Geology and climate influence rhizobiome composition of the phenotypically diverse tropical tree Tabebuia heterophylla

RESEARCH ARTICLE Geology and climate influence rhizobiome composition of the phenotypically diverse tropical tree Tabebuia heterophylla Yakshi Ortiz1, Carla RestrepoID1, Brayan Vilanova-Cuevas2, Eugenio Santiago-Valentin1, Susannah G. Tringe3, Filipa Godoy-VitorinoID2* 1 Department of Biology, University of Puerto Rico, San Juan, Puerto Rico, 2 Department of Microbiology and Medical Zoology, University of Puerto Rico, School of Medicine, San Juan, Puerto Rico, 3 Department of Energy, Joint Genome Institute, Walnut Creek, California, United States of America * filipa.godoy@upr.edu Abstract Plant-associated microbial communities have diverse phenotypic effects on their hosts that are only beginning to be revealed. We hypothesized that morpho-physiological variations in the tropical tree Tabebuia heterophylla, observed on different geological substrates, arise in part due to microbial processes in the rhizosphere. We characterized the microbiota of the rhizosphere and soil communities associated with T. heterophylla trees in high and low alti- tude sites (with varying temperature and precipitation) of volcanic, karst and serpentine geologies across Puerto Rico. We sampled 6 areas across the island in three geological materials including volcanic, serpentine and karst soils. Collection was done in 2 elevations (>450m and 0-300m high), that included 3 trees for each site and 4 replicate soil samples per tree of both bulk and rhizosphere. Genomic DNA was extracted from 144 samples, and 16S rRNA V4 sequencing was performed on the Illumina MiSeq platform. Proteobacteria,

Actinobacteria, and Verrucomicrobia were the most dominant phyla, and microbiomes clus- tered by geological substrate and elevation. Volcanic samples were enriched in Verrucomi- crobia; karst was dominated by nitrogen-fixing Proteobacteria, and serpentine sites harbored the most diverse communities, with dominant Cyanobacteria. Sites with similar cli- mates but differing geologies showed significant differences on rhizobiota diversity and composition demonstrating the importance of geology in shaping the rhizosphere micro- biota, with implications for the plant’s phenotype. Our study sheds light on the combined role of geology and climate in the rhizosphere microbial consortia, likely contributing to the phe- notypic plasticity of the trees. Introduction Plant phenotypic plasticity–the capacity to produce more than one phenotype from a single genotype–represents a plant’s response to environmental conditions [1–5], including nutrient availability and climatic conditions such as temperature and moisture [6]. Thus, plants of the PLOS ONE PLOS ONE | https://doi.org/10.1371/journal.pone.0231083 April 7, 2020 1 / 16 a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 OPEN ACCESS Citation: Ortiz Y, Restrepo C, Vilanova-Cuevas B, Santiago-Valentin E, Tringe SG, Godoy-Vitorino F (2020) Geology and climate influence rhizobiome composition of the phenotypically diverse tropical tree Tabebuia heterophylla. PLoS ONE 15(4): e0231083. https://doi.org/10.1371/journal. pone.0231083 Editor: Ying Ma, Universidade de Coimbra, PORTUGAL Received: September 3, 2019

Accepted: March 17, 2020 Published: April 7, 2020 Copyright: © 2020 Ortiz 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: Itag data can be downloaded from the JGI repository (https:// genome.jgi.doe.gov/portal/pages/ dynamicOrganismDownload.jsf?organism= Tabitaplate2_FD). Funding: Sequencing work was conducted by the U.S. Department of Energy Joint Genome Institute, a DOE Office of Science User Facility, supported by the Office of Science of the U.S. Department of Energy under Contract No. DE-AC02-05CH11231