Streptomyces cocklensis DSM 42063 and Actinacidiphila bryophytorum DSM 42138 Colonize Arabidopsis thaliana and Modulate Its Proteome

Streptomycetaceae are found ubiquitously within plant microbiota. Several species belonging to this family are plant growth-promoting bacteria or may inhibit phytopathogens. Such bacteria therefore exert crucial functions in host development and resistance to stresses. Recent studies have shown that plants select beneficial bacteria into their microbiota. However, the selection process and the molecular mechanisms by which selected bacteria modulate the physiology of their host are not yet fully understood. Previous work revealed that the metabolic status of Arabidopsis thaliana was crucial for the selection of Streptomycetaceae into the microbiota, in particular bacteria phylogenetically related to Streptomyces cocklensis or Actinacidiphila bryophytorum (previously named Streptomyces bryophytorum). Here, the Arabidopsis-Streptomycetaceae interaction was further depicted by inoculating axenic A. thaliana with S. cocklensis DSM 42063 or A. bryophytorum DSM 42138. We showed that these two bacteria colonize A. thaliana ecotype Columbia-0 plants, but the colonization efficiency is reduced in a chs5 mutant of the same ecotype, being altered in isoprenoid, phenylpropanoid, and lipid profiles. We observed that A. bryophytorum inhibits growth of the chs5 mutant but not of the wild type, suggesting that the Arabidopsis-Actinacidiphila interaction depends on the metabolic status of the host. Using a mass spectrometry-based proteomic approach, we showed that S. cocklensis and A. bryophytorum modulate the A. thaliana proteome, in particular components involved in photosynthesis or phytohormone homeostasis. This study unveils specific aspects of the Arabidopsis-Streptomycetaceae interaction and highlights its complexity and diversity. [Figure: see text] Copyright © 2024 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.