PURPOSE OF REVIEW: To relate genomic changes to phenotypic adaptation and evolution from environmental bacteria to obligate human pathogens, focusing on the examples within Bordetella species. RECENT FINDINGS: Recent studies showed that animal-pathogenic and human-pathogenic Bordetella species evolved from environmental ancestors in soil. The animal-pathogenic Bordetella bronchiseptica can hijack the life cycle of the soil-living amoeba Dictyostelium discoideum, surviving inside single-celled trophozoites, translocating to the fruiting bodies and disseminating along with amoeba spores. The association with amoeba may have been a 'training ground' for bacteria during the evolution to pathogens. Adaptation to an animal-associated life style was characterized by decreasing metabolic versatility and genome size and by acquisition of 'virulence factors' mediating the interaction with the new animal hosts. Subsequent emergence of human-specific pathogens, such as Bordetella pertussis from zoonoses of broader host range progenitors, was accompanied by a dramatic reduction in genome size, marked by the loss of hundreds of genes. SUMMARY: The evolution of Bordetella from environmental microbes to animal-adapted and obligate human pathogens was accompanied by significant genome reduction with large-scale gene loss during divergence.
PURPOSE OF REVIEW: To relate genomic changes to phenotypic adaptation and evolution from environmental bacteria to obligate human pathogens, focusing on the examples within Bordetella species. RECENT FINDINGS: Recent studies showed that animal-pathogenic and human-pathogenic Bordetella species evolved from environmental ancestors in soil. The animal-pathogenic Bordetella bronchiseptica can hijack the life cycle of the soil-living amoeba Dictyostelium discoideum, surviving inside single-celled trophozoites, translocating to the fruiting bodies and disseminating along with amoeba spores. The association with amoeba may have been a 'training ground' for bacteria during the evolution to pathogens. Adaptation to an animal-associated life style was characterized by decreasing metabolic versatility and genome size and by acquisition of 'virulence factors' mediating the interaction with the new animal hosts. Subsequent emergence of human-specific pathogens, such as Bordetella pertussis from zoonoses of broader host range progenitors, was accompanied by a dramatic reduction in genome size, marked by the loss of hundreds of genes. SUMMARY: The evolution of Bordetella from environmental microbes to animal-adapted and obligate human pathogens was accompanied by significant genome reduction with large-scale gene loss during divergence.
Authors: Julian Parkhill; Mohammed Sebaihia; Andrew Preston; Lee D Murphy; Nicholas Thomson; David E Harris; Matthew T G Holden; Carol M Churcher; Stephen D Bentley; Karen L Mungall; Ana M Cerdeño-Tárraga; Louise Temple; Keith James; Barbara Harris; Michael A Quail; Mark Achtman; Rebecca Atkin; Steven Baker; David Basham; Nathalie Bason; Inna Cherevach; Tracey Chillingworth; Matthew Collins; Anne Cronin; Paul Davis; Jonathan Doggett; Theresa Feltwell; Arlette Goble; Nancy Hamlin; Heidi Hauser; Simon Holroyd; Kay Jagels; Sampsa Leather; Sharon Moule; Halina Norberczak; Susan O'Neil; Doug Ormond; Claire Price; Ester Rabbinowitsch; Simon Rutter; Mandy Sanders; David Saunders; Katherine Seeger; Sarah Sharp; Mark Simmonds; Jason Skelton; Robert Squares; Steven Squares; Kim Stevens; Louise Unwin; Sally Whitehead; Bart G Barrell; Duncan J Maskell Journal: Nat Genet Date: 2003-08-10 Impact factor: 38.330
Authors: Peter A Vandamme; Charlotte Peeters; Margo Cnockaert; Elisabeth Inganäs; Enevold Falsen; Edward R B Moore; Olga C Nunes; Célia M Manaia; Theodore Spilker; John J LiPuma Journal: Int J Syst Evol Microbiol Date: 2015-10 Impact factor: 2.747
Authors: Sara E Hester; Laura L Goodfield; Jihye Park; Heather A Feaga; Yury V Ivanov; Liron Bendor; Dawn L Taylor; Eric T Harvill Journal: PLoS One Date: 2015-07-09 Impact factor: 3.240
Authors: Marieke J Bart; Simon R Harris; Abdolreza Advani; Yoshichika Arakawa; Daniela Bottero; Valérie Bouchez; Pamela K Cassiday; Chuen-Sheue Chiang; Tine Dalby; Norman K Fry; María Emilia Gaillard; Marjolein van Gent; Nicole Guiso; Hans O Hallander; Eric T Harvill; Qiushui He; Han G J van der Heide; Kees Heuvelman; Daniela F Hozbor; Kazunari Kamachi; Gennady I Karataev; Ruiting Lan; Anna Lutyńska; Ram P Maharjan; Jussi Mertsola; Tatsuo Miyamura; Sophie Octavia; Andrew Preston; Michael A Quail; Vitali Sintchenko; Paola Stefanelli; M Lucia Tondella; Raymond S W Tsang; Yinghua Xu; Shu-Man Yao; Shumin Zhang; Julian Parkhill; Frits R Mooi Journal: mBio Date: 2014-04-22 Impact factor: 7.867
Authors: Dawn L Taylor-Mulneix; Liron Bendor; Bodo Linz; Israel Rivera; Valerie E Ryman; Kalyan K Dewan; Shannon M Wagner; Emily F Wilson; Lindsay J Hilburger; Laura E Cuff; Christopher M West; Eric T Harvill Journal: PLoS Biol Date: 2017-04-12 Impact factor: 8.029
Authors: Yury V Ivanov; Nikki Shariat; Karen B Register; Bodo Linz; Israel Rivera; Kai Hu; Edward G Dudley; Eric T Harvill Journal: BMC Genomics Date: 2015-10-26 Impact factor: 3.969
Authors: Israel Rivera; Bodo Linz; Kalyan K Dewan; Longhuan Ma; Christopher A Rice; Dennis E Kyle; Eric T Harvill Journal: Front Microbiol Date: 2019-12-11 Impact factor: 5.640
Authors: Jakub Novák; David Jurnečka; Irena Linhartová; Jana Holubová; Ondřej Staněk; Daniel Štipl; Ana Dienstbier; Branislav Večerek; Nayara Azevedo; Jan Provazník; Vladimír Beneš; Peter Šebo Journal: mSystems Date: 2020-12-08 Impact factor: 6.496