N-Acetylglucosamine Promotes Tomato Plant Growth by Shaping the Community Structure and Metabolism of the Rhizosphere Microbiome

Abstract

ABSTRACT Communication between plants and microorganisms is vital because it influences their growth, development, defense, propagation, and metabolism in achieving maximal fitness. N-acetylglucosamine (N-GlcNAc), the building block of bacterial and fungal cell walls, was first reported to promote tomato plant growth via stimulation of microorganisms typically known to dominate the tomato root rhizosphere, such as members of Proteobacteria and Actinobacteria. Using KEGG pathway analysis of the rhizosphere microbial operational taxonomic units, the streptomycin biosynthesis pathway was enriched in the presence of N-GlcNAc. The biosynthesis of 3-hydroxy-2-butanone (acetoin) and 2,3-butanediol, two foremost types of plant growth promotion-related volatile organic compounds, were activated in both Bacillus subtilis and Streptomyces thermocarboxydus strains when they were cocultured with N-GlcNAc. In addition, the application of N-GlcNAc increased indole-3-acetic acid production in a dose-dependent manner in strains of Bacillus cereus, Proteus mirabilis, Pseudomonas putida, and S. thermocarboxydus that were isolated from an N-GlcNAc-treated tomato rhizosphere. Overall, this study found that N-GlcNAc could function as microbial signaling molecules to shape the community structure and metabolism of the rhizosphere microbiome, thereby regulating plant growth and development and preventing plant disease through complementary plant–microbe interactions. IMPORTANCE While the benefits of using plant growth-promoting rhizobacteria (PGPRs) to enhance crop production have been recognized and studied extensively under laboratory conditions, the success of their application in the field varies immensely. More fundamentally explicit processes of positive, plant–PGPRs interactions are needed. The utilization of organic amendments, such as chitin and its derivatives, is one of the most economical and practical options for improving soil and substrate quality as well as plant growth and resilience. In this study, we observed that the chitin monomer N-GlcNAc, a key microbial signaling molecule produced through interactions between chitin, soil microbes, and the plants, positively shaped the community structure and metabolism of the rhizosphere microbiome of tomatoes. Our findings also provide a new direction for enhancing the benefits and stability of PGPRs in the field.

Keywords

• N-acetylglucosamine
• chitin
• rhizosphere microbiome
• Streptomyces
• acetoin
• indole-3-acetic acid