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.

Highlights

  • Bacterial genomes are flexible and can be changed under different growth conditions for survival [1]

  • Our results suggest that adaptive evolution by sacrifice of a specific gene to overcome unfavorable growth conditions could cause unexpected and devastating outcomes for plant pathogenic bacteria such as B. glumae

  • Emergence of morphologically distinct spontaneous mutants in static culture To determine the viability of aerobic B. glumae wild-type BGR1 in static culture, aliquots of the static culture were taken each day for a week

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Summary

Introduction

Bacterial genomes are flexible and can be changed under different growth conditions for survival [1]. Synthesized bacterial cellulosic biofilms float at the air–liquid interface as pellicles where available oxygen is most abundant, and cells with various colony forms exist at the interface [3, 6, 7]. Constrained environments, such as static culture conditions in which sufficient oxygen for normal growth of aerobic bacteria is lacking, require aerobic bacteria to survive and adapt in an oxygen-deficient environment [7,8,9]. This forces them to evolve in ways that maximize their metabolism for survival [10,11,12]

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