Abstract

The importance of plant-microbe associations for the invasion of plant species have not been often tested under field conditions. The research sought to determine patterns of change in microbial communities associated with the establishment of invasive plants with different taxonomic and phenetic traits. Three independent locations in Virginia, USA were selected. One site was invaded by a grass (Microstegium vimineum), another by a shrub (Rhamnus davurica), and the third by a tree (Ailanthus altissima). The native vegetation from these sites was used as reference. 16S rRNA and ITS regions were sequenced to study root-zone bacterial and fungal communities, respectively, in invaded and non-invaded samples and analyzed using Quantitative Insights Into Microbial Ecology (QIIME). Though root-zone microbial community structure initially differed across locations, plant invasion shifted communities in similar ways. Indicator species analysis revealed that Operational Taxonomic Units (OTUs) closely related to Proteobacteria, Acidobacteria, Actinobacteria, and Ascomycota increased in abundance due to plant invasions. The Hyphomonadaceae family in the Rhodobacterales order and ammonia-oxidizing Nitrospirae phylum showed greater relative abundance in the invaded root-zone soils. Hyphomicrobiaceae, another bacterial family within the phyla Proteobacteria increased as a result of plant invasion, but the effect associated most strongly with root-zones of M. vimineum and R. davurica. Functional analysis using Phylogenetic Investigation of Communities by Reconstruction of Unobserved States (PICRUSt) showed bacteria responsible for nitrogen cycling in soil increased in relative abundance in association with plant invasion. In agreement with phylogenetic and functional analyses, greater turnover of ammonium and nitrate was associated with plant invasion. Overall, bacterial and fungal communities changed congruently across plant invaders, and support the hypothesis that nitrogen cycling bacteria and functions are important factors in plant invasions. Whether the changes in microbial communities are driven by direct plant microbial interactions or a result of plant-driven changes in soil properties remains to be determined.

Highlights

  • Invasive plants are implicated in altering plant community dynamics, disturbance regimes, net primary productivity, and nutrient cycles [1,2,3], which threaten ecosystem functioning and stability

  • It is well known that invasive species have direct and indirect effects on the surrounding noninvaded plant community, especially through root exudates: Centaurea spp. [71]; Ailanthus altissima [72]; and Artemisia vulgaris [73]

  • Functional predictions based on the phylogeny of bacteria agreed with field measurements of N turnover rates and suggest that changes in N cycling bacteria, which include nitrifiers and diazotrophs, may be a significant cog in the success of invasive plant encroachment and success into non-invaded/remnant ecosystems

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Summary

Introduction

Invasive plants are implicated in altering plant community dynamics, disturbance regimes, net primary productivity, and nutrient cycles [1,2,3], which threaten ecosystem functioning and stability. The soil microbial community plays a central role in ecosystem functioning, including serving as plant symbionts, mediating plant nutrient acquisition, nutrient cycles, and soil formation [4] These belowground communities have been implicated in invasive species success, but only a few studies have assessed how belowground microbial taxa change with plant invasions into ecosystems [5]. Uncommon native plants were shown to be more negatively affected by pathogens while invaders, in contrast, showed evidence of more positive plant-microbial feedbacks [11, 12] These results have been further corroborated using reciprocal transplant studies of plant-soil-microbial feedbacks associated with invaded and native ranges of Triadica sebifera [13] and Pinus contorta [14]. Meta-analysis have concluded, that nitrogen turnover is greatly altered and often greater following exotic plant invasion of ecosystems dominated by native plants [16, 17]

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