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
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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)