Leaf, root, and soil microbiomes of an invasive plant, Ardisia crenata, differ between its native and exotic ranges

Front Microbiol. 2023 Nov 22:14:1302167. doi: 10.3389/fmicb.2023.1302167. eCollection 2023.

Abstract

Introduction: Ecological underpinnings of the invasion success of exotic plants may be found in their interactions with microbes, either through the enemy release hypothesis and the enhanced mutualism hypothesis. Whereas recent high-throughput sequencing techniques have significantly expanded our understanding of plant-associated microbiomes and their functional guilds, few studies to date have used these techniques to compare the microbiome associated with invasive plants between their native and exotic ranges.

Methods: We extracted fungal and bacterial DNA within leaf endosphere, root endosphere and soil of an invasive plant, Ardisia crenata, sampled from their native range Japan and exotic range Florida, USA. Using Illumina sequencing data, we compared microbial community compositions and diversity between the native and exotic ranges, and tested whether abundance of pathogenic or mutualistic microbes differ between the native or exotic ranges in accordance to the enemy release hypothesis or the enhanced mutualism hypothesis.

Results: Fungal and bacterial community compositions differed among leaves, roots and soil, and between the native and exotic ranges. Despite a higher microbial diversity in the soil in the exotic range than in the native range, the microbial diversity within leaf and root was lower in the exotic range compared to the native range. In addition, leaves in the native range harbored a greater number of plant pathogenic fungi compared to those in the exotic range.

Discussion: These patterns suggest plant controls over what microbes become associated with leaves and roots. The higher abundance of leaf pathogenic fungi, including the pathogen which is known to cause specific disease in A. crenata in the exotic range than in the native range, support the enemy release hypothesis and highlighted potential importance of examining microbial communities both above- and below-ground.

Keywords: bacteria; exotic invasive species; functional guilds; fungi; leaf endophytes; next generation sequencing; plant-microbe interactions; soil microbial community.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. Research and publication of this article was supported by the Management Expense Grant of Kyoto University.