Open Access

Genomic information of the arsenic-resistant bacterium Lysobacter arseniciresistens type strain ZS79T and comparison of Lysobacter draft genomes

Standards in Genomic Sciences201510:88

https://doi.org/10.1186/s40793-015-0070-5

Received: 29 October 2014

Accepted: 8 October 2015

Published: 27 October 2015

Abstract

Lysobacter arseniciresistens ZS79T is a highly arsenic-resistant,rod-shaped, motile, non-spore-forming, aerobic, Gram-negative bacterium. In this study, four Lysobacter type strains were sequenced and the genomic information of L. arseniciresistens ZS79T and the comparative genomics results of the Lysobacter strains were described. The draft genome sequence of the strain ZS79T consists of 3,086,721 bp and is distributed in 109 contigs. It has a G+C content of 69.5 % and contains 2,363 protein-coding genes including eight arsenic resistant genes.

Keywords

Lysobacter Lysobacter arseniciresistens Comparative genomicsGenome sequence Xanthomonadaceae

Introduction

Lysobacter arseniciresistens type strain ZS79T (=CGMCC 1.10752T = KCTC 23365 T) belongs to family Xanthomonadaceae [1]. It is an arsenic-resistant bacterium isolated from subsurface soil of Tieshan iron mine, Daye City, P. R. China [1]. So far, there are 32 validly published species of Lysobacter [2]. Most of these Lysobacter strains were isolated from soil except that Lysobacter brunescens [3] and Lysobacter oligotrophicus [4] were isolated from water, and Lysobacter concretionis [5], Lysobacter daecheongensis [6] Lysobacter spongiicola [7] were isolated from sludge, sediment and deep-sea sponge, respectively.

So far, the genomic sequences of two Lysobacter strains have been published ( Lysobacter capsici AZ78 [8, 9] and Lysobacter antibioticus 13-6 [10]), but the annotation of L. antibioticus 13-6 was not completed. In order to provide genome information of genus Lysobacter , we performed whole genome sequencing of four strains of Lysobacter ( L. arseniciresistens ZS79T, Lysobacter conceretionis Ko07T [5], Lysobacter daejeonensis GH1-9T [11], and Lysobacter defluvii IMMIB APB-9T [12]). In this study, the genome features of L. arseniciresistens ZS79T is provided and the comparative results of five genomes of Lysobacter are presented.

Organism information

Classification and features

Members of genus Lysobacter are rod-shaped, aerobic, Gram-negative bacteria [3]. Their G+C contents are 65.4–70.1 %. They use NO3 , NH4 +, glutamate, asparaginate as sole nitrogen sources, Q-8 as the major respiratory quinone, and diphosphatidylglycerol, phosphatidylethanolamine, phosphatidylglycerol, phosphatidyl-N-methylethanolamine as the major polar lipids [3, 8]. In addition, they could lyse cells of many creatures including bacteria, filamentous fungi, yeasts, algae and nematodes [3].

Phylogenetic analyses of L. arseniciresistens ZS79T and its related strains of family Xanthomonadaceae were performed based on 16S rRNA genes (Fig. 1a) and 831 conserved proteins (Fig. 1b). In both trees, strain ZS79T is clustered with the other four strains of genus Lysobacter . The phylogenies of the two trees are similar but genomic based tree is more stable than the 16S rRNA gene one (Fig. 1b vs 1a).
Fig. 1

Phylogenetic analyses indicating the position of L. arseniciresistens (in bold) in family Xanthomonadaceae. a The NJ tree based on aligned sequences of 16S rRNA of ten strains of family Xanthomonadaceae. b The NJ tree based on 831 conserved proteins among the ten Xanthomonadaceae strains. Phylogenetic analyses were performed using MEGA version 6 [33]. The trees were built using p-distance model and a bootstrap analysis of 1000 replicates. The GenBank numbers are listed after each strain

L. arseniciresistens ZS79T is aerobic, motile, and Gram-negative bacterium with a Minimum Inhibitory Concentration of 14 mM arsenite in R2A medium (Table 1). The cells are rod-shaped with one flagellum and non-spore-forming (Fig. 2). Colonies of this strain are yellow, nontransparent, convex, circular, and, smooth [1].
Table 1

Classification and general features of L. arseniciresistens ZS79T according to the MIGS recommendations [27]

MIGS ID

Property

Term

Evidence codea

 

Classification

Domain Bacteria

TAS [28]

Phylum Proteobacteria

TAS [29]

Class Gammaproteobacteria

TAS [29, 30]

Order Xanthomonadales

TAS [30, 31]

Family Xanthomonadaceae

TAS [30, 31]

Genus Lysobacter

TAS [3]

Species Lysobacter arseniciresistens

TAS [1]

Type strain: ZS79T (=CGMCC 1.10752T = KCTC 23365T).

