Open Access

High quality draft genomic sequence of Arenimonas donghaensis DSM 18148T

Standards in Genomic Sciences201510:59

DOI: 10.1186/s40793-015-0055-4

Received: 22 September 2014

Accepted: 5 August 2015

Published: 26 August 2015

Abstract

Arenimonas donghaensis is the type species of genus Arenimonas which belongs to family Xanthomonadaceae within Gammaproteobacteria. In this study, a total of five type strains of Arenimonas were sequenced. The draft genomic information of A. donghaensis DSM 18148T is described and compared with other four genomes of Arenimonas. The genome size of A. donghaensis DSM 18148T is 2,977,056 bp distributed in 51 contigs, containing 2685 protein-coding genes and 49 RNA genes.

Keywords

Arenimonas Arenimonas donghaensis Comparative genomics Genome sequence Xanthomonadaceae

Introduction

Arenimonas donghaensis DSM 18148T (= HO3-R19T = KACC 11381T ) was isolated from seashore sand [1] which belongs to family Xanthomonadaceae . So far, the genus Arenimonas contained seven species, Arenimonas donghaensis (type species) [1], Arenimonas malthae [2], Arenimonas oryziterrae [3], Arenimonas composti [3], Arenimonas metalli [4], Arenimonas daejeonensis [5] and Arenimonas daechungensis [6]. These bacteria were isolated from seashore sand [1], oil-contaminated soil [2], rice rhizosphere [3], compost [3], iron mine [4], compost [5] and sediment of a eutrophic reservoir [6], respectively. The species A. composti [3] was previously classified as Aspromonas composti [7].

The common characteristics of the Arenimonas strains are Gram-staining-negative, aerobic, rod-shaped, non-spore-forming, oxidase-positive, non-indole-producing, non-nitrate-reducing, containing iso-C16:0 and iso-C15:0 as the major fatty acids, phosphatidylglycerol and phosphatidylethanolamine as the major polar lipids, Q-8 as the major respiratory quinone, and possessing relatively high DNA G + C content (63.9–70.8 mol %) [17].

In order to provide genome information and determine genomic differences of Arenimonas species, we performed genome sequencing of strains A. donghaensis DSM 18148T , A. composti KCTC 12666T , A. malthae CCUG 53596T , A. metalli CF5-1T and A. oryziterrae KCTC 22247T . In this study, we report the genomic features of A. donghaensis DSM 18148T and compare it to the close relatives.

Organism information

Classification and features

Strain A. donghaensis DSM 18148T shares 93.1–95.7 % 16S rRNA gene identities with the other six type strains of Arenimonas species, A. malthae CC-JY-1T (DQ239766) (95.7 %), A. daejeonensis T7-07T (AM229325) (95.7 %), A. metalli CF5-1T (HQ698842) (94.6 %), A. oryziterrae YC6267T (EU376961) (94.3 %), A. composti TR7-09T (AM229324) (94.3 %) and A. daechungensis CH15-1T (JN033774) (93.1 %). A 16S rRNA gene based neighbor-joining phylogenetic tree of the related strains was obtained using MEGA 5.05 software [8] (Fig. 1).
Fig. 1

A phylogenetic tree based on the 16S rRNA gene sequences highlighting the position of A. donghaensis HO3-R19T (shown in bold) related to the strains of Arenimonas. The GenBank accession numbers are shown in parentheses. Sequences were aligned using CLUSTALW, and phylogenetic inferences were obtained using the neighbor-joining method within the MEGA 5.05 software [8]. Numbers at the nodes represent percentages of bootstrap values obtained by repeating the analysis 1000 times to generate a majority consensus tree. The scale bar indicates 0.02 nucleotide change per nucleotide position

