Caenorhabditis elegans Extracts Stimulate IAA Biosynthesis in Arthrobacter pascens ZZ21 via the Indole-3-pyruvic Acid Pathway

Abstract

Inter-organismal metabolites play important roles in regulating organism behavior and the communication between organisms. Nematodes, the most abundant animals on earth, are crucial participants in soil ecosystems through their interactions with microbes. For example, bacterial-feeding nematodes increase the activity of indole-3-acetic acid (IAA)-producing bacteria and the IAA content in soil. However, the way in which these nematodes interact with bacteria and affect IAA biosynthesis is not well understood. Here, using the model nematode Caenorhabditis elegans and the plant-beneficial bacterium Arthrobacter pascens ZZ21, we examined the effects of nematode excretions or extracts on bacterial IAA biosynthesis. To explore the underlying regulatory mechanism in more detail, we performed transcriptome sequencing and metabolomic analysis. Our findings suggest that C. elegans extracts promote IAA biosynthesis in A. pascens ZZ21 by increasing the expression of genes and the abundance of intermediates involved in the indole-3-pyruvic acid (IPyA) pathway. C. elegans extracts also significantly influenced biosynthetic and metabolic activity in A. pascens ZZ21. Treatment with C. elegans extracts promoted pyruvate metabolism, the citrate cycle (TCA) cycle and the production of some TCA-cycle-related amino acids and inhibited oxidative phosphorylation, which induced the accumulation of reduced nicotinamide adenine dinucleotide (NADH). We propose that the extracts altered the metabolism of A. pascens ZZ21 to help the bacteria resist stress caused by their predator. Our findings indicate that bacterial-feeding nematodes mediate the interaction between nematodes and bacteria via their extracts, providing insights into the ecological function of C. elegans in soil.