Gram stain

negative

TAS [1]

Cell shape

rod-shaped

TAS [1]

Motility

motile

TAS [1]

Sporulation

non-spore-forming

TAS [1]

Temperature range

4–37 °C

TAS [1]

Optimum temperature

28 °C

TAS [1]

pH range; Optimum

5.0–9.0; 7.0

TAS [1]

Carbon source

tyrosine, hippurate, gelatin, 3-hydroxybutyric acid

TAS [1]

MIGS-6

Habitat subsurface soil

TAS [1]

MIGS-6.3

Salinity

0–4 % NaCl (w/v)

TAS [1]

MIGS-22

Oxygen requirement

aerobic

TAS [1]

MIGS-15

Biotic relationship

free-living

NAS

MIGS-14

Pathogenicity

non-pathogen

NAS

MIGS-4

Geographic location

Daye City, Hubei province, China

TAS [1]

MIGS-5

Sample collection

2011

TAS [1]

MIGS-4.1

Latitude

30.207178 N

TAS [1]

MIGS-4.2

Longitude

114.901092 E

TAS [1]

MIGS-4.4

Altitude

not reported

 

a: Evidence codes – TAS: Traceable Author Statement (i.e., a direct report exists in the literature); NAS: Non-traceable Author Statement (i.e., not directly observed for the living, isolated sample, but based on a generally accepted property for the species, or anecdotal evidence). These evidence codes are from the Gene Ontology project [32]

Fig. 2

Transmission electron microscopy of L. arseniciresistens ZS79T

The major ubiquinone is Q-8, the major cellular fatty acids (>10 %) are iso-C15 : 0, iso-C17 :1 ω9ϲ, iso-C16 :0, iso-C11 :0 and iso-C11 :0 3-OH. The polar lipids are diphosphatidylglycerol, phosphatidylethanolamine, phosphatidylglycerol and a kind of unknown phospholipid The C + G content is was 70.7 mol% (HPLC) [1].

Genome sequencing and annotation

Genome project history

The genome of L. arseniciresistens ZS79T was sequenced in April, 2013 and finished within two months. The high-quality draft genome sequence is available in GenBank database under accession number AVPT00000000. The genome sequencing project information is summarized in Table 2.
Table 2

Project information

MIGS ID

Property

Term

MIGS 31

Finishing quality

High-quality draft

MIGS-28

Libraries used

Illumina Paired-End library (300 bp insert size)

MIGS 29

Sequencing platforms

Illumina Hiseq2000

MIGS 31.2

Fold coverage

272.6×

MIGS 30

Assemblers

SOAPdenovo v1.05

MIGS 32

Gene calling method

GeneMarkS+

 

Locus Tag

N799

 

GenBank ID

AVPT00000000

 

GenBank Date of Release

2014/10/24

 

GOLD ID

Gi0055236

 

BIOPROJECT

PRJNA214588

MIGS 31

Source Material Identifier

ZS79T

 

Project relevance

Genome comparison

Growth conditions and genomic DNA preparation

L. arseniciresistens ZS79T was cultured in 50 ml of LB (Luria–Bertani) medium at 28 °C for 3 days with 160 160 r/min shaking. About 10 mg cells were harvested by centrifugation and suspended in normal saline, and then lysed using lysozyme. DNA was isolated using cells were harvested by centrifugation and suspended in normal saline, and then lysed using lysozyme. The DNA was extracted and purified using the QiAamp kit according to the manufacturer’s instruction (Qiagen, Germany).