Cells of A. donghaensis DSM 18148T are Gram-negative, aerobic, non-spore-forming, straight or slightly curved rods, motile by means of a single polar flagellum. Colonies are yellowish white, translucent and convex on R2A agar after 3 d cultivation (Fig. 2). API ID 32 GN and Biolog GN2 MicroPlate systems (bioMe’rieux) were used to investigate sole carbon source utilization, and β-hydroxybutyric acid, L-alaninamide, L-glutamic acid and glycyl-L-glutamic acid could be utilized by strain DSM 18148T (Table 1).
Fig. 2

A scanning electron micrograph of A. donghaensis DSM 18148T cells

Table 1

Classification and general features of A. donghaensis strain DSM 18148T according to the MIGS recommendations [21]

MIGS ID

Property

Term

Evidence codea

 

Classification

Domain Bacteria

TAS [22]

Phylum Proteobacteria

TAS [23]

Class Gammaproteobacteria

TAS [24, 25]

Order Xanthomonadales

TAS [24, 26]

Family Xanthomonadaceae

TAS [24, 26]

Genus Arenimonas

TAS [1]

Species Arenimonas donghaensis

TAS [1]

Type strain: HO3-R19T (= KACC 11381T = DSM 18148T)

Gram stain

negative

TAS [1]

Cell shape

straight or slightly curved rod

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

7.0–9.0; 8.0

TAS [1]

Carbon source

casein, tyrosine and gelatin; β-hydroxybutyric acid, L-alaninamide, L-glutamic acid and glycyl-L-glutamic acid

IDA

GS-6

Habitat

seashore sand

TAS [1]

MIGS-6.3

Salinity

0–3 % 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

Pohang city, Korea

TAS [1]

MIGS-5

Sample collection

not reported

 

MIGS-4.1

Latitude

not reported

 

MIGS-4.2

Longitude

not reported

 

MIGS-4.4

Altitude

not reported

 

a,Evidence codes – IDA Inferred from Direct Assay, 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 [27]

The major fatty acids of A. donghaensis DSM 18148T are iso-branched types, such as iso-C16:0, iso-C15:0 and iso-C17:1 ω9c [1]. Major isoprenoid quinone of this bacterium is Q-8 [1]. Diphosphatidylglycerol (DPG), PG and PE are the major polar lipids of this strain [1].

Genome sequencing information

Genome project history

Genome sequencing project of A. donghaensis DSM 18148T was carried out in April, 2013 and was finished in two months. The obtained high-quality draft genome of A. donghaensis DSM 18148T has been deposited at DDBJ/EMBL/GenBank under accession number AVCJ00000000. The version described in this study is the first version, AVCJ01000000. 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

332.4×

MIGS 30

Assemblers

SOAPdenovo v1.05

MIGS 32

Gene calling method

GeneMarkS+

 

Locus Tag

N788

 

GenBank ID

AVCJ00000000

 

GenBank Date of Release

2014/08/25

 

GOLD ID

Gi0067066

 

BIOPROJECT

PRJNA214575

MIGS 13

Source Material Identifier

DSM 18148

 

Project relevance

Genome comparison

Growth conditions and genomic DNA preparation

A. donghaensis DSM 18148T was cultivated aerobically in LB medium at 28 °C for 3 d. The DNA was extracted, concentrated and purified using the QiAamp kit according to the manufacturer’s instruction (Qiagen, Germany).

Genome sequencing and assembly

The whole-genome sequence of A. donghaensis DSM 18148T was determined using the Illumina Hiseq2000 [9] with the Paired-End library strategy (300 bp insert size) at Shanghai Majorbio Bio-pharm Technology Co., Ltd. [10] (Shanghai, China). A total of 9,571,421 reads with an average read length of 93 bp (885.9 Mb data) was obtained. The detailed methods of library construction and sequencing can be found at Illumina’s official website [9]. Using SOAPdenovo v1.05 [11], these reads were assembled into 51 contigs (>200 bp) with a genome size of 2,977,056 bp and an average coverage of 332.4 x.

