Impact of a Bacterial Volatile 2,3-Butanediol on Bacillus subtilis Rhizosphere Robustness

Abstract

Volatile compounds, such as short chain alcohols, acetoin, and 2,3-butanediol, produced by certain strains of root-associated bacteria (rhizobacteria) elicit induced systemic resistance in plants. The effects of bacterial volatile compounds (BVCs) on plant and fungal growth have been extensively studied; however, the impact of bacterial BVCs on bacterial growth remains poorly understood. In this study the effects of a well-characterized bacterial volatile, 2,3-butanediol, produced by the rhizobacterium Bacillus subtilis, were examined in the rhizosphere. The nature of 2,3-butanediol on bacterial cells was assessed, and the effect of the molecule on root colonization was also determined. Pepper roots were inoculated with three B. subtilis strains: the wild type, a 2,3-butanediol overexpressor, and a 2,3-butanediol null mutant. The B. subtilis null strain was the first to be eliminated in the rhizosphere, followed by the wild-type strain. The overexpressor mutant was maintained at roots for the duration of the experiment. Rhizosphere colonization by a saprophytic fungus declined from 14 days post-inoculation in roots treated with the B. subtilis overexpressor strain. Next, exudates from roots exposed to 2,3-butanediol were assessed for their impact on fungal and bacterial growth in vitro. Exudates from plant roots pre-treated with the 2,3-butanediol overexpressor were used to challenge various microorganisms. Growth was inhibited in a saprophytic fungus (Trichoderma sp.), the 2,3-butanediol null B. subtilis strain, and a soil-borne pathogen, Ralstonia solanacearum. Direct application of 2,3-butanediol to pepper roots, followed by exposure to R. solanacearum, induced expression of Pathogenesis-Related (PR) genes such as CaPR2, CaSAR8.2, and CaPAL. These results indicate that 2,3-butanediol triggers the secretion of root exudates that modulate soil fungi and rhizosphere bacteria. These data broaden our knowledge regarding bacterial volatiles in the rhizosphere and their roles in bacterial fitness and as important inducers of plant defenses.

Diversity of phytobeneficial traits revealed by whole‐genome analysis of worldwide‐isolated phenazine‐producing Pseudomonas spp.

“…). These volatile organic compounds are known as plant‐growth promoting factors (Ryu et al, ) and 2,3‐butanediol has been shown to induce systemic resistance (Han et al, ) and modulates root exudation (Yi et al, ). Every strain also possesses the pyrroloquinoline quinone (PQQ) biosynthetic operon pqqFABCDEF (Fig.…”

Wars between microbes on roots and fruits

“…More recently, Ryu’s group studied rhizosphere colonization of pepper, using the wild-type 2,3-butanediol producer B. subtilis 168, its null mutant, and a 2,3-butanediol-overproducing derivative. The results showed that a higher level of 2,3-butanediol production correlates with improved rhizosphere competence of B. subtilis itself and that 2,3-butanediol production by B. subtilis suppresses the growth of the saprophytic fungus Trichoderma in the rhizosphere 74 . Furthermore, growth experiments were carried out in exudates of roots pre-treated with the 2,3-butanediol-overproducing strain.…”

“…The same pre-treatment also inhibited the growth of the soil-borne bacterial pathogen R. solanacearum but enhanced the growth of the saprophytic biocontrol bacterium P. protegens Pf-5. Apparently, 2,3-butanediol alters the root exudate composition 74 .…”

“…by raising the pH of the culture medium 57 , negatively affecting biofilm formation 57, 67 , eliciting ISR in a plant 68– 73 , eliciting induced systemic tolerance to stresses caused by drought and heavy metals 60, 69 , and promoting plant robustness 74 and plant growth 68, 75 .…”

Inheritance of seed and rhizosphere microbial communities through plant–soil feedback and soil memory

“…Microbiota that suppress plant disease typically accumulate in soil after a response to plant stress, such as disease occurrence, in the field. During disease development, plants secrete root exudates that recruit disease-suppressive microbiota (Yi et al, 2016). Such microbiota can accumulate even after diseased plants are removed from the field.…”