Genome sequencing and assembly

The whole genome sequencing of L. arseniciresistens ZS79T was performed on Illumina Hiseq2000 with Paired-End library strategy (300 bp insert size) at Majorbio Biomedical Science and Technology Co. Ltd. DNA libraries with insert sizes from 300 to 500 bp was constructed using the established protocol [13]. The obtained high quality data contains 4,528,542 × 2 pared reads and 194,996 single reads with an average read length of 91 bp. The sequencing depth was 272.6×. Using SOAPdenovo v1.05 [14] the reads were assembled into 109 contigs with a cumulative genome size of 3,086,721 bp.

Genome annotation

The draft sequence of L. arseniciresistens ZS79T was annotated using the National Center for Biotechnology Information Prokaryotic Genomes Annotation Pipeline [15]. The functions of the predicted genes were determined through blast alignment against the NCBI protein database. Genes were identified using the gene caller GeneMarkS+ with the similarity-based gene detection approach [16]. The different features were predicted by WebMGA [17], TMHMM [18] and SignalP [19].

Genome properties

The whole genome sequence of L. arseniciresistens ZS79T is 3,086,721 bp long with a G+C content of 69.6 % and is distributed into 109 contigs. It has 2,422 predicted genes including 2,363 (97.6 %) protein coding genes, 50 (2.1 %) RNA genes, and 9 (0.4 %) pseudo genes. A total of 1633 (67.4 %) genes have functional prediction, and 1,858 (76.7 %) genes could be assigned to Clusters of Orthologous Groups [20]. More detailed information of the genome statistics is showed in Table 3. The protein functional classification according to COGs is showed in Table 4. The genome map is showed in Fig. 3.
Table 3

Genome statistics

Attribute

Value

% of Total

Genome size (bp)

3,086,721

100.00

DNA coding (bp)

2,284,152

74.00

DNA G+C (bp)

2,147,191

69.56

DNA scaffolds

109

 

Total genes

2,422

100.00

Protein coding genes

2,363

97.56

RNA genes

50

2.06

Pseudo genes

9

0.37

Genes in internal clusters

811

34.32

Genes with function prediction

1633

67.42

Genes assigned to COGs

1858

76.71

Genes with Pfam domains

2038

84.14

Genes with signal peptides

539

22.81

Genes with transmembrane helices

527

22.25

CRISPR repeats

1

0.41

Table 4

Number of genes associated with general COG functional categories

Code

Value

%age

Description

J

157

6.48

Translation, ribosomal structure and biogenesis

A

1

0.04

RNA processing and modification

K

116

4.79

Transcription

L

127

5.24

Replication, recombination and repair

B

2

0.08

Chromatin structure and dynamics

D

27

1.11

Cell cycle control, Cell division, chromosome partitioning

V

37

1.53

Defense mechanisms

T

104

4.29

Signal transduction mechanisms

M

125

5.16

Cell wall/membrane biogenesis

N

73

3.01

Cell motility

U

89

3.67

Intracellular trafficking and secretion

O

108

4.46

Posttranslational modification, protein turnover, chaperones

C

128

5.28

Energy production and conversion

G

70

2.89

Carbohydrate transport and metabolism

E

148

6.11

Amino acid transport and metabolism

F

50

2.06

Nucleotide transport and metabolism

H

91

3.76

Coenzyme transport and metabolism

I

90

3.72

Lipid transport and metabolism

P

107

4.42

Inorganic ion transport and metabolism

Q

53

2.19

Secondary metabolites biosynthesis, transport and catabolism

R

233

9.62

General function prediction only

S

185

7.64

Function unknown

-

564

23.29

Not in COGs

The total is based on the total number of protein coding genes in the genome

Fig. 3

Graphical circular map of L. arseniciresistens ZS79T genome. From outer to inner, ring 1 shows the genomic islands (red bars) that were predicted by IslandViewer [34]; ring 3,4 show the predicted genes on forward/reverse strand; ring 2,5 show the genes assigned to COGs; ring 6-9 show the ORFs similarity between the genome of L. arseniciresistens ZS79T and the genomes of L. conceretionis Ko07T, L. daejeonensis GH1-9T, L. capsici AZ78 and L. defluvii IMMIB APB-9T; ring 10 shows the G+C% content plot

