Enriched root bacterial microbiome in invaded vs native ranges of the model grass allotetraploid Brachypodium hybridum

Biological Invasions, Dec 2021

Invasive species can shift the composition of key soil microbial groups, thus creating novel soil microbial communities. To better understand the biological drivers of invasion, we studied plant-microbial interactions in species of the Brachypodium distachyon complex, a model system for functional genomic studies of temperate grasses and bioenergy crops. While Brachypodium hybridum invasion in California is in an incipient stage, threatening natural and agricultural systems, its diploid progenitor species B. distachyon is not invasive in California. We investigated the root, soil, and rhizosphere bacterial composition of Brachypodium hybridum in both its native and invaded range, and of B. distachyon in the native range. We used high-throughput, amplicon sequencing to evaluate if the bacteria associated with these plants differ, and whether biotic controls may be driving B. hybridum invasion. Bacterial community composition of B. hybridum differed based on provenance (native or invaded range) for root, rhizosphere, and bulk soils, as did the abundance of dominant bacterial taxa. Bacteroidetes, Cyanobacteria and Bacillus spp. (species) were significantly more abundant in B. hybridum roots from the invaded range, whereas Proteobacteria, Firmicutes, Erwinia and Pseudomonas were more abundant in the native range roots. Brachypodium hybridum forms novel biotic interactions with a diverse suite of rhizosphere microbes from the invaded range, which may not exert a similar influence within its native range, ostensibly contributing to B. hybridum’s invasiveness. These associated plant microbiomes could inform future management approaches for B. hybridum in its invaded range and could be key to understanding, predicting, and preventing future plant invasions.

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Enriched root bacterial microbiome in invaded vs native ranges of the model grass allotetraploid Brachypodium hybridum

