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Computational Biology and Chemistry xxx (xxxx) xxx-xxx

Contents lists available at ScienceDirect

Computational Biology and Chemistry

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journal homepage: http://ees
...
com

Research article

Re-Genome sequence and analysis of Burkholderia glumae strain AU6208 and evidence
of toxoflavin: A potential bacterial toxin
Annam Hussain a ,b ,1 , Maham Shahbaz b ,1 , Maria Tariq b , Muhammad Ibrahim b , Xianxian Hong a ,
Faryal Naeem b , Zunera Khalid b , Hafiz Muhammad Zeeshan Raza b , Zhu Bo c ,⁎⁎ , Li Bin a ,⁎
a
b
c

State Key Laboratory of Rice Biology and Key Lab of Molecular Biology of Crop Pathogens and Insects, Institute of Biotechnology, Zhejiang University, Hangzhou, China
Genomics and Computational Biology Laboratory, Department of Biosciences, COMSATS University Islamabad, Sahiwal Campus, Pakistan
Key Laboratory of Urban Agriculture by Ministry of Agriculture of China, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai, China

ABSTRACT

Keywords

Burkholderia glumae, the primary causative agent of bacterial panicle blight in rice, has been reported as an opportunistic pathogen in patients with chronic infections
...

glumae strain AU6208 and comparatively analyze its genome using B
...
Re-sequencing results revealed that the genome of strain AU6208 comprised 96 contigs corresponding
to a 6
...
2 % GC content; this is much
larger compared to the genome previously sequenced by us and described by Seo et al (2015), which was reported to be 4
...
31 % GC content
...
2 Mbp genome of BGR1, which encodes 6491 coding sequences and has 68
...
Further computational analysis revealed that the strain AU6208 encodes several bacteriocin biosynthesis genes, antibiotic, as well as virulent genes such as toxoflavin genes, which included
425 specialty genes and 12 toxoflavin genes
...
Upon comparison with BGR1, the structural characterizations of selected toxoflavin genes (ToxB,
ToxC, ToxG, H, and TofI) revealed variations in 2D and 3D structures such as differences in α-helix, β-sheets,
loops, physiological properties of proteins, RMSD values, etc
...
In addition to understanding the epidemiology of
strain AU6208, this updated genomics data will also unfold the pathogenicity of bacteria in diversity of various
hosts and anti-virulence
...
Introduction

Burkholderia glumae (earlier known as Pseudomonas glumae) are
Gram-negative, aerobic, and capsulated (a polysaccharide layer lying
outside cell envelop) bacteria, and belongs to the β-subclass of the proteobacteria (Karki et al
...
They are slow-growing non-sporulating bacteria and forms circular grayish-white colonies
...

They are dependent on the stages of rice growth and causes grain rot,
sheath rot, and seedling rot
...
glumae has been reported as a

pathogen of rice crop in other rice-growing countries
...

Involvement of multiple virulent factors in B
...
Many molecular genetics research
groups have identified significant factors that make B
...
Phytotoxins and lipases are identified as the
significant virulent factors (Degrassi et al
...
KatG catalase, the
Hrp type-III secretion system (Hrp-T3SS), and PehA and PehB poly

Corresponding author at: State Key laboratory of Rice Biology and Key Lab of Molecular Biology of Crop Pathogens and Insects, Institute of Biotechnology, Zhejiang University, Hangzhou,
China
...

E-mail addresses: bzhu1981@sjtu
...
cn (Z
...
edu
...
Bin)
1 Contributed equally
...
org/10
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compbiolchem
...
107245
Received 2 December 2019; Received in revised form 1 March 2020; Accepted 3 March 2020
Available online xxx
1476-9271/© 2020
...
Hussain et al
...
66 scores
...
Clusters of Orthologous Groups (COGs) of proteins
and their functional predictions were determined using eggNOG 4
...
Bacterial genomes encode some interesting
genes, such as virulence factors, antibiotic resistance genes, drug targets, and human homologs, which play key roles in infectious disease
...


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galacturonase (Degrassi et al
...
, 2009) are some of
the additional factors responsible for the virulence of B
...
, 2008)
...
glumae,
toxoflavin, a bright yellow pigment, is the most significant phytotoxin
...
The optimum temperature for toxoflavin production is
37 °C, while no production was detected at 25 °C–28 °C (Kim et al
...
Toxoflavin and fervenulin are essential for the
pathogenicity of rice seedling and grain rot, which result in the reduced
growth of leaves and roots in rice seedlings, and lead to chlorotic symptoms on rice panicles (Jeong et al
...

