Revealing Microbiome Structure and Assembly Process in Three Rhizocompartments of Achyranthes bidentata Under Continuous Monoculture Regimes

Juanying Wang; Hongmiao Wu; Linkun Wu; Ye Liu; Puleng Letuma; Xianjin Qin; Ting Chen; Christopher Rensing; Sheng Lin; Wenxiong Lin

doi:10.3389/fmicb.2021.677654

Revealing Microbiome Structure and Assembly Process in Three Rhizocompartments of Achyranthes bidentata Under Continuous Monoculture Regimes

Front Microbiol. 2021 Jun 14:12:677654. doi: 10.3389/fmicb.2021.677654. eCollection 2021.

Authors

Juanying Wang^{1

2}, Hongmiao Wu^{1

2}, Linkun Wu^{1

2}, Ye Liu^{1

2}, Puleng Letuma³, Xianjin Qin^{2

4}, Ting Chen^{1

2}, Christopher Rensing⁵, Sheng Lin^{1

2}, Wenxiong Lin^{1

2}

Affiliations

¹ Fujian Provincial Key Laboratory of Agroecological Processing and Safety Monitoring, College of Life Sciences, Fujian Agriculture and Forestry University, Fuzhou, China.
² Key Laboratory for Genetics, Breeding and Multiple Utilization of Crops, Ministry of Education, College of Crop Sciences, Fujian Agriculture and Forestry University, Fuzhou, China.
³ Department of Crop Science, National University of Lesotho, Maseru, Lesotho.
⁴ College of Crop Sciences, Fujian Agriculture and Forestry University, Fuzhou, China.
⁵ Fujian Provincial Key Laboratory of Soil Environmental Health and Regulation, College of Resources and Environment, Fujian Agriculture and Forestry University, Fuzhou, China.

Abstract

The complex composition and interaction of root-associated microbes are critical to plant health and performance. In this study, we presented a detailed characterization of three rhizocompartment (rhizosphere, rhizoplane, and root) microbiomes of Achyranthes bidentata under different years of consecutive monoculture by deep sequencing in order to determine keystone microorganisms via co-occurrence network analysis. The network analysis showed that multiple consecutive monoculture (MCM, represented 5Y and 10Y) soils generated some distinct beneficial bacterial taxa such as Bacillus, Fictibacillus, Bradyrhizobium, Shinella, and Herbaspirillum. For fungi, Mortierella substituted for Fusarium in occupying an important position in different rhizocompartments under A. bidentate monoculture. Quantitative PCR analysis confirmed a significant increase in Bacillus, Pseudomonas, and Burkholderia spp. The results of the inoculation assay showed that addition of beneficial bacteria Bacillus subtilis 74 and Bacillus halodurans 75 significantly increased the root length and fresh weight of A. bidentata. Furthermore, three types of phytosterones, as the main allochemicals, were identified both in the rhizosphere soil and in culture medium under sterile conditions by LC-MS/MS. When looking at in vitro interactions, it was found that phytosterones displayed a positive interaction with dominant beneficial species (Bacillus amyloliquefaciens 4 and B. halodurans 75) and had a negative effect on the presence of the pathogenic fungi Fusarium solani and Fusarium oxysporum. Overall, this study demonstrated that consecutive monoculture of A. bidentata can alter the bacterial and fungal community by secreting root exudates, leading to recruitment of beneficial microbes and replacement of plant-specific pathogenic fungi with plant beneficial fungi.

Keywords: co-occurrence network; plant–soil interactions; rhizoplane; rhizosphere; root.