Nanyang Technological University, Singapore 637551, Singapore. Harvill@uga.edu. 11. Department of Infectious Diseases, College of Veterinary Medicine, University of Georgia, Athens, GA 30602, USA. Harvill@uga.edu.
Abstract
BACKGROUND: The 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. RESULTS: Both 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. CONCLUSIONS: Acquisition 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.
BACKGROUND: The 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. RESULTS: Both 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. CONCLUSIONS: Acquisition 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.
Authors: I Gadea; M Cuenca-Estrella; N Benito; A Blanco; M L Fernández-Guerrero; P L Valero-Guillén; F Soriano Journal: J Infect Date: 2000-05 Impact factor: 6.072
Authors: Katie L Sealey; Simon R Harris; Norman K Fry; Laurence D Hurst; Andrew R Gorringe; Julian Parkhill; Andrew Preston Journal: J Infect Dis Date: 2014-12-08 Impact factor: 5.226
Authors: Valorie C Burns; Elizabeth J Pishko; Andrew Preston; Duncan J Maskell; Eric T Harvill Journal: Infect Immun Date: 2003-01 Impact factor: 3.441
Authors: Jihye Park; Ying Zhang; Anne M Buboltz; Xuqing Zhang; Stephan C Schuster; Umesh Ahuja; Minghsun Liu; Jeff F Miller; Mohammed Sebaihia; Stephen D Bentley; Julian Parkhill; Eric T Harvill Journal: BMC Genomics Date: 2012-10-10 Impact factor: 3.969
Authors: Norman K Fry; John Duncan; Henry Malnick; Marina Warner; Andrew J Smith; Margaret S Jackson; Ashraf Ayoub Journal: Emerg Infect Dis Date: 2005-07 Impact factor: 6.883
Authors: Eric T Harvill; Laura L Goodfield; Yury Ivanov; Jessica A Meyer; Christopher Newth; Pamela Cassiday; Maria Lucia Tondella; Patty Liao; Jerry Zimmerman; Kathleen Meert; David Wessel; John Berger; J Michael Dean; Richard Holubkov; Jeri Burr; Teresa Liu; Lauren Brinkac; Maria Kim; Liliana Losada Journal: Genome Announc Date: 2013-12-19
Authors: Dawn L Taylor-Mulneix; Illiassou Hamidou Soumana; Bodo Linz; Eric T Harvill Journal: Front Cell Infect Microbiol Date: 2017-12-11 Impact factor: 5.293