Induction of Biofilm Formation in the Betaproteobacterium Burkholderia unamae CK43B Exposed to Exogenous Indole and Gallic Acid

Abstract

bBurkholderia unamae CK43B, a member of the Betaproteobacteria that was isolated from the rhizosphere of a Shorea balangeran sapling in a tropical peat swamp forest, produces neither indole nor extracellular polymeric substances associated with biofilm formation. When cultured in a modified Winogradsky's medium supplemented with up to 1.7 mM indole, B. unamae CK43B maintains its planktonic state by cell swelling and effectively degrades exogenous indole. However, in medium supplemented with 1.7 mM exogenous indole and 1.0 mM gallic acid, B. unamae CK43B produced extracellular polymeric substances and formed a biofilm. The concentration indicated above of gallic acid alone had no effect on either the growth or the differentiation of B. unamae CK43B cells above a certain concentration threshold, whereas it inhibited indole degradation by B. unamae CK43B to 3-hydroxyindoxyl. In addition, coculture of B. unamae CK43B with indole-producing Escherichia coli in nutrient-rich Luria-Bertani medium supplemented with 1.0 mM gallic acid led to the formation of mixed cell aggregates. The viability and active growth of B. unamae CK43B cells in a coculture system with Escherichia coli were evidenced by fluorescence in situ hybridization. Our data thus suggest that indole facilitates intergenus communication between indole-producing gammaproteobacteria and some indole-degrading bacteria, particularly in gallic acid-rich environments.

The multifaceted roles of the interspecies signalling molecule indole in Agrobacterium tumefaciens

“…Because indole modulates the biofilm formation of various bacteria (Lee et al ., 2007a; 2009; Kim et al ., ), we examined the effects of indole and indole‐3‐acetic acid on A . tumefaciens biofilm formation in 96‐well polystyrene plates.…”

“…Because indole modulates the biofilm formation of various bacteria (Lee et al, 2007a;Kim et al, 2013), we examined the effects of indole and indole-3-acetic acid on A. tumefaciens biofilm formation in 96-well polystyrene plates. Indole at (0-1.0 mM) concentration dependently increased A. tumefaciens biofilm formation by up to 6.4 ± 1.6-fold ( Fig.…”

“…Moreover, it is likely non‐indole‐producing bacteria use indole for defence purposes, for example, indole has been reported to enhance antibiotic tolerance of Salmonella typhimurium by oxidative stress response (Vega et al ., ). Also, indole increased antibiotic tolerance and biofilm formation of Burkholderia unamae (Kim et al ., ) and antibiotic resistance of Pseudomonas putida (Molina‐Santiago et al ., ). It was initially reported that indole was not toxic to P .…”

Roles of Indole as an Interspecies and Interkingdom Signaling Molecule

“…For example, indole inhibits the attachment of the fungal pathogen Candida albicans to intestinal epithelial HT-29 cells [56] and reduces the production of the virulence factor staphyloxanthin in Staphylococcus aureus [57]; both of these studies demonstrated virulence reduction in a Caenorhabditis elegans model [56,57]. Indole also inhibits cyanobacterial blooms caused by the formation of periphyton biofilms [58], induces biofilm formation by rhizospheric Burkholderia unamae [59], and delays predation by Bdellovibrio bacteriovorus [60]. It would be interesting to determine whether indole affects the virulence of other pathogens as well as those of environmental bacteria.…”

Highly Active Modulators of Indole Signaling Alter Pathogenic Behaviors in Gram‐Negative and Gram‐Positive Bacteria

“…To date, over 85 bacterial species, both Gram negative and Gram positive, have been reported to produce indole, whereas both indole‐producing and non‐indole‐producing strains of bacteria will adapt their behavior in response to extracellular indole 8. 9, 10 It has been shown that indole controls a variety of key pathogenic phenotypes. In E. coli, indole decreases acid resistance,11 induces the expression of multidrug exporter genes and increases antibiotic resistance 12.…”