Biol Invasions https://doi.org/10.1007/s10530-021-02692-4 (0123456789().,-volV) ( 01234567 89().,-volV) ORIGINAL PAPER Enriched root bacterial microbiome in invaded vs native ranges of the model grass allotetraploid Brachypodium hybridum Brooke Pickett . Chelsea J. Carey . Keshav Arogyaswamy . Jon Botthoff . Mia Maltz . Pilar Catalán . Emma L. Aronson Received: 15 July 2021 / Accepted: 17 November 2021  The Author(s) 2021 Abstract Invasive species can shift the composition of key soil microbial groups, thus creating novel soil microbial communities. To better understand the biological drivers of invasion, we studied plantmicrobial interactions in species of the Brachypodium distachyon complex, a model system for functional genomic studies of temperate grasses and bioenergy crops. While Brachypodium hybridum invasion in California is in an incipient stage, threatening natural and agricultural systems, its diploid progenitor species B. distachyon is not invasive in California. We investigated the root, soil, and rhizosphere bacterial composition of Brachypodium hybridum in both its native and invaded range, and of B. distachyon in the native range. We used high-throughput, amplicon sequencing to evaluate if the bacteria associated with these plants differ, and whether biotic controls may be Supplementary Information The online version contains supplementary material available at https://doi.org/10.1007/ s10530-021-02692-4. B. Pickett (&) Division of Biological Sciences, University of California, San Diego, San Diego, CA 92093, USA e-mail: J. Botthoff  M. Maltz  E. L. Aronson Center for Conservation Biology, University of California, Riverside, CA 3411, USA e-mail: B. Pickett  C. J. Carey  K. Arogyaswamy  M. Maltz  E. L. Aronson (&) Department of Microbiology and Plant Pathology, University of California, Riverside, Riverside, CA, USA e-mail: P. Catalán Departamento de Ciencias Agrarias y del Medio Natural, Escuela Politécnica Superior de Huesca, Universidad de Zaragoza, Zaragoza, Spain e-mail: C. J. Carey e-mail: P. Catalán Grupo de Bioquı́mica, Biofı́sica y Biologı́a Computacional (BIFI, UNIZAR), Unidad Asociada al CSIC, Zaragoza, Spain K. Arogyaswamy e-mail: M. Maltz e-mail: P. Catalán Tomsk State University, Tomsk, Russia C. J. Carey Point Blue Conservation Science, Petaluma, CA, USA 123 B. Pickett et al. driving B. hybridum invasion. Bacterial community composition of B. hybridum differed based on provenance (native or invaded range) for root, rhizosphere, and bulk soils, as did the abundance of dominant bacterial taxa. Bacteroidetes, Cyanobacteria and Bacillus spp. (species) were significantly more abundant in B. hybridum roots from the invaded range, whereas Proteobacteria, Firmicutes, Erwinia and Pseudomonas were more abundant in the native range roots. Brachypodium hybridum forms novel biotic interactions with a diverse suite of rhizosphere microbes from the invaded range, which may not exert a similar influence within its native range, ostensibly contributing to B. hybridum’s invasiveness. These associated plant microbiomes could inform future management approaches for B. hybridum in its invaded range and could be key to understanding, predicting, and preventing future plant invasions. Keywords Endophytic bacteria  Brachypodium  Invasive species  Rhizosphere  Root  Soil Abbreviations spp QIIME PERMANOVA PCoA Hill 0 Hill 1 OTU N N2 Species Quantitative insights into microbial ecology Permutational multivariate analyses of variance Principal Coordinates Analysis Hill number of 0 Hill number of 1 Operational taxonomic unit Nitrogen Dinitrogen Background Invasive species are eroding native biodiversity and ecosystem services in natural areas around the world, concerning resource conservation practitioners and land managers who are actively involved in reducing the spread of invasive species. While we are beginning to understand abiotic factors, such as resource availability, driving plant invasions (Corbin and D’Antonio 2012), we still have a limited understanding of the biological factors contributing to these invasions (Callaway et al. 2004; Dawson and Schrama 2016). 123 This is particularly true for relationships between plant invasion and microbial communities, despite ongoing research in this area (Egidi and Franks 2018; Le Roux et al. 2017; Lu et al. 2018; Ramirez et al. 2019). Root-associated and rhizosphere microbes, which can differ based on geographic location and soil type, can directly and indirectly influence nutrient supplies, pathogen loads, and invasive host plants’ stress tolerance. Although plant-soil feedbacks between invasive species and their associated microbes remain difficult to interpret, previous studies demonstrate that invasive species can shift the composition of key soil microbial groups, thus creating novel soil microbial communities (Busby et al. 2011; Hausmann and Hawkes 2009; Phillips et al. 2019; Zhang et al. 2010). Despite these insights, we have much to learn about the microbial dynamics of root and rhizosphere communities associated with invasive plants, and how they might differ across native and invaded ranges. Greater understanding of these dynamics could help us develop hypotheses about whether invasion may be partially controlled by biotic mechanisms, while providing important contextual information to better understand, predict, prevent and control plant invasions. When investigating the plant-associated microbial community, it can be insightful to characterize different plant-associated microbiomes, such as endophytic root, rhizosphere, and bulk soil communities. The rhizosphere (i.e. plant-root interface) is a structured microhabitat driven by plant physiological processes and inhabited by numerous microbes (Hartmann et al. 2009; Hintner 1904). Previous studies show that rhizosphere microbial communities are influenced by site history and soil type, and may often illustrate greater similarities to bulk soil communities of the same site than to rhizosphere communities of other sites (Bakker et al. 2015; de Ridder-Duine et al. 2005; Singh et al. 2007). In invaded ecosystems, inputs from invasive plant species may differ from those of native plant species, and may influence root-associated and rhizosphere microbes (Reinhart et al. 2010; Wolfe and Klironomos 2005), invasive plant success (Inderjit and van der Putten 2010), and subsequent restoration outcomes (Richardson et al. 2011). Biotic interactions among invasive plants, rhizosphere soil, or rootassociated microbes at the plant-root interface (i.e., rhizosphere mechanisms) could promote invasion, ostensibly due to the invasive plant producing foreign Enriched root bacterial microbiome in invaded vs native ranges of the model grass… Fig. 1 Effective species count (Hill number of order 0) and Exponent of Shannon diversity (Hill number of order 1) for each microbiome pool between B. hybridum native and invaded range root, (...truncated)


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Pickett, Brooke, Carey, Chelsea J., Arogyaswamy, Keshav, Botthoff, Jon, Maltz, Mia, Catalán, Pilar, Aronson, Emma L.. Enriched root bacterial microbiome in invaded vs native ranges of the model grass allotetraploid Brachypodium hybridum, Biological Invasions, 2021, pp. 1-20, DOI: 10.1007/s10530-021-02692-4