Virulent factors of human and plant pathogens are continuously
evolving in order to successfully infect their respective hosts
...
, 2011)
...
, 2011)
...

This study has examined the demonstration and differentiation in
pathogenicity of B
...
glumae strain
AU6208 by keeping toxoflavin as a key pathogenic factor at genome
level
...
Transcriptomics approaches by
high-throughput sequencing could offer better evidences to elucidate the
genetic lineages and mechanism of invasion of these pathogens in plant
and alternative human model
...
3
...
InterPro was used to determine the domains, families, and associated functions in toxoflavin proteins of AU6208 in comparison to those
of the BGR1 strain
...
, 2017) and NCBI CDD database (Yar et al
...
The grand average of hydropathicity (GRAVY) value for a protein
or a peptide that indicates the protein hydrophobicity is calculated by
adding the hydropathy values of each amino acid residues and dividing
the sum by the length of protein sequence
...
The GRAVY values for the virulent
proteins were measured by Protparam Expasy tool (Nazir et al
...

3
...

The amino acid sequences of toxoflavin proteins of strain BGR1 were retrieved in FASTA format from UniProt Knowledgebase (UniProtKB) and
aligned by BLASTp to explore the sequence similarity in strain AU6208
...
glumae BGR1 and
AU6208 were searched in the Protein Data Bank (Bernstein et al
...
Comparative structure prediction was done through manual as
well as automated model building
...
14 (Fiser and Sali, 2003)
...
, 2015) and Phyre2 (Kelley et al
...
These predicted structures were
then evaluated using different Bioinformatics evaluation tools
...
Verify-3D (Eisenberg et al
...
The sequence and structure of B
...
glumae AU6208
toxoflavin proteins
...
, 2012), while secondary structure elements were compared
using UCSF Chimera 1
...
1(Pettersen et al
...

The 3D structure of toxoflavins ToxA, ToxD, ToxE, ToxG, TofI, and
TofR were excluded as they have 100 % protein structure similarity or
PDB template similarity
...
glumae BGR1 and
AU6208) were predicted, ToxF and ToxG proteins were exceptional having no template, therefore, Ab initio structure prediction was carried
out by Phyre2 and I-TASSER
...
14,
I-TASSER, and Phyre2
...


2
...
1
...
glumae strain AU6208 was inoculated into 2 mL
of Luria-Bertani (LB) medium, and incubated for 24 h at 37 °C, 170 rpm
...
5 ml of this culture was taken to isolate the genomic DNA by
using DNA purification kit (Promega, Madison, WI) as per the manufacturer’s instructions
...
The sequence of the genome reads were de
novo assembled by latest version of Geneious Pro (v11
...
Strain
AU6208 was annotated using the most closely related strain B
...
B
...
, 2008; Gillespie et al
...

2
...
Genome-wide gene prediction and analysis

Further computational analyses for the identification of bacteriocin
biosynthesis, antibiotic as well as virulent genes such as specialty genes
were conducted using RAST and PATRIC online tools
...
The retrieved protein sequences were used as query sequences in a local BLAST search (BLASTN, BLASTX, pBLAST) in the
RAST server (Aziz et al
...

glumae AU6208
...
Hussain et al
...
1
...
glumae BGR1 which contains 68
...
The strain AU6208 belongs to a human patient (Kumar et al
...
Similarly,
the difference in GC content refers to the difference in the number of
protein-coding sequences, as the majority of the prokaryotic genome encodes for protein-coding sequences (Devescovi et al
...
Moreover, the re-sequence of strain AU6208 has also updated the genome
dataset including size of the genome from 4
...
1 Mbp, number of contigs from >1200 to 96, and CDS from 4361 to 5322 as described by Seo et al
...
, 2015)
...
glumae AU6208
re-sequenced genome shared >80 % genome identity as shown in Figs
...
Circular map of strain AU6208 was constructed with the
CGView Comparison Tool
...
The outermost circle in pink shows matching nucleotide base pairs representing the BLAST analysis and gaps in
the genome alignment are indicated in white
...
In the 3rd inner
circle, the region in green represents the G + C content of the forward
strand, and the region in purple represents the G + C content of the
reverse strand
...

In prokaryotes, the composition of genomic DNA base (GC content)
is envisaged to notably influence the genome species ecology and functioning
...
The high
GC content of B
...
The close association of B
...


