Open Access

Draft genome sequence of Marinobacterium rhizophilum CL-YJ9T (DSM 18822T), isolated from the rhizosphere of the coastal tidal-flat plant Suaeda japonica

  • Dong Han Choi1,
  • Gwang II Jang2,
  • Alla Lapidus3, 4,
  • Alex Copeland5,
  • T. B. K. Reddy5,
  • Supratim Mukherjee5,
  • Marcel Huntemann5,
  • Neha Varghese4,
  • Natalia Ivanova5,
  • Manoj Pillay6,
  • Brian J. Tindall7,
  • Markus Göker7,
  • Tanja Woyke5,
  • Hans-Peter Klenk8,
  • Nikos C. Kyrpides5 and
  • Byung Cheol Cho2Email author
Contributed equally
Standards in Genomic Sciences201712:65

https://doi.org/10.1186/s40793-017-0275-x

Received: 24 May 2017

Accepted: 25 September 2017

Published: 30 October 2017

Abstract

The genus Marinobacterium belongs to the family Alteromonadaceae within the class Gammaproteobacteria and was reported in 1997. Currently the genus Marinobacterium contains 16 species. Marinobacterium rhizophilum CL-YJ9T was isolated from sediment associated with the roots of a plant growing in a tidal flat of Youngjong Island, Korea. The genome of the strain CL-YJ9T was sequenced through the Genomic Encyclopedia of Type Strains, Phase I: KMG project. Here we report the main features of the draft genome of the strain. The 5,364,574 bp long draft genome consists of 58 scaffolds with 4762 protein-coding and 91 RNA genes. Based on the genomic analyses, the strain seems to adapt to osmotic changes by intracellular production as well as extracellular uptake of compatible solutes, such as ectoine and betaine. In addition, the strain has a number of genes to defense against oxygen stresses such as reactive oxygen species and hypoxia.

Keywords

Genome Marinobacterium rhizophilum Suaeda Japonica RhizosphereGEBA

Introduction

The genus Marinobacterium within the family Alteromonadaceae was established in 1997 by González et al. [1]. Currently the genus Marinobacterium contains 16 species with validly published names (Fig. 1). All Marinobacterium strains have been isolated from marine environments [111] such as sea water, tidal flat, deep-sea sediment, and coral mucus. Interestingly, their habitats include tropical waters [12, 13], Arctic marine sediment [7], tidal flats [4, 11] as well as deep sea sediment [10], indicating that the genus has well adapted to diverse environments. In the GOLD database [14], genome sequencing of 38 strains from 11 Marinobacterium species are identified to be finished or in progress. In addition, six genome sequences from five species ( M. jannaschii , M. litorale , M. rhizophilum , M. stanieri and M. profundum ) and one unidentified strain are found in the GenBank database. Among them, genomic features of M. rhizophilum CL-YJ9T (=DSM 18822=KCCM 42386 T), isolated from the rhizosphere of a plant Suaeda japonica inhabiting a coastal tidal flat, Korea, will be presented here.
Fig. 1

Neighbour-joining phylogenetic tree, based on 16S rRNA gene sequences, showing the relationships between strain CL-YJ9T, members of the genus Marinobacterium and other related genera. Bootstrap percentages >60% (based on 1000 resamplings) are shown below or above the corresponding branches. Solid circles indicate that the corresponding nodes are also recovered in the maximum-likelihood and maximum-parsimony trees. Terasakiella pusillum IFO 13613T (AB006768) was used as an outgroup. Bar, 0.02 nucleotide substitutions per site

Organism information

Classification and features

By phylogenetic analysis of the 16S rRNA gene sequence (Fig. 1), M. rhizophilum strain CL-YJ9T was positioned within the genus Marinobacterium and formed a distinct branch together with Marinobacterium profundum PAMC 27536 T and Marinobacterium nitratireducens CN44T (Fig. 1). Strain CL-YJ9T was most closely related to Marinobacterium profundum PAMC 27536 T, which appeared as its sister species in the tree. Strain CL-YJ9T grows under strictly aerobic conditions (Table 1). The optimal growth of strain CL-YJ9T occurs at pH 7.0, with a growth range of pH 6.0–9.0. Growth occurs in the presence of 1.0–5.0% (w/v) NaCl (optimum 3.0%) and at 5–30 °C (optimum 25 °C) (Table 1). Cells of strain CL-YJ9T are rod-shaped, on average approximately 0.3–0.4 μm wide and 0.6–0.8 μm long and motile by means of monopolar flagella (Fig. 2).
Table 1

