Biodiversity Data Journal 9: e63086 CO)
doi: 10.3897/BDJ.9.e63086 open access

Research Article

Cataloguing the bacterial diversity in the active
ectomycorrhizal zone of Astraeus from a dry
deciduous forest of Shorea

Vineet Vishal*:$, Somnath Singh Munda?, Geetanjali Singh*, Shalini Lal*

+ Department of Botany, Dr Shyama Prasad Mukherjee University, Ranchi-834008, India
§ Department of Botany, Bangabasi Evening College, Kolkata-700009, India

Corresponding author: Shalini Lal (shalini.kumari@gmail.com)

Academic editor: Vesela Evtimova

Received: 13 Jan 2021 | Accepted: 26 Apr 2021 | Published: 19 May 2021

Citation: Vishal V, Munda SS, Singh G, Lal S (2021) Cataloguing the bacterial diversity in the active
ectomycorrhizal zone of Astraeus from a dry deciduous forest of Shorea. Biodiversity Data Journal 9: e63086.
https://doi.org/10.3897/BDJ.9.e63086

Abstract

The plant microbiome has been considered one of the most researched areas of microbial
biodiversity, yet very little information is available on the microbial communities prevailing
in the mushroom's ectomycorrhizosphere. Ectomycorrhizal symbioses often result in the
formation of a favourable niche which enables the thriving of various microbial symbionts
where these symbionts endorse functions, such as quorum sensing, biofilm formation,
volatile microbial compound (VOC) production, regulation of microbial gene expression,
symbiosis and virulence. The identification of hidden uncultured microbial communities
around the active ectomycorrhizal zone of Astraeus from dry deciduous sal forest of
Jharkhand, India was carried out using MinION Oxford Nanopore sequencing of 16S rRNA
amplicons genes. High richness of Operational Taxonomic Units (1,905 OTUs) was
observed. We recorded 25 distinct phyla. Proteobacteria (36%) was the most abundant
phylum, followed by Firmicutes (28%), Actinobacteria (10%) and Bacteroidetes (6%),
whereas Gammaproteobacteria was the most abundant class of bacterial communities in
the active ectomycorrhizal zone. The ectomycorrhizosphere soil has abundant phosphate-
solubilising bacteria (PSB). This is the first report of the ectomycorrhizosphere microbiome
associated with Astraeus.

© Vishal V et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY
4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are
credited.

2 Vishal V et al

Keywords

Astraeus, Ectomycorrhizae, Gammaproteobacteria, microbiome, PSB, OTUs

Introduction

Mycorrhizal symbioses are ubiquitous and form a major component of the microbiota in
most boreal, temperate and dry deciduous tropical forest ecosystems. They contribute
huge amounts of organic carbon fluxes from leaf-litter, wood or plant biomass, resulting in
an enrichment of the microbial populace and their associated functions. The
ectomycorrhizosphere is a zone of active interchange between plant root and soil
microorganisms (ectomycorrhizal fungi and bacteria) that can inhibit or stimulate each
other (Poole et al. 2001). The ectomycorrhizosphere also serves as a nutritional hotspot for
microbes which benefit forest trees in a number of ways. Moreover, the
ectomycorrhizosphere microbiome is driving processes like quorum sensing, regulation of
microbial gene expression, symbiosis, biofilm formation, antibiotic production, motility,
conjugation, virulence etc. (Churchland and Grayston 2014). Garbaye (1994) and Bonfante
and Anca (2009) suggested that bacteria could potentially stimulate mycorrhizal formation,
assist in the fungal-plant recognition system and receptivity of the host root to the
mycorrhizal fungus. Uroz et al. (2007), Uroz and Oger (2015) isolated 61 bacterial strains
from the ectomycorrhizosphere of an oak forest, where they have experimentally shown
that bacteria (Burkholderia, Collimonas, Pseudomonas and Sphingomonas) and
ectomycorrhizal fungi (Scleroderma citrinum) are jointly involved in mineral weathering and
solubilisation processes.

Mushrooms are one of the finest creations in nature and exhibit wide variation. The wild
edible mushrooms of Astraeus Phosri. (order Boletales), inhabiting the roots of Shorea
robusta Gaertn., are a group of epigeous non-hygroscopic macro fungi found only during
the monsoon season. They are recognised by the star-like pattern at maturity (Phosri et al.
2007) and are commonly known as earthstar. These ectomycorrhizal edible fungi grow
extensively in the sandy and red laterite soil of Dipterocarp sal dry deciduous forest. Owing
to their high nutritional property, these mushrooms are sold regularly in local markets
during the monsoon season. However, due to changes in climatic conditions, decrease in
rainfall, global warming and unauthorised anthropogenic influence, the production is
declining rapidly, causing serious threats to these mushrooms. Although there are many
reports on the morphology, photochemistry and nutritional property of Astraeus, little is
known about the effect of bacteria on the growth and development of mushrooms of
Astraeus. This may be one of the reasons that, despite nearly a decade of research,
attempts to cultivate Astraeus have largely been unsuccessful (Trappe 1967, Petcharat
2003, Biswas et al. 2017, Biswas et al. 2011).