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Nucleotide sequences encoding the toxoflavin proteins of B
...
Phylogenetic tree
was constructed using the Maximum Likelihood method provided in
the list of Phylogeny functions of MEGA7 software (Nei and Kumar,
2000)
...
Branches corresponding to partitions reproduced in less than 50
% bootstrap replicates are collapsed
...
The analysis involved 24 protein sequences
...
Results and discussion
4
...
Comparative genome analysis

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Advancement in next generation sequencing technology has enabled
us to explore in-depth information on pathogenic bacteria resourced
from plant and human niches via whole-genome sequencing (WGS) and
to study genetic differences between B
...
The genome sequence of B
...
By using the RAST annotation
server, number of RNAs, GC content, the number of contigs, number of
coding regions, and the number of missing genes were procured
...
glumae AU6208 possesses 68
...
glumae AU6208 and LMG2196
...
of coding sequence
No
...
glumae AU6208

B
...
7
5322
5383

7284683
64
67
...
2
...
Distribution
of genes within COG categories is provided in Fig
...
1
...

3

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Computational Biology and Chemistry xxx (xxxx) xxx-xxx

in the sequence similarity may lead to the structure variation and the
differences in the function
...
ToxC, D, and H are essential for the biosynthesis of
toxoflavin, but their functions are yet not clear (Philmus et al
...

The variations in sequence similarity show that this protein might have
a similar role in the adaption of their respective environment but could
be inferred by structural analysis and experimentations
...
coli and
deaminase/reductase proteins such as RibD protein from E
...
, 2016)
...
glumae BGR1 and
AU6208, as it has been reported that ToxE and ToxB catalyze the first
step of riboflavin biosynthesis, which is the initial step of toxoflavin
biosynthesis, and is predicted to be analogous with GTP being the initial
substrate by previous studies (Suzuki et al
...

Previously, it is reported that B
...
Advancement in next generation and availability of bulk genomic data, following accessibility of advanced computational tools has enhanced our understanding of the taxonomic and evolutionary relationships between industrially, environmentally, clinically,
and agriculturally important bacteria such as B
...
Evolutionary association of all toxoflavin genes retrieved from strain AU6208
with those of strain BGR1 made two clusters: 1st consisting ToxB, I, G D,
F, and H and 2nd consisting ToxE, C, A, J, F, TofR, and TofI genes (Fig
...


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as reference
...
glumae strain AU6208 and
BGR1 shows differences in protein distribution (Fig
...
Various key differences in the number of genes were noted such as virulence, disease,
and defense genes in B
...
1)
...
glumae strain AU6208, its
pathogenicity, and drug resistance as well as population genetic characteristics
...
glumae strain AU6208 has gone either under rapid genome
rearrangement or deletion according to niche or has evolved rapidly
...

4
...
Gene prediction and In-silico characterizations

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The genome of B
...
B
...
Interestingly, all the specialty genes encoded in strain BGR1 were also present in strain AU6208 except with some sequence variation
...
Such as full virulence of B
...
4], all these genes were present in strain AU6208
...
glumae strain BGR1 were used as a
bait to identify the toxoflavin proteins in the genome sequence of B
...
BLASTn and BLASTp searches were
conducted using all 12 genes ToxA, B, C, D, E, ToxF, G, H, I, J, TofI, and
TofR in RAST server and PATRIC Blast tool (Wattam et al
...
All
12 toxoflavin genes were present in strain AU6208
...
glumae strain AU6208
...
, 2013)
...

ToxA, ToxF, and TofI were the proteins having 100 % similarity
with that of reference strain BGR1 (Table 2)
...
, 2016), leading to the virulence
...
, 2012), under the control of which
toxoflavin works
...
Moreover, the 100 % similarity
also endorses these reports indicating that many virulence determinants
encoded in plant-pathogen have the capability to attack other hosts,
which are beyond the plant kingdom such as humans, animals, and insects (Kirzinger, 2012)
...
This variation

4
...
Functional characterization based on protein domains and families
The results showed that all toxoflavin proteins retrieved from BGR1
or AU6208 encodes same conserved domain
...
The proteomes built in contemporary organisms
due to the collection of proteins owned through duplication and recombination of a limited set of domains
...

