LETTER
doi:10.1038/nature11336
Revealing structure and assembly cues for
Arabidopsis root-inhabiting bacterial microbiota
Davide Bulgarelli
1
*, Matthias Rott
1
*, Klaus Schlaeppi
1
*, Emiel Ver Loren van Themaat
1
*, Nahal Ahmadinejad
1
{, Federica Assenza
1
,
Philipp Rauf
1
{, Bruno Huettel
2
, Richard Reinhardt
2
, Elmon Schmelzer
3
, Joerg Peplies
4
, Frank Oliver Gloeckner
4,5
, Rudolf Amann
5
,
Thilo Eickhorst
6
& Paul Schulze-Lefert
1
The plant root defines the interface between a multicellular eukaryote
and soil, one of the richest microbial ecosystems on Earth
1
. Notably,
soil bacteria are able to multiply inside roots as benign endophytes
and modulate plant growth and development
2
, with implications
ranging from enhanced crop productivity
3
to phytoremediation
4
.
Endophytic colonization represents an apparent paradox of plant
innate immunity because plant cells can detect an array of microbe-
associated molecular patterns (also known as MAMPs) to initiate
immune responses to terminate microbial multiplication
5
. Several
studies attempted to describe the structure of bacterial root endo-
phytes
6
; however, different sampling protocols and low-resolution
profiling methods make it difficult to infer general principles. Here
we describe methodology to characterize and compare soil- and root-
inhabiting bacterial communities, which reveals not only a function
for metabolically active plant cells but also for inert cell-wall features
in the selection of soil bacteria for host colonization. We show that the
roots of Arabidopsis thaliana, grown in different natural soils under
controlled environmental conditions, are preferentially colonized by
Proteobacteria, Bacteroidetes and Actinobacteria, and each bacterial
phylum is represented by a dominating class or family. Soil type
defines the composition of root-inhabiting bacterial communities
and host genotype determines their ribotype profiles to a limited
extent. The identification of soil-type-specific members within the
root-inhabiting assemblies supports our conclusion that these rep-
resent soil-derived root endophytes. Surprisingly, plant cell-wall
features of other tested plant species seem to provide a sufficient
cue for the assembly of approximately 40% of the Arabidopsis
bacterial root-inhabiting microbiota, with a bias for Betaproteobacteria.
Thus, this root sub-community may not be Arabidopsis-specific but
saprophytic bacteria that would naturally be found on any plant
root or plant debris in the tested soils. By contrast, colonization of
Arabidopsis roots by members of the Actinobacteria depends on
other cues from metabolically active host cells.
We have grown Arabidopsis ecotypes Shakdara (Sha) and Landsberg
erecta (Ler) in natural soils of contrasting geochemistry, designated
Cologne (clay- and silt-rich) or Golm (sand- rich) soil, under
controlled environmental conditions and at a defined planting density
(Supplementary Fig. 1 and Supplementary Table 1). At early flowering
stage we collected samples from three compartments: ‘unplanted soil’
(number of replicates: Cologne n
C
5 13, Golm n
G
5 12), ‘rhizosphere’
(n
C
5 15, n
G
5 12) and ‘root’ (n
C
5 18, n
G
5 14). The ‘rhizosphere
compartment’ defines the soil particles firmly attached to roots
collected by centrifugation of root washings (Supplementary Movie
1). The ‘root compartment’ is defined as root tissue depleted of soil
particles and epiphytic bacteria by sequential washing and sonication
treatments and is therefore enriched for root-inhabiting bacteria
(Supplementary Fig. 2). We used pyrosequencing of an approximately
400 base pairs PCR amplicon of the bacterial 16S ribosomal RNA gene
and analysed the variable gene segments V5–V6.
To examine the taxonomic structure of the bacterial communities
we performed a supervised taxonomy classification of all high quality
reads using the SILVA
7
database. This classification identified a total of
43 bacterial phyla and divisions and revealed an anomalous
Chloroflexi abundance in all samples (Fig. 1a). PCR-independent
catalysed reporter deposition-fluorescence in situ hybridization
(CARD-FISH) analysis on soil samples (Supplementary Fig. 3) and
comparative PCR primer analysis indicated this is due to a PCR primer
bias (Supplementary Information and Supplementary Fig. 4). After
removal of reads assigned to Chloroflexi we identified Proteobacteria,
Actinobacteria and Bacteroidetes as dominating phyla in root bacterial
communities and significantly enriched compared to soil and
*These authors contributed equally to this work.
1
Department of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research, 50829 Cologne, Germany.
2
Max Planck Genome Centre, Max Planck Institute for Plant Breeding Research,
50829 Cologne, Germany.
3
Central Microscopy, Max Planck Institute for Plant Breeding Research, 50829 Cologne, Germany.
4
Ribocon GmbH, 28359 Bremen, Germany.
5
Department of Molecular
Ecology, Max Planck Institute for Marine Microbiology, 28359 Bremen, Germany.
6
Soil Science, Faculty of Biology and Chemistry, University of Bremen, 28359 Bremen, Germany. {Present addresses:
INRES - Crop Bioinformatics, University of Bonn, 53115 Bonn, Germany (N.A.); Department of Developmental Immunology, Max Planck Institute of Immunobiology and Epigenetics, 79108 Freiburg,
Germany (P.R.).
Chlorolexi
Acidobacteria
Planctomycetes
Firmicutes
TM7
Bacteroidetes
Actinobacteria
Proteobacteria
Flavobacteriaceae
Streptomycetaceae
Rhizobiaceae
Comamonadaceae
Oxalobacteraceae
Pseudomonadaceae
Xanthomonadaceae
a
b
c
0
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1,000
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1,000
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Relative abundance (‰)
Soil Rhizosphere Root
Bacteroidetes
Actinobacteria
Alphaproteobacteria
Betaproteobacteria
Gammaproteobacteria
Golm soil
Cologne soil
Figure 1 | Taxa at high taxonomic ranks define building blocks of root-
associated bacterial communities. a, Average relative abundance
(% 6 s.e.m.) of the phylum Chloroflexi detected in the indicated
compartments. b, Average relative abundance (% 6 s.e.m.) of the dominant
phyla (. 5 %) detected in root compartments of the indicated soil types.
c, Average relative abundance (% 6 s.e.m.) of families belonging to the three
dominant phyla in the root compartment. In b and c average relative
abundances are calculated after removal of reads assigned to Chloroflexi.
Asterisks indicate significant enrichment (Benjamini–Hochberg false-
discovery-rate (FDR) adjusted P value , 0.05) in the root compartment
compared to soil and rhizosphere compartments.
2 AUGUST 2012 | VOL 488 | NATURE | 91
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