A detailed study on the biology and fruiting body production of Astraeus in a forest of sal
and the co-occurrence between this fungus and other microbes (especially bacteria), is
very important for a successful cultivation of mushroom and for a better yield. The main
objective of the present work was to collect soil samples from a dry deciduous sal forest

Cataloguing the bacterial diversity in the active ectomycorrhizal zone ... 3

and to analyse the abundance of microorganisms around the ectomycorrhizosphere of
Astraeus. In order to evaluate the optimum microbial content for proper nourishment of the
taxon, the MinlION Oxford Nanopore 16s amplicon sequencing platform was used.

Material and Methods

Collection and sample preparation

Rhizosphere samples of ectomycorrhizosphere (RUGA-1) were collected from the village
of Bandgaon under the Porahat forest division, West Singhbhum, Jharkhand, India (
22.84°N, 85.35°E; Fig. 1) from a dry deciduous forest of Shorea during the monsoon
season in July 2019. The soil in this region is red laterite and sandy, having a thin organic
layer. The soil samples (n = 3) were collected at a depth of 5-10 cm. The separation of the
soil samples into ectomycorrhizosphere were performed in the lab. Plant roots were
carefully eliminated from the soil and shaken gently to remove loosely adhering soil.
Ectomycorrhizosphere soils were sieved (2 mm mesh) and homogenised prior to freezing
(Uroz et al. 2010).

[a |
‘Sahibganj
Godda
\

DISTRICT OF
WEST SINGHBHUM

0 250 500 1.000 Km

5 Le Ee

Figure 1. EES]
Area of study and collection of soil samples. A. Location and collection sites of soil samples
from Porahat forest division (22.84°N, 85.35°E) of West Singhbhum District of Jharkhand
State of India; B. Satellite image of the collection site; C. Natural vegetation of forest of Shorea
from Porahat forest division; D-E. Collection of ectomycorrhizosphere soil samples. Scale bar
C-D = 20 mm.

DNA extraction, 16S rRNA gene amplification and sequencing

From a minimum of 1 g of soil, DNA was isolated using the EXpure Microbial DNA isolation
kit (BogarBio Bee stores Pvt Ltd). DNA concentration was measured using a Qubit

4 Vishal V et al

Flurometer 3.0 and DNA was stored at -20°C. Full-length 16S rRNA gene was amplified
using the primers 27F (5'-AGAGTTTGATCCTGGCTCAG-3') and 1492R = (5'-
GGTTACCTTGTTACGACTT-3'). Metagenomic 16s amplicon sequencing was performed
by taking 1 ug of DNA template using MinlION Oxford Nanopore platform at Yaaz Xenomics
(Coimbatore, India). The raw fastq files were uploaded to the metagenome rapid
annotation using subsystem technology (MG-RAST server; see Aziz et al. 2008) and
annotated using default parameters. Artificial duplicate reads were eliminated using
DRISEE (Duplicate Read Inferred Sequencing Error Estimation; see Gomez-Alvarez et al.
2009). Taxonomic assignment of the ectomycorrhizosphere reads were performed with the
analysis tools provided by MG-RAST, using the Greengenes (DeSantis et al. 2006), RDP
(Cole et al. 2014) and SILVA SSU (Quast et al. 2012). As a reference database, we used a
minimum cut-off identity of 60% and e-value of 5. The final taxonomy was decided, based
on the best BLAST match for given representative sequence reads of the above dataset.
The metagenome data are available at the NCBI - Sequence Read Archive with accession
number: SRX8009931.

Results

After QC and deduplication, a total of 50,213 reads with size 13,969,056 bp with an
average length of 278 bp and G+C% 50+4 dataset were recovered from the active zone of
ectomycorrhizosphere (RUGA-1). Taxonomic assignment was performed with the analysis
tools provided by MG-RAST, using the SILVA SSU as a reference database with the default
parameters, as it provides maximum number of matched reads, based on the BLAST score
compared with RDP and Greengenes databases (Table 1). High species richness was
observed in ectomycorrhizosphere. The reads were clustered using > 97% sequence
identity to 1,905 microbial OTUs, which were classified and represented 24 bacterial and
one archaeal phyla.