Variation in protein domain may lead to variations in the protein architectures, information, and functions (Han et al
...
The conservation of domains in all toxoflavins shows that these proteins may be vital,
have similar function, and are key proteins, but variations in sequence
is another aspect that leads to variation in structure and function
...
All the proteins have hydrophilic nature and there was no
difference in GRAVY of each protein resourced from either niches i
...
,
ToxA of BGR1 and ToxA of AU6208 both has hydrophilic nature (Table
3)
...
,
2002)
...
5
...
glumae BGR1 and B
...
The details
of evaluation scores for top selected models of toxoflavin proteins resourced from both strains are listed in Table 4
...
Structural analysis shows that ToxB strain BGR1
has α-β fold with a central core of mainly antiparallel β-sheet at C-ter

4

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Computational Biology and Chemistry xxx (xxxx) xxx-xxx

Table 2
Template searching for toxoflavin proteins of B
...
glumae AU6208
...
A

RND efflux
membrane

N
...
3)
...

ToxB AU6208 possesses α-β fold with a central core of mainly antiparallel β-sheets interconnected by loops and helices
...
Residues 187–218 at the end of C-terminus are positioned away from the backbone of the protein containing one β-sheet
β-8 and one α-helix α-7 connected by a loop from residues 190–197
(Fig
...
A number of structural variations noted between the ToxB
BGR1 and AU6208 depicted that there could be functional differences

PDB
Template

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UniProt ID

PDB
(Identity)

100 %

100 %

79 %

82

99 %

100 %

TRP-2

Riboflavin
biosynthesis

AHL receptor

N
...
A

Structure
Prediction
Approach
Structure
Prediction
not
required
Homology
Modeling
Homology
Modeling
Structure
Prediction
not
required
Structure
Prediction
not
required
Ab Initio

Ab Initio

Homology
Modeling
Homology
Modeling

Homology
Modeling
Homology
Modeling

among them based on their structural differences (Koch et al
...
, 2005)
...

The ToxC protein encoded in strain BGR1 consists of two β-propellers
i
...
, seven-bladed β-propeller at N-terminus and five-bladed β-propeller
(1–289 residues) at C-terminus with no α-helices
...
Compared to ToxC of BGR1, ToxC of AU6208 encodes the
structural difference which contains β-propeller structure with eight
blades, three α-helices α-1 (4–6 residues), α-2 (19–25

5

Computational Biology and Chemistry xxx (xxxx) xxx-xxx

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A
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Fig
...
Phylogenetic analysis of toxoflavin genes of B
...
glumae strain BGR1
...
The β-propeller folds
in proteins are naturally ubiquitous and extensively employed as structural scaffolds for enzymatic activity as well as ligand binding activities
(Andreeva and Murzin, 2006)
...

Structure analysis of protein ToxG of BGR1 represent that it contains
six α helices, eight β sheets: β-1 (44–47 residues), β-2 (56–64 residues),
β-3 (68–71 residues), β-4 (79–82 residues), β-5 (88–90 residues), β-6
(95–99 residues) between α-1 (3–22 residues), α-2 (102–132 residues),
and α-3 (136–163 residues) with α-3 connected to β-7 (64–66 residues)
without any loop
...
The rest of the structure consists of nine β sheets
(β-11 to β-19) from residues 234–341 with β-11 connected to α-5
(285–287 residues)
...

Compared to this, ToxG of AU6208 protein encodes a loop structure
formed from residues 3–22 in place of α-1 in ToxB BGR1
...
However, this may also lead to the functional difference between both the proteins
...
Moreover, there are little structural
variations between both proteins, which may lead to change in their
function
...
The protein function is dependent directly on its 3-D
structure (Mittag et al
...


It can be concluded that if there is a difference in proteins at the
sequence level then there will be variations at structure level too
...
This structural variation does not always need to be
vary drastically because slight changes in structure, like the changes in
loops and secondary structure orientation, can change the protein folding and shape, thus making the protein non-functional (Schaefer and
Rost, 2012)
...
glumae AU6208, a human-associated strain, is a virulent determinant, but the mechanism of
pathogenicity seems to be different than that of B
...