Genome annotation

The draft sequence of strain A. donghaensis DSM 18148T was submitted to NCBI Prokaryotic Genome Annotation Pipeline [12] for annotation according to the draft WGS annotation guideline at this website. This annotation pipeline combines the GeneMarkS+ algorithm with the similarity-based gene detection approach to calling gene. The function of the predicted genes from the automatic result was manually modified through BlastX analysis against the NCBI protein database with E-value cutoff 1-e20.

Genome properties

The whole genome of A. donghaensis DSM 18148T is 2,977,056 bp in length, with a G + C content of 68.7 % (Fig. 3 and Table 3), and distributed in 51 contigs (>200 bp). Of the 2735 predicted genes, 2685 (98.17 %) are protein-coding genes, 49 (1.79 %) are RNA genes and 1 (0.04 %) are pseudogenes. A total of 472 (17.26 %) CDSs were assigned with putative functions, while the remaining ones were annotated as hypothetical proteins. The result of protein function classification is shown in Table 4, which was performed by searching all the predicted coding sequences of strain DSM 18148T against the Clusters of Orthologous Groups protein database [13] using BlastP algorithm with E-value cutoff 1-e10. A more detailed summary of the genome properties about this strain is provided in Table 3.
Fig. 3

Graphical circular map of A. donghaensis DSM 18148T genome. From outside to center, ring 1, 4 show protein-coding genes colored by COG categories on forward/reverse strand; ring 2, 3 denote genes on forward/reverse strand; ring 5 shows G + C% content plot, and the innermost ring shows GC skew

Table 3

Genome statistics

Attribute

Value

% of Total

Genome size (bp)

2,977,056

100.00

DNA coding (bp)

2,722,012

91.43

DNA G + C (bp)

2,046,559

68.74

DNA scaffolds

49

 

Total genes

2735

100.00

Protein coding genes

2685

98.17

RNA genes

49

1.79

Pseudo genes

1

0.04

Genes in internal clusters

  

Genes with function prediction

472

17.26

Genes assigned to COGs

2244

82.05

Genes with Pfam domains

2194

80.22

Genes with signal peptides

362

13.24

Genes with transmembrane helices

717

26.22

CRISPR repeats

0

0.00

Table 4

Number of genes associated with general COG functional categories

Code

Value

% age

Description

J

163

6.07

Translation, ribosomal structure and biogenesis

A

1

0.04

RNA processing and modification

K

127

4.73

Transcription

L

107

3.99

Replication, recombination and repair

B

1

0.04

Chromatin structure and dynamics

D

28

1.04

Cell cycle control, Cell division, chromosome partitioning

V

56

2.09

Defense mechanisms

T

171

6.37

Signal transduction mechanisms

M

155

5.77

Cell wall/membrane biogenesis

N

37

1.38

Cell motility

U

68

2.53

Intracellular trafficking and secretion

O

114

4.25

Posttranslational modification, protein turnover, chaperones

C

146

5.44

Energy production and conversion

G

57

2.12

Carbohydrate transport and metabolism

E

173

6.44

Amino acid transport and metabolism

F

55

2.05

Nucleotide transport and metabolism

H

111

4.13

Coenzyme transport and metabolism

I

102

3.80

Lipid transport and metabolism

P

96

3.58

Inorganic ion transport and metabolism

Q

49

1.82

Secondary metabolites biosynthesis, transport and catabolism

R

241

8.98

General function prediction only

S

186

6.93

Function unknown

-

441

16.42

Not in COGs

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

Insights from the genome sequences

Strain A. donghaensis DSM 18148T can only use several sole carbon sources and cannot assimilate glucose and other sugars [1]. Genome analysis using the Kyoto Encyclopedia of Genes and Genomes (KEGG) [14] orthology and pathway assignment analysis revealed this strain has a complete TCA cycle, but lacks the hexokinase which catalyzes the first step of glycolysis, as well as the glucose-6-phosphate dehydrogenase, gluconolactonase and 6-phosphogluconate dehydrogenase that responsible for the oxidative phase of pentose phosphate pathway. This is in agreement with the experimental result that this bacterium can only use several sole carbon sources.

