Tangled bank of experimentally evolvedBurkholderiabiofilms reflects selection during chronic infections
Open Access
- 27 December 2012
- journal article
- research article
- Published by Proceedings of the National Academy of Sciences in Proceedings of the National Academy of Sciences of the United States of America
- Vol. 110 (3), E250-E259
- https://doi.org/10.1073/pnas.1207025110
Abstract
How diversity evolves and persists in biofilms is essential for understanding much of microbial life, including the uncertain dynamics of chronic infections. We developed a biofilm model enabling long-term selection for daily adherence to and dispersal from a plastic bead in a test tube. Focusing on a pathogen of the cystic fibrosis lung, Burkholderia cenocepacia, we sequenced clones and metagenomes to unravel the mutations and evolutionary forces responsible for adaptation and diversification of a single biofilm community during 1,050 generations of selection. The mutational patterns revealed recurrent evolution of biofilm specialists from generalist types and multiple adaptive alleles at relatively few loci. Fitness assays also demonstrated strong interference competition among contending mutants that preserved genetic diversity. Metagenomes from five other independently evolved biofilm lineages revealed extraordinary mutational parallelism that outlined common routes of adaptation, a subset of which was found, surprisingly, in a planktonic population. These mutations in turn were surprisingly well represented among mutations that evolved in cystic fibrosis isolates of both Burkholderia and Pseudomonas. These convergent pathways included altered metabolism of cyclic diguanosine monophosphate, polysaccharide production, tricarboxylic acid cycle enzymes, global transcription, and iron scavenging. Evolution in chronic infections therefore may be driven by mutations in relatively few pathways also favored during laboratory selection, creating hope that experimental evolution may illuminate the ecology and selective dynamics of chronic infections and improve treatment strategies.This publication has 54 references indexed in Scilit:
- Parallel bacterial evolution within multiple patients identifies candidate pathogenicity genesNature Genetics, 2011
- RNA polymerase mutants found through adaptive evolution reprogram Escherichia coli for optimal growth in minimal mediaProceedings of the National Academy of Sciences of the United States of America, 2010
- Robustness and EvolvabilityTrends in Genetics, 2010
- Ecological succession in long-term experimentally evolved biofilms produces synergistic communitiesThe ISME Journal, 2010
- Dynamics of Adaptive Microevolution of HypermutablePseudomonas aeruginosaduring Chronic Pulmonary Infection in Patients with Cystic FibrosisThe Journal of Infectious Diseases, 2009
- Clonal interference in large populationsProceedings of the National Academy of Sciences of the United States of America, 2007
- Epistasis correlates to genomic complexityProceedings of the National Academy of Sciences of the United States of America, 2006
- Evolving stealth: Genetic adaptation of Pseudomonas aeruginosa during cystic fibrosis infectionsProceedings of the National Academy of Sciences of the United States of America, 2006
- Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patientsProceedings of the National Academy of Sciences of the United States of America, 2006
- The multifarious, multireplicon Burkholderia cepacia complexNature Reviews Microbiology, 2005