Plant Invasions Associated with Change in Root-Zone Microbial Community Structure and Diversity

RESEARCH ARTICLE Plant Invasions Associated with Change in Root-Zone Microbial Community Structure and Diversity Richard R. Rodrigues1, Rosana P. Pineda2, Jacob N. Barney3, Erik T. Nilsen4, John E. Barrett4, Mark A. Williams1,2* 1 Interdisciplinary Ph.D. Program in Genetics, Bioinformatics, and Computational Biology, Virginia Tech, Blacksburg, Virginia, United States of America, 2 Department of Horticulture, Virginia Tech, Blacksburg, Virginia, United States of America, 3 Department of Plant Pathology, Physiology, and Weed Science, Virginia Tech, Blacksburg, Virginia, United States of America, 4 Department of Biological Sciences, Virginia Tech, Blacksburg, Virginia, United States of America * OPEN ACCESS Citation: Rodrigues RR, Pineda RP, Barney JN, Nilsen ET, Barrett JE, Williams MA (2015) Plant Invasions Associated with Change in Root-Zone Microbial Community Structure and Diversity. PLoS ONE 10(10): e0141424. doi:10.1371/journal. pone.0141424 Editor: Jian Liu, Shandong University, CHINA Received: June 10, 2015 Accepted: October 8, 2015 Published: October 27, 2015 Copyright: © 2015 Rodrigues et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: All relevant data are within the paper and its Supporting Information files. Data are submitted under Biosamples of SAMN04099948 - SAMN04099953, BioProject PRJNA296487, accession SRP064489 at NCBI (SRA). Funding: Funding provided by the Organismal Biology and Ecology program of the Fralin Institute of Virginia Tech to ETN, MAW, JNB, JEB; Genetics, bioinformatics, and computational biology program at Virginia Tech in support of RRR, MAW; College of agriculture and life sciences at Virginia Tech in support of MAW, RPP, RRR; and National Science 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. PLOS ONE | DOI:10.1371/journal.pone.0141424 October 27, 2015 1 / 19 Plant Invasions Associated with Change in Root-Zone Microbiome Foundation award 1216074 to MAW. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. Introduction Invasive plants are implicated in altering plant community dynamics, disturbance regimes, net primary productivity, and nutrient cycles [1–3], 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]. Important feedbacks between plants and the soil biotic community have begun to shed new light on plant rarity and invasiveness. High density of native species, such as Rhododendron maximum, reduced soil nutrient availability and mycorrhizae abundance associated with surrounding plants [6–9]. Alliaria petiolata in contrast, an invasive plant, reduced arbuscular mycorrhizal fungi (AMF) colonization of native trees and overall tree growth [10]. It was thought that the reduction in AMF occurred as a result of the plant releasing glucosinolate containing root exudates [5]. Relatively uncommon native plants were also 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]. Still, other effects related to soil nutrient cycling indicated that a mixture of the exotic grasses Avena barbata and Bromus hordeaceous had elevated levels of nitrate, ammonia oxidizers, microbial N, and gross nitrification rates compared to the native grass Nasella sp. [15]. Overall, these results show that microbial communities and their processes are altered due to the invasion of exotic plants, and provide evidence that invader and plants native to an ecosystem have underlying differences in their interactions with belowground microbial communities. Meta-analysis have concluded, specifically, that nitrogen turnover is greatly altered and often greater following exotic plant invasion of ecosystems dominated by native plants [16, 17]. Most of the microbial studies conducted have either been based on greenhouse plantings or field establishment o (...truncated)