Open Access

High-quality draft genome sequence of Gracilimonas tropica CL-CB462T (DSM 19535T), isolated from a Synechococcus culture

  • Dong Han Choi1,
  • Chisang Ahn2,
  • Gwang Il Jang2,
  • Alla Lapidus3, 4,
  • James Han5,
  • T. B. K. Reddy5,
  • Marcel Huntemann5,
  • Amrita Pati4,
  • Natalia Ivanova5,
  • Victor Markowitz6,
  • Manfred Rohde7,
  • Brian Tindall8,
  • Markus Göker8,
  • Tanja Woyke5,
  • Hans-Peter Klenk8, 9,
  • Nikos C Kyrpides5, 10 and
  • Byung Cheol Cho2Email author
Standards in Genomic Sciences201510:98

DOI: 10.1186/s40793-015-0088-8

Received: 29 September 2014

Accepted: 23 October 2015

Published: 11 November 2015

Abstract

Gracilimonas tropica Choi et al. 2009 is a member of order Sphingobacteriales, class Sphingobacteriia. Three species of the genus Gracilimonas have been isolated from marine seawater or a salt mine and showed extremely halotolerant and mesophilic features, although close relatives are extremely halophilic or thermophilic. The type strain of the type species of Gracilimonas, G. tropica DSM19535T, was isolated from a Synechococcus culture which was established from the tropical sea-surface water of the Pacific Ocean. The genome of the strain DSM19535T was sequenced through the Genomic Encyclopedia of Type Strains, Phase I: the one thousand microbial genomes project. Here, we describe the genomic features of the strain. The 3,831,242 bp long draft genome consists of 48 contigs with 3373 protein-coding and 53 RNA genes. The strain seems to adapt to phosphate limitation and requires amino acids from external environment. In addition, genomic analyses and pasteurization experiment suggested that G. tropica DSM19535T did not form spore.

Keywords

Genome Gracilimonas tropica Marine Sphingobacteriia GEBA

Introduction

The genus Gracilimonas was first established in 2009 [1], and at the time of writing this paper there are three species that comprise this genus, G. tropica [1], G. mengyeensis [2], and G. rosea [3]. They are Gram-negative, catalase- and oxidase-positive, aerobic and facultatively anaerobic and have rod-shaped cells (Fig. 1) [13]. In addition, they form endospores except G. mengyeensis [3]. Gracilimonas tropica CL-CB462T (=KCCM 90063T = DSM 19535T ), the type strain of the type species of the genus Gracilimonas , was isolated from a Synechococcus culture which was established from the tropical sea-surface water of the Pacific Ocean [1]. Interestingly, the genus Gracilimonas formed a robust clade together with extremely halophilic or thermophilic bacteria ( Salinibacter ruber and Rhodothermus marinus , respectively). On the contrary, Gracilimonas species show only extremely halotolerant and mesophilic features. Considering the phenotypic diversity within the clade, their comparative genomic analyses could provide a good clue to understand bacterial adaptation to extreme environments based on genomic context. Here we present a summary of the genomic features of G. tropica DSM 19535T , which is the first genome-sequenced type strain from the genus Gracilimonas .
Fig. 1

Scanning electron microscopy image of Gracilimonas tropica DSM19535T

Organism information

Classification and features

Phylogenetic analysis based on 16S rRNA gene sequence comparison revealed G. tropica DSM19535T is classified into the genus Gracilimonas (Fig. 2). The type strains which were most closely related to strain DSM19535T were Gracilimonas mengyeensis YIM J14T with 16S rRNA sequence similarity of 96.9 %, and Gracilimonas rosea CL-KR2T with a similarity of 96.1 %. Strain DSM19535T is tolerant of high salinity (up to 20 %) with a growth occurring over the range of salinity of 1–20 % (w/v) sea salts (optimum 3–6 %) (Table 1). Growth occurs under either aerobic or facultatively anaerobic conditions. The optimum pH is 7.0–8.0 with a growth range of pH 6–10 (Table 1). The strain was auxotroph for isoleucine and methionine (Table 1). Despite the phylum Bacteroidetes is known to be as a non-spore forming group [4], the strain was reported to form endospores, together with G. rosea [3]. However, strain DSM19535T could not be asserted to form spore by the genomic analysis (see ‘Insights from the genome sequence’).
Fig. 2