Insights from the genome sequences

To obtain features of Lysobacter genomes, we sequenced four genomes of genus Lysobacter and performed comparative genomic analysis among the five available genomes of this genus. The general features of these five genomes are summarized in Table 5. To calculate the pan-genome and core-genome of these five genomes, we performed orthologs clustering analysis using OrthoMCL [21]. The pan-genome has 6,409 orthologs families and the core-genome has 1,207 orthologs. The numbers of unique genes of each genome are showed in Fig. 4. To evaluate the genome variation of these five genomes, we first performed multiple alignments among these genome sequences using MAUVE [22] and then calculated the nucleotide diversity using DnaSP v5 [23]. These five genomes shared 0.73 Mb co-linear sequences. The π value of these sequences among these five genomes is 0.173 which means that the approximate nucleotide sequence homology is 83 % among genomes of Lysobacter [23].
Table 5

General features of the five Lysobacter genomesa

Strains

Source

Size (Mb)

G+C content

CDSs

rRNA clusters

tRNAs

Genome status

GenBank No.

Draft/finished

Contigs

Contigs N50 (bp)

L. arseniciresistens ZS79T

Iron-mined soil

3.1

69.58 %

2,363

3

46

Draft

109

101,761

AVPT00000000

L. conceretionis Ko07T

Anaerobic granules

3.0

67.25 %

2,232

3

46

Draft

26

386,139

AVPS00000000

L. daejeonensis GH1-9T

Green house soils

3.3

67.29 %

2,570

4

48

Draft

99

101,460

AVPU00000000

L. defluvii IMMIB APB-9T

Municipal solid waste

2.7

70.22 %

2,443

13

44

Draft

578

16,113

AVBH00000000

L. capsici AZ78

Tobacco & tomato rhizosphere

6.3

66.43 %

5,139

8

65

Draft

174

101,988

JAJA00000000

aThe genome of L. arseniciresistens ZS79T, L. conceretionis Ko07T, L. daejeonensis GH1-9T and L. defluvii IMMIB APB-9T are sequenced in this study. The genome of L. capsici AZ78 was sequenced by Puoplo et al. [9]

Fig. 4

The core-genome and the unique genes of the five Lysobacter genomes. The Venn diagram shows the number of orthologous gene families of the core-genome (in the center) and the numbers of unique genes of each genome

In the genome of L. arseniciresistens ZS79T, we found that the genomic island distributions are consistent with the genome C + G content anomaly areas (Fig. 3). In addition, few gene sequences from the other four Lysobacter genomes could be aligned with these genomic island regions (Fig. 3, ring 6 to ring 9). These results indicated that the genes within the genomic islands were most probably acquired by horizontal transfer [24] and these regions are unique in the genome of L. arseniciresistens ZS79T.

According to Kyoto Encyclopedia of Genes and Genomes [25] annotation result, all of the five Lysobacter genomes have a nearly complete type II secretion system which could secret cell wall degrading enzymes [26]. This result may correspond to the behavior of Lysobacter members that were able to lyse cells of many microorganisms [3]. In addition, the genomes of L. arseniciresistens ZS79T, L. concretionis Ko07T and L. defluvii IMMIB APB-9T contain genes for flagellar assembly, whereas the genome of L. daejeonensis GH1-9T does not contain any genes for flagellar assembly and L. capsici AZ78 does not contain genes for flagellar filament (Additional file 1: Table S2). These genotypes correspond to the phenotype descriptions that L. daejeonensis and L. capsici are non-motile [8, 11].

Genomic analysis showed eight genes corresponding to arsenic resistance in the genomes of L. arseniciresistens ZS79T (Additional file 1: Table S3). This result well explained the arsenite resistance of this strain [1]. By contrast, fewer arsenic resistance were found in the genomes of L. concretionis Ko07T, L. defluvii IMMIB APB-9T, L. capsici AZ78, and L. daejeonensis GH1-9T compared to strain ZS79T.

Conclusions

The genomic information of L. arseniciresistens ZS79T and the comparative genomics analysis of the five Lysobacter strains are obtained. The genomic based phylogeny is in agreement with the 16S rRNA gene based one indicating the usefulness of genomic information for bacterial taxonomic classification. Analysis of the genomes show certain correlation between the genotypes and the phenotypes.

Declarations

Acknowledgements

This work was supported by the National High Technology Research and Development Program of China (2012AA101402) and the National Natural Science Foundation of China (31470226).

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

(1)
State Key Laboratory of Agricultural Microbiology, College of Life Sciences and Technology, Huazhong Agricultural University

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Copyright

© Liu et al. 2015