Adverse effects of adaptive mutation to survive static culture conditions on successful fitness of the rice pathogen Burkholderia glumae in a host

PLoS One. 2020 Aug 24;15(8):e0238151. doi: 10.1371/journal.pone.0238151. eCollection 2020.

Abstract

Bacteria often possess relatively flexible genome structures and adaptive genetic variants that allow survival in unfavorable growth conditions. Bacterial survival tactics in disadvantageous microenvironments include mutations that are beneficial against threats in their niche. Here, we report that the aerobic rice bacterial pathogen Burkholderia glumae BGR1 changes a specific gene for improved survival in static culture conditions. Static culture triggered formation of colony variants with deletions or point mutations in the gene bspP (BGLU_RS28885), which putatively encodes a protein that contains PDC2, PAS-9, SpoIIE, and HATPase domains. The null mutant of bspP survived longer in static culture conditions and produced a higher level of bis-(3'-5')-cyclic dimeric guanosine monophosphate than the wild type. Expression of the bacterial cellulose synthase regulator (bcsB) gene was upregulated in the mutant, consistent with the observation that the mutant formed pellicles faster than the wild type. Mature pellicle formation was observed in the bspP mutant before pellicle formation in wild-type BGR1. However, the population density of the bspP null mutant decreased substantially when grown in Luria-Bertani medium with vigorous agitation due to failure of oxalate-mediated detoxification of the alkaline environment. The bspP null mutant was less virulent and exhibited less effective colonization of rice plants than the wild type. All phenotypes caused by mutations in bspP were recovered to those of the wild type by genetic complementation. Thus, although wild-type B. glumae BGR1 prolonged viability by spontaneous mutation under static culture conditions, such genetic changes negatively affected colonization in rice plants. These results suggest that adaptive gene sacrifice of B. glumae to survive unfavorable growth conditions is not always desirable as it can adversely affect adaptability in the host.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptation, Biological / genetics*
  • Burkholderia / genetics*
  • Burkholderia / metabolism*
  • Burkholderia / pathogenicity
  • Gene Expression Regulation, Bacterial / genetics
  • Genome, Bacterial / genetics
  • Genomics / methods
  • Mutation
  • Oryza / microbiology
  • Plant Diseases / microbiology
  • Quorum Sensing / genetics
  • Virulence / genetics

Supplementary concepts

  • Burkholderia glumae

Grants and funding

This work was supported by the National Research Foundation of Korea (NRF: https://www.nrf.re.kr) grant funded by the Ministry of Science and ICT of the Korean Government (No.2017R1A2B4005815) (I.H.); and by the Basic Science Research Program through the NRF funded by the Ministry of Education (No.2016R1D1A1B03932635) (E.G.). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.