Neighbour-joining tree, based on 16S rRNA gene sequences, showing the phylogenetic position of G. tropica DSM 19535T. Bootstrap percentages >50 % (based on 1000 resampling) are shown at branching points. Solid circles indicate that the corresponding nodes are also recovered in the maximum-likelihood and maximum-parsimony trees. Prolixibacter bellariivorans F2T was used as an outgroup. Bar, 0.02 nucleotide substitutions per site

Table 1

Classification and general features of G. tropica DSM 19535T [38, 39]

MIGS ID

Property

Term

Evidence codea

 

Current classification

Domain Bacteria

TAS [40]

Phylum Bacteriodetes

TAS [4]

Class Sphingobacteriia

TAS [41]

Order Sphingobacteriales

TAS [41]

Genus Gracilimonas

TAS [1]

Species Gracilimonas tropica

TAS [1]

Type strain CL-CB462T

TAS [1]

 

Gram stain

Negative

TAS [1]

 

Cell shape

Rod-shaped

TAS [1]

 

Motility

Non-motile

TAS [1]

 

Sporulation

Non-sporulation

IDA

 

Temperature range

20–40 °C

TAS [1]

 

Optimum temperature

35 °C

TAS [1]

 

Energy source

Heterotroph

TAS [1]

 

Auxotroph for

L-isoleucine, L-methionine

IDA

 

Carbon source

Glucose, fructose, aspartate

TAS [1]

MIGS-6

Habitat

Marine, aquatic

TAS [1]

MIGS-6.2

pH

6–10

TAS [1]

MIGS-6.3

Salinity

1–20 % (optimum: 3–6 %)

TAS [1]

MIGS-22

Oxygen requirement

Facultative

TAS [1]

MIGS-15

Biotic relationship

Free living

TAS [1]

MIGS-14

Pathogenicity

Unknown

NAS

MIGS-4

Geographic location

Tropical NW Pacific

TAS [1]

MIGS-5

Sample collection

2009

TAS [1]

MIGS-4.1

Latitude

Unknown

NAS

MIGS-4.2

Longitude

Unknown

NAS

MIGS-4.4

Altitude

0 m

NAS

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 [42]

By phylogenetic analyses (Fig. 2), the genus Gracilimonas formed a sister clade with the genus Balneola which shows mesophilic features [5, 6]. At an outer branch, the clade with Gracilimonas and Balneola formed a robust clade with the moderate halophilic Fodinibius salinus (Fig. 2). Moreover, at a deeper branch, the clade formed a robust association with a clade that includes the thermophilic genus Rhodothermus [7] and the genus of extremely halophilic Salinibacter [8], despite the relatively low (ca. 80 %) similarities between the two clades. Thus, the phylogentically robust clade contains both extremophiles and non-extremophiles.

Auxotrophy for amino acids was examined using a minimal medium (glucose, 2 g; pyruvate, 0.3 g; K2HPO4, 3 g; NaH2PO4, 1 g; NH4Cl, 1 g; MgSO4•7H2O, 0.3 g; 1 ml of Holden’s trace elements [9]; 1 ml of Balch’s vitamin solution [10]; 1 L of artificial seawater [11]) supplemented with 0.3 mM or 3 mM of all amino acids except a focal amino acid. The strain could not grow in minimal medium without supplementation of L-isoleucine and L-methionine. But, the strain did not require other amino acids (L-alanine, L-arginine, L-asparagine, L-aspartate, L-cysteine, L-glutamate, L-glutamine, glycine, L-histidine, L-lysine, L-phenylalanine, L-proline, L-serine, L-threonine, L-tryptophan, L-tyrosine and selenocysteine) for growth.

