Abstract

Bacterial indole-3-acetic acid (IAA), an effector molecule in microbial physiology, plays an important role in plant growth-promotion. Here, we comprehensively analyzed about 7282 prokaryotic genomes representing diverse bacterial phyla, combined with root-associated metagenomic data to unravel the distribution of tryptophan-dependent IAA synthesis pathways and to quantify the IAA synthesis-related genes in the plant root environments. We found that 82.2% of the analyzed bacterial genomes were potentially capable of synthesizing IAA from tryptophan (Trp) or intermediates. Interestingly, several phylogenetically diverse bacteria showed a preferential tendency to utilize different pathways and tryptamine and indole-3-pyruvate pathways are most prevalent in bacteria. About 45.3% of the studied genomes displayed multiple coexisting pathways, constituting complex IAA synthesis systems. Furthermore, root-associated metagenomic analyses revealed that rhizobacteria mainly synthesize IAA via indole-3-acetamide (IAM) and tryptamine (TMP) pathways and might possess stronger IAA synthesis abilities than bacteria colonizing other environments. The obtained results refurbished our understanding of bacterial IAA synthesis pathways and provided a faster and less labor-intensive alternative to physiological screening based on genome collections. The better understanding of IAA synthesis among bacterial communities could maximize the utilization of bacterial IAA to augment the crop growth and physiological function.

Highlights

  • Indole-3-acetic acid (IAA) is a crucial phytohormone in plant development, controlling many important physiological processes, including cell enlargement and division, tissue differentiation, and responses to light and gravity [1]

  • We found that 18.5% or 82.2% of bacteria from diverse environments could potentially synthesize indole-3-acetic acid (IAA) from Trp or intermediates, respectively, so this phenomenon emphasized that IAA probably has a profound impact on shaping microbial physiology

  • A recent study on cobamide biosynthesis in bacteria revealed that many bacteria only contained incomplete pathways and the authors experimentally verified that bacteria could truly synthesize cobamide from intermediates [30]

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Summary

Introduction

Indole-3-acetic acid (IAA) is a crucial phytohormone in plant development, controlling many important physiological processes, including cell enlargement and division, tissue differentiation, and responses to light and gravity [1]. The ability to synthesize IAA is a well-characterized trait in many plant growth-promoting bacteria [2]. Several experiments have proven that bacterial IAA enhances plant growth [3,4,5,6]. Bacterial IAA is known as a notorious virulence factor which could induce gall tumors [7,8]. In addition to its involvement in bacteria–plant interactions, IAA plays an important role in microbial physiology.

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