The general features of the five Arenimonas sequenced genomes are summarized in Table 5. Orthologs clustering analysis was performed using OrthoMCL [15] with Match cutoff of 50 % and E-value Exponent cutoff of 1-e5 for the five Arenimonas genomes. These five Arenimonas bacteria share 1014 genes, which are classified into 21 COG functional categories. The major categories are energy production and conversion (8.7 %), amino acid transport and metabolism (8.7 %), coenzyme transport and metabolism (5.8 %), lipid transport and metabolism (5.1 %), translation, ribosomal structure and biogenesis (12.4 %), replication, recombination and repair (5.2 %), cell wall/membrane/envelope biogenesis (5.9 %), posttranslational modification, protein turnover, chaperones (6.3 %), general function prediction only (8.4 %), function unknown (7.3 %) and signal transduction mechanisms (5.3 %) (Fig. 4 and Table 6).
Table 5

General features of the five Arenimonas genomes

Strains

Source

Size (Mb)

CDSs

rRNA clusters

tRNAs

Draft/finished

Genome status contigs

Contigs N50

GenBank no.

A. composti KCTC 12666T

Compost

3.16

2849

3

45

Draft

95

81,415

AWXU00000000

A. donghaensis DSM 18148T

Seashore sand

2.98

2685

4

45

Draft

51

159,562

AVCJ00000000

A. malthae CCUG 53596T

Oil-contaminated soil

3.11

2861

5

44

Draft

221

29,626

AVCH00000000

A. metalli CF5-1T

Iron mine

3.06

2775

2

44

Draft

65

99,300

AVCK00000000

A. oryziterrae KCTC 22247T

Rice rhizosphere

3.09

2897

3

45

Draft

45

441,364

AVCI00000000

Fig. 4

Genome comparison among the five Arenimonas species. Venn diagram illustrates the number of genes unique or shared among the five Arenimonas genomes

Table 6

Number of genes in the core genome of the five analyzed Arenimonas genomes associated with general COG functional categories

Code

Value

% age

Description

A

1

0.10

RNA processing and modification

C

88

8.68

Energy production and conversion

D

16

1.58

Cell cycle control, cell division, chromosome partitioning

E

88

8.68

Amino acid transport and metabolism

F

42

4.14

Nucleotide transport and metabolism

G

20

1.97

Carbohydrate transport and metabolism

H

59

5.82

Coenzyme transport and metabolism

I

52

5.13

Lipid transport and metabolism

J

126

12.43

Translation, ribosomal structure and biogenesis

K

44

4.34

Transcription

L

53

5.23

Replication, recombination and repair

M

60

5.92

Cell wall/membrane/envelope biogenesis

N

12

1.18

Cell motility

O

64

6.31

Posttranslational modification, protein turnover, chaperones

P

32

3.16

Inorganic ion transport and metabolism

Q

22

2.17

Secondary metabolites biosynthesis, transport and catabolism

R

85

8.38

General function prediction only

S

74

7.30

Function unknown

T

54

5.33

Signal transduction mechanisms

U

27

2.66

Intracellular trafficking, secretion, and vesicular transport

V

11

1.08

Defense mechanisms

-

0

0.00

Not in COGs

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

There are 601 strain-specific genes for A. donghaensis DSM 18148T which may contribute to species-specific features of this bacterium. Among them, 359 are classified into 20 COG functional categories major belonging to transcription (6.3 %), general function prediction only (8.5 %), function unknown (7.3 %) and signal transduction mechanisms (9.0 %). The remaining 242 unique genes (40.3 %) are not classified into any COG categories (Fig. 4 and Table 7). In addition, the five Arenimonas strains had a pan-genome [16] size of 7501 genes. The nucleotide diversity (π) was calculated using MAUVE v2.3 [17] and DnaSP v5 [18]. The five genomes of Arenimonas species had a nucleotide diversity (π) value of 0.18, which means an approximate genus-wide nucleotide sequence homology of 82 %.
Table 7