Genome sequencing information

Genome project history

A culture of DSM 19535T (strain CL-CB462T) was selected for sequencing on the basis of its phylogenetic position [12, 13], and is part of the Genomic Encyclopedia of Type Strains, Phase I: the one thousand microbial genomes project [14], a follow-up of the Genomic Encyclopedia of Bacteria and Archaea pilot project [15], which aims in increasing the sequencing coverage of key reference microbial genomes and to generate a large genomic basis for the discovery of genes encoding novel enzymes [16]. The one thousand microbial genomes-I is the first of the production phases of the Genomic Encyclopedia of Bacteria and Archaea: sequencing a myriad of type strains initiative [17] and a Genomic Standards Consortium project [18]. The genome project is deposited in the Genomes On Line Database [19] and the genome sequence is available from GenBank. Sequencing, finishing and annotation were performed by the DOE Joint Genome Institute (JGI) using state of the art sequencing technology [20]. A summary of the project information is presented in Table 2.
Table 2

Project information

MIGS ID

Property

Term

MIGS-31

Finishing quality

Level 2: High Quality Draft

MIGS-28

Libraries used

Illumina Std shotgun library

MIGS-29

Sequencing platforms

Illumina

MIGS-31.2

Sequencing coverage

421×

MIGS-30

Assemblers

Velvet v. 1.1.04, ALLPATHS v. R41043

MIGS-32

Gene calling method

Prodigal v2.5

 

NCBI project ID

169,820

 

Genbank ID

AQXG00000000

 

Genbank Date of Release

December 12, 2013

 

GOLD ID

Gp0013655

 

BIOPROJECT

PRJNA169820

MIGS-13

Source Material Identifier

DSM 19,535

 

Project relevance

GEBA-KMG, Tree of Life

Growth conditions and genomic DNA preparation

G. tropica DSM 19535T , was grown in DSMZ medium 514 (Bacto Marine Broth) [21] at 28 °C. Genomic DNA was isolated from about 0.5 g of cell paste using Jetflex Purification Kit (Epicentre MGP04100) following the standard protocol as recommended by the manufacturer with an additional protease K (50 μl; 21 mg/ml) digest for 60 min. at 58 °C followed by addition of 200 μl Protein Precipitation Buffer after protein precipitation and overnight incubation on ice [22]. DNA was quality controlled according to JGI guidelines and is available through the DNA Bank Network [23].

Genome sequencing and assembly

The draft genome was generated using Illumina technology [24]. An Illumina Std shotgun library was constructed and sequenced using the Illumina HiSeq 2000 platform which generated 14,058,618 reads totaling 2108.8 Mbp. All general aspects of library construction and sequencing performed at the JGI can be found at [25]. All raw Illumina sequence data was passed through DUK, a filtering program developed at JGI, which removes known Illumina sequencing and library preparation artifacts (Mingkun L, Copeland A, Han J. DUK, unpublished, 2011). Artifact filtered sequence data was then screened and trimmed according to the k–mers present in the dataset (Mingkun L. kmernorm, unpublished, 2011). High–depth k–mers, presumably derived from MDA amplification bias, cause problems in the assembly, especially if the k–mer depth varies in orders of magnitude for different regions of the genome. Reads with high k–mer coverage (>30 × average k–mer depth) were normalized to an average depth of 30×. Reads with an average kmer depth of less than 2× were removed. Following steps were then performed for assembly: (1) normalized Illumina reads were assembled using Velvet version 1.1.04 [26], (2) 1–3 Kbp simulated paired end reads were created from Velvet contigs using wgsim [27], (3) normalized Illumina reads were assembled with simulated read pairs using Allpaths–LG (version r41043) [28]. Parameters for assembly steps were: 1) Velvet (velveth: 63 –shortPaired and velvetg: −very clean yes –exportFiltered yes –min contig lgth 500 –scaffolding no –cov cutoff 10), 2) wgsim (−e 0 –1 100 –2 100 –r 0 –R 0 –X 0), 3) Allpaths–LG (PrepareAllpathsInputs: PHRED 64 = 1 PLOIDY = 1 FRAG COVERAGE = 125 JUMP COVERAGE = 25 LONG JUMP COV = 50, RunAllpathsLG: THREADS = 8 RUN = std shredpairs TARGETS = standard VAPI WARN ONLY = True OVERWRITE = True). The final draft assembly contained 48 contigs in 48 scaffolds. The total size of the genome is 3.8 Mbp and the final assembly is based on 457.7 Mbp of Illumina data. Based on a presumed genome size of 5Mbp, the average coverage of the genome was 421 × .