Table 1.

Summary statistics table.

Reads Sequences bp Count Mean Seq. Mean No. of hits- No. of hits No. of hits -
Count Length GC % Greengenes -RDP Silva SSU
Pre-QC = 59,358 18,009,487 3034191 bp 504+4% 15,943 24,505 28,806

bp
Post-QC 50,213 13,969,056 278+199bp 50+4%

bp

Bacteria were further classified into 45 classes, 103 orders and 224 families (Fig. 2). The
most abundant phyla were Proteobacteria (36%), followed by Firmicutes (28%),
Actinobacteria (10%) and Bacteroidetes (6%) (Fig. 3). In the active ectomycorrhizosphere
zone, the most abundant superphylum Proteobacteria comprised of Gammaproteobacteria
(28%), Alphaproteobacteria (4.5%), Deltaproteobacteria (1.3%), Betaproteobacteria
(1.29%) and Epsilonproteobacteria (0.1%) (Fig. 3B), whereas Acidobacteria,
Planctomycetes, Tenericutes and Spirochaetes were significantly more frequent.

Cataloguing the bacterial diversity in the active ectomycorrhizal zone ...

Figure 2. EES

Krona chart of taxonomic affiliation of ectomycorrhizosphere and their relative abundance. The
inner circle represents the higher taxonomic rank, while the outer circle represents a lower
taxonomic rank up to the species level.

2A
ENRICHED BACTERIAL PHYLUM

Figure 3. EES

® Proteobacteria
= Finmicutes

@ unclassified (derived from Bacteria)

® Actinobacteria

® Bacteroidetes

® Acidobacteria

8 Cyanobacteria

@ Planctomycetes

= Tenericutes

™ Spirochaetes

® Gemunatimonadetes
@ Synergistetes

® Verrucomicrobia

®@ Nitrospirae

® Chloroflexi

® Deinococcus-Thermus
= Chlamydiae

™ Fusobacteria

§ Deferribacteres
=Chlorobi

@ Aquificae
®Dictyoglomi

® Thermotogae

@ Candidatus Poribacteria
@ Crenarchacota

2B

1.00

090 B® Alphaproteobacteria
WB Betaproteodactena

0.80 1 Detaproteobacteria

070 @ Epstionproteovactena
HH Gammaproteobacteria

0.60 unclassified (derived from Proteobacteria)

0.50

040

0.30

020

0.10

0.00

> -)
wo

2c
1.00
0.90 B Acidithiobaciiaies
B® Avromonadaies
0.80 Ateromonadaies
070 @ Cardiobactenales
Chromatiates
0.60 @ Enterodactensles
@ Legionetales
a @ Methylococcaies
0.40 © Oc0anospintiaies
B@ Pasteureliaies
09 Pseudomonadales
020 @ Thictrcnales
® Virionaes
0.10 @ Xanthomonadaies
sis I unclassified (derived trom Gammaproteobacteria)
A
wr

Taxonomic coverage of the ectomycorrhizosphere of Astraeus. A. Pie-chart showing the
distribution of enriched microbial phyla; B. Stacked bar showing the distribution of relative
abundant classes of Proteobacteria; C. Stacked bar showing of distribution of most relative

abundant families of Gammaproteobacteria.

6 Vishal V et al

Few members of Cyanobacteria and Archaea (Crenarchaeota) and pathogenic bacteria,
such as Escherichia, Salmonella, Vibrio, Helicobacter, Klebsiella and Shigella were also
identified in the study. A higher number of genera were identified in the active zone of
ectomycorrhizosphere (n = 652). The most abundant species from the
ectomycorrhizosphere was the Gram-negative rod-shaped Pseudomonas aeruginosa
(8.2%) of Gammaproteobacteria, followed by the Gram-positive rod-shaped Lactobacillus
delbrueckii (5%) of Firmicutes (Fig. 2). A number of significant reads fell under uncultured/
unclassified OTUs (Suppl. material 1).

Discussion

To our knowledge, this is the first high-resolution study of microbial diversity and their
distribution in the active zone of the ectomycorrhizosphere of wild edible mushrooms of
Astraeus from a dry deciduous forest of Shorea found in the red and sandy laterite soil with
pH ranges from 5.0 to 6.0. In this study, we explored the abundance of microorganisms
around the ectomycorrhizosphere and the hidden uncultured microbial communities. Such
studies serve as baseline information for future research on the dynamics and distribution
of microbial communities and how they relate to the physical environment and resilience.
Mogge et al. (2000) and Khetmalas et al. (2002) reported that bacteria are common
inhabitants in the mycorrhizosphere and they are more abundant in the mycorrhizosphere
as compared to the bulk soil.

