Indole‐associated predator–prey interactions between the nematode Caenorhabditis elegans and bacteria

Abstract

Indole is an intercellular and interkingdom signalling molecule found in diverse ecological niches. Caenorhabditis elegans is a bacterivorous nematode that lives in soil and compost environments and a useful model host for studies of host-microbe interactions. Although various bacteria and some plants produce large quantities of extracellular indole, little is known about the effects of indole, its derivatives, or of indole-producing bacteria on the behaviours of C. elegans or other animals. Here, they show that C. elegans senses and moves toward indole and several indole-producing bacteria, but avoids non-indole producing pathogenic bacteria. Furthermore, it was found indole-producing and non-indole-producing bacteria exert divergent effects on the egg-laying behaviour of C. elegans, and that various indole derivatives also modulate chemotaxis, egg-laying behaviour and the survival of C. elegans. In contrast, indole at high concentration can kill C. elegans, which in turn, has the ability to detoxify indole by oxidation and glucosylation. Transcriptional analysis showed indole markedly up-regulated the gene expressions of cytochrome P450s, UDP-glucuronosyltransferases and glutathione S-transferase, which well explained the modification of indole by C. elegans while indole down-regulated the expressions of collagen and F-box genes. Their findings suggest that indole and its derivatives are important signalling molecules during bacteria-nematode interactions.

Cyanide Production by Chromobacterium piscinae Shields It from Bdellovibrio bacteriovorus HD100 Predation

“…One well-known secondary metabolite with defensive capabilities is indole. With respect to predation, indole is both toxic to the bacterivorous nematode Caenorhabditis elegans ( 5 ) and capable of blocking predation of Escherichia coli and Salmonella by the bacterial predator Bdellovibrio bacteriovorus HD100 ( 6 ). Indole is produced by both Gram-positive and Gram-negative bacteria ( 7 , 8 ) and can reach concentrations of up to 1.1 mM within mammalian guts ( 9 , 10 ).…”

“…Indole is produced by both Gram-positive and Gram-negative bacteria ( 7 , 8 ) and can reach concentrations of up to 1.1 mM within mammalian guts ( 9 , 10 ). With C. elegans , a significant loss in viability was seen when indole was present at 0.5 mM or higher ( 5 ), while concentrations between 1 and 2 mM inhibited B. bacteriovorus mobility and hindered its development within the bdelloplast ( 6 ).…”

Indole Biodegradation in Acinetobacter sp. Strain O153: Genetic and Biochemical Characterization

“…Indole acts as cell-to-cell signaling molecule that regulates the expression of several virulence genes (2-4), promotes biofilm formation (5-7), and mediates complex predator-prey interactions (8,9). At high concentrations, indole and its derivatives exhibit toxic activity to both prokaryotic cells and animals and are even considered mutagens (10).…”

Bioconversion of Biologically Active Indole Derivatives with Indole-3-Acetic Acid-Degrading Enzymes from Caballeronia glathei DSM50014

“…Indole itself has recently been recognized as an interkingdom signaling molecule [1]. It is produced mainly by gut bacteria following the activity of tryptophanase [2], but can alter the physiology and metabolism of a very wide range of organisms, including the producent itself [3,4], other bacteria [5,6], eukaryotes [7], and even mammals [8,9]. The 3-substituted derivatives of indole bearing a carboxylic acid group are regarded as auxins, the plant growth-regulating hormones.…”