Genome annotation

Genes were identified using Prodigal [29] as part of the DOE-JGI Annotation pipeline [30, 31] followed by a round of manual curation using the JGI GenePRIMP pipeline [32]. The predicted CDSs were translated and used to search the National Center for Biotechnology Information non-redundant database, UniProt, TIGRFam, Pfam, PRIAM, KEGG, COG, and InterPro databases. Additional gene prediction analysis and functional annotation was performed within the Integrated Microbial Genomes [33].

Genome properties

The genome of the strain is 3,831,242 bp long and comprises 48 contigs ranging 1177 to 783,752 bp, with an overall GC content of 42.9 % (Table 3). Of the 3426 genes predicted, 3373 were protein coding genes, and 53 were RNA genes. A total of 2413 genes (70.4 %) were assigned a putative function while the remaining ones were annotated as hypothetical or unknown proteins. The distribution of genes into COG functional categories is presented in Table 4. The properties and the statistics of the genome are summarized in Tables 3 and 4.
Table 3

Genome statistics

Attribute

Number

% of Totala

Genome size (bp)

3,831,242

100.00

DNA coding (bp)

3,482,093

90.89

DNA G + C (bp)

1,645,319

42.94

DNA scaffolds

48

100.00

Total genes

3426

100.00

Protein-coding genes

3373

98.45

RNA genes

53

1.55

Pseudo genes

0

 

Genes in internal clusters

1042

30.41

Genes with function prediction

2413

70.43

Genes assigned to COGs

1931

56.36

Genes with Pfam domains

2557

74.64

Genes with signal peptides

385

11.24

Genes with transmembrane helices

912

26.62

CRISPR repeats

0

 

aThe total is based on either the size of the genome in base pairs or the total number of protein coding genes in the annotated genome

Table 4

Number of genes associated with general COG functional categories

Code

Value

% age

Description

J

138

6.56

Translation, ribosomal structure and biogenesis

A

0

0.00

RNA processing and modification

K

112

5.32

Transcription

L

107

5.09

Replication, recombination and repair

B

1

0.05

Chromatin structure and dynamics

D

24

1.14

Cell cycle control, cell division, chromosome partitioning

V

53

2.52

Defense mechanisms

T

96

4.56

Signal transduction mechanisms

M

175

8.32

Cell wall/membrane biogenesis

N

17

0.81

Cell motility

U

44

2.09

Intracellular trafficking and secretion

O

93

4.42

Posttranslational modification, protein turnover, chaperones

C

133

6.32

Energy production and conversion

G

95

4.52

Carbohydrate transport and metabolism

E

178

8.46

Amino acid transport and metabolism

F

60

2.85

Nucleotide transport and metabolism

H

96

4.56

Coenzyme transport and metabolism

I

80

3.80

Lipid transport and metabolism

P

103

4.90

Inorganic ion transport and metabolism

Q

53

2.52

Secondary metabolites biosynthesis, transport and catabolism

R

263

12.50

General function prediction only

S

183

8.79

Function unknown

-

1495

43.64

Not in COGs

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

Insights from the genome sequence

Based on genomic analysis of the metabolic features, G. tropica DSM19535T is predicted to be an auxotroph for L-lysine, L-phenylalanine, L-tyrosine, L-arginine, L-aspartic acid, L-isoleucine, L-proline, and L-methionine. In the auxotroph test, however, the strain was found to be auxotroph only for L-isoleucine and L-methionine (Table 1). This discrepancy might be due to missing annotations of essential genes by incomplete sequencing or presence of unknown genes related with transport and/or assimilation. In addition, despite selenocysteine was one of essential amino acids required for growth by the genomic analysis, the strain could grow in a medium without selenocysteine. Genome analysis also revealed that strain DSM19535T has a copper-containing nitrite reductase gene (nirK) homolog, suggesting that the strain may transform nitrite to nitric oxide (NO) under low oxygen or anoxic conditions. In addition, the strain contains DnrN (nitric oxide-dependent regulator) gene and this may protect cells from nitrosative stress [34]. However, the nitrate, nitric oxide and nitrous oxide reductases involved in denitrification were not found. The strain has an ATP-dependent glutamine synthetase and a NADPH-dependent glutamate-oxoglutarate amidotransferase, and thus can assimilate ammonia into glutamate and glutamine. In the strain, ammonium may be transported by an ammonium transport protein. Genes participating in phosphate metabolism were also identified in the genome of the strain DSM19535T . Inorganic pyrophosphatase catalyzing the conversion of pyrophosphate to phosphate ion, and polyphosphate kinase catalyzing the formation of polyphosphate from ATP were found in the genome. The strain has several genes of Pho regulon (phoH, phoU, phoR and phoB) mediating an adaptive response to inorganic phosphate limitation but not high affinity phosphate binding protein and transporter (pstS and pstACB). In addition, the strain may hydrolyze phosphate groups from many types of organic molecules using alkaline phosphatase.

