Kill and cure: genomic phylogeny and bioactivity of Burkholderia gladioli bacteria capable of pathogenic and beneficial lifestyles

Author:

Jones Cerith12ORCID,Webster Gordon2ORCID,Mullins Alex J.2ORCID,Jenner Matthew34ORCID,Bull Matthew J.52ORCID,Dashti Yousef64ORCID,Spilker Theodore7ORCID,Parkhill Julian89ORCID,Connor Thomas R.2ORCID,LiPuma John J.7ORCID,Challis Gregory L.4310ORCID,Mahenthiralingam Eshwar2ORCID

Affiliation:

1. Present address: School of Applied Sciences, Faculty of Computing, Engineering and Science, University of South Wales, Pontypridd, CF37 4BD, UK

2. Microbiomes, Microbes and Informatics Group, Organisms and Environment Division, School of Biosciences, Cardiff University, Cardiff, CF10 3AX, UK

3. Warwick Integrative Synthetic Biology Centre, University of Warwick, Coventry CV4 7AL, UK

4. Department of Chemistry and Warwick Integrative Synthetic Biology Centre, University of Warwick, CV4 7AL, UK

5. Present address: Pathogen Genomics Unit, Public Health Wales Microbiology Cardiff, University Hospital of Wales, Cardiff, CF14 4XW, UK

6. Present address: The Centre for Bacterial Cell Biology, Biosciences Institute, Medical School, Newcastle University, Newcastle upon Tyne, NE2 4AX, UK

7. Department of Pediatrics, University of Michigan Medical School, Ann Arbor, Michigan, USA

8. Present address: Department of Veterinary Medicine, University of Cambridge, Madingley Road, Cambridge CB3 0ES, UK

9. Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK

10. Department of Biochemistry and Molecular Biology, Biomedicine Discovery Institute, Monash University, Clayton, VIC 3800, Australia

Abstract

Burkholderia gladioli is a bacterium with a broad ecology spanning disease in humans, animals and plants, but also encompassing multiple beneficial interactions. It is a plant pathogen, a toxin-producing food-poisoning agent, and causes lung infections in people with cystic fibrosis (CF). Contrasting beneficial traits include antifungal production exploited by insects to protect their eggs, plant protective abilities and antibiotic biosynthesis. We explored the genomic diversity and specialized metabolic potential of 206 B. gladioli strains, phylogenomically defining 5 clades. Historical disease pathovars (pv.) B. gladioli pv. allicola and B. gladioli pv. cocovenenans were distinct, while B. gladioli pv. gladioli and B. gladioli pv. agaricicola were indistinguishable; soft-rot disease and CF infection were conserved across all pathovars. Biosynthetic gene clusters (BGCs) for toxoflavin, caryoynencin and enacyloxin were dispersed across B. gladioli , but bongkrekic acid and gladiolin production were clade-specific. Strikingly, 13 % of CF infection strains characterized were bongkrekic acid-positive, uniquely linking this food-poisoning toxin to this aspect of B. gladioli disease. Mapping the population biology and metabolite production of B. gladioli has shed light on its diverse ecology, and by demonstrating that the antibiotic trimethoprim suppresses bongkrekic acid production, a potential therapeutic strategy to minimize poisoning risk in CF has been identified.

Funder

Biotechnology and Biological Sciences Research Council

Medical Research Council

Publisher

Microbiology Society

Subject

General Medicine

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