Number of strain-specific genes of A. donghaensis DSM 18148T associated with general COG functional categories

Code

Value

% age

Description

C

15

2.50

Energy production and conversion

D

3

0.50

Cell cycle control, cell division, chromosome partitioning

E

17

2.83

Amino acid transport and metabolism

F

3

0.50

Nucleotide transport and metabolism

G

6

1.00

Carbohydrate transport and metabolism

H

15

2.50

Coenzyme transport and metabolism

I

9

1.50

Lipid transport and metabolism

J

7

1.16

Translation, ribosomal structure and biogenesis

K

38

6.32

Transcription

L

11

1.83

Replication, recombination and repair

M

25

4.16

Cell wall/membrane/envelope biogenesis

N

4

0.67

Cell motility

O

10

1.66

Posttranslational modification, protein turnover, chaperones

P

18

3.00

Inorganic ion transport and metabolism

Q

6

1.00

Secondary metabolites biosynthesis, transport and catabolism

R

51

8.49

General function prediction only

S

44

7.32

Function unknown

T

54

8.99

Signal transduction mechanisms

U

7

1.16

Intracellular trafficking, secretion, and vesicular transport

V

16

2.66

Defense mechanisms

-

242

40.27

Not in COGs

The total is based on the total number of strain-specific genes of A. donghaensis DSM 18148T

The clustered regularly interspaced short palindromic repeats (CRISPRs) mediate resistance to foreign genetic material and thus inhibit horizontal gene transfer [19]. Screening the CRISPRs system in the five Arenimonas genomes using CRISPRfinder program online [20] found that only one CRISPR system (on contig 41) exist in the genome of A. composti KCTC 12666T . This CRISPR length is 5331 bp, with 29 bp direct repeat (DR) sequences be separated by 87 spacers.

Fifteen available genome sequences of the family Xanthomonadaceae were chosen for genomic based phylogenetic analysis, including the five Arenimonas genomes that were sequenced by us. In total, 1014 core protein sequences were extracted using the cluster algorithm tool OrthoMCL with default parameters [15]. The neighbor-joining (NJ) phylogenetic tree showed that the five Arenimonas species clustered into the same branch (Fig. 5), which is in accordance with the 16S rRNA gene-based phylogeny (Fig. 1).
Fig. 5

A phylogenetic tree highlighting the phylogenetic position of A. donghaensis DSM 18148T. The conserved protein was analyzed by OrthoMCL with Match Cutoff 50 % and E-value Exponent Cutoff 1-e5 [15]. The phylogenetic tree was constructed based on the 1014 single-copy conserved proteins shared among the fifteen genomes. The phylogenies were inferred by MEGA 5.05 with NJ algorithm [8], and 1000 bootstrap repetitions were computed to estimate the reliability of the tree. The genome accession numbers of the strains are shown in parentheses

Similar to A. donghaensis DSM 18148T , the TCA cycle is complete and hexokinase is absent in all the five Arenimonas strains. The proteins responsible for the oxidative phase of pentose phosphate pathway are also incomplete in five Arenimonas strains, this may be part of the reasons that the five Arenimonas strains can only use several single carbon sources.

Conclusions

To the best of our knowledge, this report provides the first genomic information of the genus Arenimonas . 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 genome shows certain correlation between the genotypes and the phenotypes especially on utilization of sole carbon sources.

Abbreviations

KACC: 

Korean Agricultural Culture Collection

DSMZ: 

German Collection of Microorganisms and Cell Cultures

DPG: 

Diphosphatidylglycerol

PG: 

Phosphatidylglycerol

PE: 

Phosphatidylethanolamine

Declarations

Acknowledgments

This work was supported by the National Natural Science Foundation of China (31470226).

Open Access This 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

© Chen et al. 2015