In the previous study, G. tropica DSM19535T was reported to be able to form spores [1]. The spore-formation is very unusual in the phylum Bacteroidetes [4]. Despite four and five proteins were annotated as stage II sporulation protein E (SpoIIE) and sporulation related domain, respectively, by search against the Pfam database, more than a hundred sporulation-related genes identified in Bacillus subtilis 168T were absent from the genome of strain DSM19535T . Further, the genes found in G. tropica were also found in genomes of phylogenetically close but non-sporulating genera, Balneola vulgaris DSM 17,893 and Salisaeta longa DSM2114. Therefore, further tests to examine spore-formation were conducted in this study. Consistent with the previous study, spore-like spherical cells were found after malachite green staining. However, after pasteurization at 60 °C for 10 and 20 min and 80, 90 and 100 °C for 10 min, re-growth of cells was never observed, suggesting that the coccoid cells may not be endospore. Actually, non-spore but spore-like spherical cells were also found in aging cultures of a variety of non-sporulating bacteria including Salinispira pacifica belonging to the phylum Spirochaetae , Prolinoborus fasciculus belonging to the class Betaproteobacteria and Anaerophaga thermohalophila belonging to the phylum Bacteroidetes [3537]. The genomic analyses and pasteurization experiment convincingly suggested that the spore-like coccoid cells of G. tropica DSM19535T are not endospores.

Conclusion

The genome of a member belonging to the genus Gracilimonas in the phylum Bacteroidetes is reported here. In addition to detailed information of genome sequencing and annotation, genetic characteristics related with nitrogen and phosphorus utilization could be understood on the basis of genomic analyses. In addition, genomic analyses and pasteurization experiments suggested that G. tropica DSM19535T does not form spores.

Notes

Declarations

Acknowledgements

The authors gratefully acknowledge the help of Susanne Schneider for growing cells of DSM 19535T and of Evelyne-Marie Brambilla (both at DSMZ), for DNA extraction and quality control. This work was performed under the auspices of the US Department of Energy’s Office of Science, Biological and Environmental Research Program, and by the University of California, Lawrence Berkeley National Laboratory under contract No. DE-AC02-05CH11231. This work was also supported in part by a research program (PE99314) of the Korea Institute of Ocean Science and Technology (KIOST), and EAST-1 and the BK21+ project of the Korean Government. This study was supported in part by Russian Ministry of Science Mega-grant no.11.G34.31.0068 (PI. Dr Stephen J O’Brien).

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)
Biological Oceanography & Marine Biology Division, Korea Institute of Ocean Science and Technology
(2)
Microbial Oceanography Laboratory, School of Earth and Environmental Sciences, and Research Institute of Oceanography, Seoul National University
(3)
Theodosius Dobzhansky Center for Genome Bioinformatics, St. Petersburg State University
(4)
Algorithmic Biology Lab, St. Petersburg Academic University
(5)
Department of Energy Joint Genome Institute, Genome Biology Program
(6)
Biological Data Management and Technology Center, Lawrence Berkeley National Laboratory
(7)
Central Facility for Microscopy, HZI – Helmholtz Centre for Infection Research
(8)
Leibniz Institute DSMZ – German Collection of Microorganisms and Cell Cultures
(9)
School of Biology, Newcastle University
(10)
Department of Biological Sciences, Faculty of Science, King Abdulaziz University

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