Jeongeuplla avenae gen. nov., sp. nov., a novel β-carotene-producing bacterium that alleviates salinity stress in Arabidopsis

Front Microbiol. 2023 Dec 6:14:1265308. doi: 10.3389/fmicb.2023.1265308. eCollection 2023.

Abstract

A novel endophytic bacterium, designated DY-R2A-6T, was isolated from oat (Avena sativa L.) seeds and found to produces β-carotene. Phylogenetic analysis based on 16S rRNA gene sequences revealed that strain DY-R2A-6T had 96.3% similarity with Jiella aquimaris LZB041T, 96.0% similarity with Aurantimonas aggregate R14M6T and Aureimonas frigidaquae JCM 14755T, and less than 95.8% similarity with other genera in the family Aurantimonadaceae. The complete genome of strain DY-R2A-6T comprised 5,929,370 base pairs, consisting of one full chromosome (5,909,198 bp) and one plasmid (20,172 bp), with a G + C content was 69.1%. The overall genome-related index (OGRI), including digital DNA-DNA hybridization (<20.5%), ANI (<79.2%), and AAI (<64.2%) values, all fell below the thresholds set for novel genera. The major cellular fatty acids (>10%) of strain DY-R2A-6T were C16:0, C19:0 cyclo ω8c, and summed feature 8 (C18:1ω7c and/or C18:1ω6c). Ubiquinone-10 was the main respiratory quinone. We identified the gene cluster responsible for carotenoid biosynthesis in the genome and found that the pink-pigment produced by strain DY-R2A-6T is β-carotene. In experiment with Arabidopsis seedlings, co-cultivation with strain DY-R2A-6T led to a 1.4-fold increase in plant biomass and chlorophyll content under salt stress conditions, demonstrating its capacity to enhance salt stress tolerance in plants. Moreover, external application of β-carotene to Arabidopsis seedlings under salt stress conditions also mitigated the stress significantly. Based on these findings, strain DY-R2A-6T is proposed to represent a novel genus and species in the family Aurantimonadaceae, named Jeongeuplla avenae gen. nov., sp. nov. The type strain is DY-R2A-6T (= KCTC 82985T = GDMCC 1.3014T). This study not only identified a new taxon but also utilized genome analysis to predict and confirm the production of β-carotene by strain DY-R2A-6T. It also demonstrated the ability of this strain to enhance salt stress tolerance in plants, suggesting potential application in agriculture to mitigate environmental stress in crops.

Keywords: Arabidopsis; polyphasic taxonomy; reactive oxygen species; salt stress; β-carotene.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This study was funded by the Korea Research Institute of Bioscience and Biotechnology (KRIBB) Research Initiative Program (KGM5282331) and the Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (2020R111A2072308).