5
...
glumae AU6208 has a genome size of 6
...
The presence and variations in
the sequence and structural component e
...
, binding sites, α-helix, and
β-sheets in 12 toxoflavin proteins encoded in strain BGR1 and AU6208
leads to the conclusions that toxoflavin proteins may be key components playing role in virulence in both niche but with different mode
of action
...
Furthermore, advancement in molecular biology, as
well as in-depth sequence analysis such as RNA, may help us to further
explore by inoculating plant pathogen into animal model as well as a
human pathogen into plant model
...
Hussain et al
...
glumae
AU6208
...
269
−0
...
200

Methyltransferase

2

BGR1
AU6208
BGR1

ToxC

−0
...
218

GTP
cyclohydrolase
II

3

AU6208
BGR1

GTP
cyclohydrolase II,
ribA

DsbC & WD40

4

ToxD

AU6208
BGR1

−0
...
191

Thiol:disulphide
interchange
protein

5

ToxE

AU6208
BGR1

−0
...
140

6

ToxF

7

ToxG

AU6208
BGR1
AU6208
BGR1

−0
...
793
0
...
076

ToxH

AU6208
BGR1

−0
...
443

ToxI

AU6208
BGR1

0
...
189

ToxJ

AU6208
BGR1

−0
...
11

TofR

AU6208
BGR1

0
...
225

TofI

AU6208
BGR1

−0
...
103

AU6208

−0
...
Zhu Bo,
Li Bin, Designing the Experimentation, Guiding the group in writing at
various steps of experimentation and analysis
...


WD40
FGE-sulfatase

MafB19-deam
super family

MafB19-deam
super family

Exporter YdcZ

DMT_YdcZ

RND efflux
pump, membrane
fusion protein

ACR_tran super
family

Declaration of Competing Interest
No conflict of interest declared
...
NZ_AMQT00000000
...
2 for Burkholderia glumae strain AU6208
...
No
...

Crop Disease Control
China

NAT_SF super
family

Appendix A
...
org/10
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compbiolchem
...

107245
...

Protein Name

Model

Residues in favored region

Residues in allowed region

Residues in outlier region

ERRAT

Verify 3D

ToxB (BGR1)
ToxB (AU6208)
ToxC (BGR1)
ToxC (AU6208)
ToxG (BGR1)
ToxG (AU6208)
ToxH (BGR1)
ToxH (AU6208)
ToxI (BGR1)
ToxI (AU6208)

I-TASSER4
I-TASSER3
I-TASSER2
I-TASSER4
I-TASSER3
I-TASSER4
I-TASSER1
I-TASSER2
I-TASSER3
I-TASSER3

171 (68
...
0 %)
410 (73
...
1%)
304 (80
...
1 %)
921 (89
...
2 %)
438 (86
...
3 %)

50 (20
...
6 %)
86 (15
...
7%)
53 (14
...
1 %)
83 (8
...
4 %)
40 (7
...
0 %)

28 (11
...
5 %)
65 (11
...
2%)
20 (5
...
8 %)
24 (2
...
4 %)
26 (5
...
8 %)

91
...
552
79
...
0881
81
...
1933
95
...
274
94
...
057

71
...
24%
90
...
92%
75
...
59%
83
...
33%
65
...
35%

7

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Computational Biology and Chemistry xxx (xxxx) xxx-xxx

Protein name

RMSD value

Alpha-helices

Beta-sheets

Loops

ToxB (BGR1)
ToxB (AU6208)
ToxC (BGR1)
ToxC (AU6208)
ToxF (BGR1)
ToxF (AU6208)
ToxG (BGR1)
ToxG (AU6208)
ToxH (BGR1)
ToxH (AU6208)
ToxI (BGR1)
ToxI (AU6208)

0
...
998Å
0
...
758Å
0
...
867Å

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Table 5
Secondary Structure elements of toxoflavin proteins in B
...


Fig
...
Three-dimensional protein structures for toxoflavin proteins
...
Hussain et al
...
Mol
...
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...
Rapid and specific detection of Burkholderia glumae in rice seed by real-time
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...
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...
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...

Kirzinger, M W B, Nadarasah, G, Stavrinides, J, 2011
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...

Koch, O, Bocola, M, Klebe, G, 2005
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Kopec, K O, Lupas, A N, 2013
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...
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...
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Raff, M, Alberts, B, Lewis, J, Johnson, A, Roberts, K, 2002
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4th edition
...
Stereochemistry of polypeptide chain configurations
...
Mol
...
7, 95–99
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Seo, Y-S, Lim, J Y, Park, J, Kim, S, Lee, H-H, Cheong, H, Kim, S-M, Moon, J S, Hwang, I,
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Curr
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The RAST Server: rapid annotations using subsystems
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...

Bernstein, F C, Koetzle, T F, Williams, G J B, Meyer, E F, Jr
...
The Protein Data Bank: a computer-based
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...
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...
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...
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...
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...
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...
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Devescovi, G, Bigirimana, J, Degrassi, G, Cabrio, L, LiPuma, J J, Kim, J, Hwang, I, Venturi, V, 2007
...
Appl
...
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