The most abundant class was methanotrophs of Gammaproteobacteria of phylum
Proteobacteria (Fig. 3B and C). They play a vital role in phosphorus and iron mobilisation
and are believed to be involved in mineral weathering and in plant- nutrition control as
demonstrated by K6berl et al. (2017). Gammaproteobacteria contain members of the
bacterial family, which are both medically and ecologically important. Pseudomonadaceae,
Vibrionaceae, Halomonadaceae and Enterobacteriaceae were the most abundant families
of Gammaproteobacteria (Fig. 3C). Pseudomonas aeruginosa is Gram-negative
Gammaproteobacteria, rod-shaped, asporogenous, aerobic, opportunistic pathogen, which
degrades polycyclic aromatic hydrocarbons and participates in biofilm formation and
quorum sensing pathways (Botzenhart and Doring 1993). Firmicutes were very widely
spread and abundant in the ectomycorrhizosphere soil. Lactobacillus delbrueckii is a
Gram-positive, rod-shaped plant growth-promoting Firmicute that is active in the utilisation
of recalcitrant carbon and inorganic nutrients (Llado et al. (2017).

Ecological processes of forest communities, though, are associated with microbes, yet,
bacterial communities inhabiting the rhizosphere in forests have not been explored vis-a-
vis grassland or agricultural systems. Several phyla and classes in this study have been
found to dominate ectomycorrhizosphere bacterial communities. The comparative analysis
of the data reveals similar bacterial community structure as reported in previous
metagenomic assemblies from the ectomycorrhizosphere of oak forest (Uroz et al. 2012)
and boreal forest (Pent et al. 2017), except for the abundance of Pseudomonas. The soils
of ectomycorrhizosphere are rich in phosphate-solubilising bacteria, primarily of Bacillus,
Arthrobacterium, Agrobacterium, Micrococcus, Enterobacterium, Vibrio, Serbia, Rhizobium,

Cataloguing the bacterial diversity in the active ectomycorrhizal zone ... 7

Aeromonas, Burkholderia and Pseudomonas (Liu 2019). Burke et al. (2008) reported
ectomycorrhizosphere metagenome from Douglas fir EcM root tips, where EcM was
dominated by Alphaproteobacteria and Bacteroidetes. Kataoka et al. (2012) observed
Sphingomonas and Acidobacterium as abundant taxa in the pine mushroom Tricholoma
from a forest of Picea abies. Stursova et al. (2012) reported Betaproteobacteria,
Bacteroidetes and Acidobacteria as an abundant phyla. Similarly, Uroz et al. (2012) have
also reported an abundance of Acidobacteria, Actinobacteria and Bacteroidetes from an
oak forest, while Sphingomonas and Alphaproteobacteria from boreal forests were
recorded by Pent et al. (2017) as abundant. However, in our investigation, we observed the
highest abundance of Gammaproteobacteria, followed by Firmicutes and Actinobacteria.
Previous studies of the metagenome of ecomycorrhizosphere of different soil types such
as sandy, clay, loamy and podzol showed that soil types have a strong effect on the shape
and structure of the rhizospheric microbiome of various environments, which may explain
the taxonomic variations between them.

Conclusion

Thus, the soil metagenomic analyses of the ectomycorrhizosphere, associated with wild
mushrooms of Astraeus, revealed a distinct and unique assemblage of methanotrophic
Gammaproteobacteria. However, other prokaryotic affiliates with a high percentage of
unassigned taxa indicate scarce knowledge in the diversity of ectomycorrhizospheric
communities.

Acknowledgements

The authors acknowledge the Head of Department of Botany, DSPMU, Ranchi and Mr
Piyush Lugun, Mr Stephan Nag, Mrs Rajni Nag and Mrs Julia Horo, for their help during
sample collection.

Author contributions

SL, GS and VV conceptualised the ideas and devised the project. VV and SSM were
involved in research and investigation process specially, to sample collection and
performing experiments. Critical feedback was provided by all the authors in shaping the
research, analysis and manuscript. SL gave final approval of the version to be submitted
and any revised version.

Conflicts of interest

The authors declare no conflict of interest.

8 Vishal V et al

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Supplementary material

Suppl. material 1: RUGA-1 EE}

Authors: VV, SSM, GS and SL

Data type: Genomic

Brief description: Taxonomic profiling of ectomycorrhizosphere soil.
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