Classification and general features of M. rhizophilum CL-YJ9T [8, 9]

MIGS ID

Property

Term

Evidence codea

 

Classification

Domain Bacteria

TAS [39]

  

Phylum Proteobacteria

TAS [40]

  

Class Gammaproteobacteria

TAS [41]

  

Order Alteromonadales

TAS [42]

  

Family Alteromonadaceae

TAS [43]

  

Genus Marinobacterium

TAS [1]

  

Species Marinobacterium rhizophilum

TAS [4]

  

Type strain CL-YJ9T

TAS [4]

 

Gram stain

Negative

TAS [4]

 

Cell shape

Straight rods

TAS [4]

 

Motility

Motile

TAS [4]

 

Sporulation

Not reported

NAS

 

Temperature range

5-30 °C

TAS [4]

 

Optimum temperature

25 °C

TAS [4]

 

pH range; Optimum

6.0-9.0; 7.0

TAS [4]

 

Carbon source

Glucose, sucrose, mannose, glycerol, glycine, mannitol

TAS [4]

MIGS-6

Habitat

Sediment closely associated with the roots of a plant (Suaeda japonica)

TAS [4]

MIGS-6.3

Salinity

1-5% (optimum: 3%)

TAS [4]

MIGS-22

Oxygen requirement

Strictly aerobic

TAS [4]

MIGS-15

Biotic relationship

Microbiota of the rhizome of Suaeda japonica

TAS [4]

MIGS-14

Pathogenicity

Non-pathogenic

NAS

MIGS-4

Geographic location

Youngjong Island, Korea

TAS [4]

MIGS-5

Sample collection

November, 2005

TAS [4]

MIGS-4.1

Latitude

37.485o N

TAS [4]

MIGS-4.2

Longitude

126.516o E

TAS [4]

MIGS-4.3

Depth

Not reported

NAS

MIGS-4.4

Altitude

Not reported

NAS

aEvidence 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 [44]

Fig. 2

Transmission electron microscopy image of Marinobacterium rhizophilum CL-YJ9T

Genome sequencing information

Genome project history

The strain CL-YJ9T was chosen for genome sequencing by the phylogeny-based selection [15, 16] as a part of the Genomic Encyclopedia of Type Strains, Phase I: the KMG project [17]. The KMG project, the first of the production phases of the GEBA: sequencing a myriad of type strains initiative [18, 19] and a Genomic Standards Consortium project [20] was set up to increase the sequencing coverage of key reference microbial genomes and to generate a large genomic basis for the discovery of genes encoding novel enzymes [21]. The genome sequencing, finishing and annotation were performed by the DOE-JGI using state of the art sequencing technology [22]. A summary of the project information is presented in Table 2.
Table 2

Genome sequencing project information

MIGS ID

Property

Term

MIGS-31

Finishing quality

Level 1: Standard Draft

MIGS-28

Libraries used

Illumina Std shotgun library

MIGS-29

Sequencing platforms

Illumina HiSeq 2000

MIGS-31.2

Fold coverage

119.1X

MIGS-30

Assemblers

Velvet v. 1.1.04, ALLPATHS v. R37654

MIGS-32

Gene calling method

Prodigal v2.5

 

Locus Tag

F451

 

Genbank ID

ARJM00000000

 

Genbank Date of Release

12-Dec-2013

 

GOLD ID

Gp0013985

 

BIOPROJECT

PRJNA181367

MIGS-13

Source Material Identifier

CL-YJ9

 

Project relevance

GEBA-KMG, Tree of Life

Growth conditions and genomic DNA preparation

M. rhizophilum strain CL-YJ9T was grown in DSMZ medium 514 (http://www.dsmz.de) at 28 °C and aerobe conditions. Genomic DNA was isolated using Jetflex Genomic DNA Purification Kit (GENOMED 600100) following the standard protocol provided by the manufacturer but additionally applying 50 μl proteinase K and using a 60 min incubation time. DNA is available through the DNA Bank Network [23].

Genome sequencing and assembly

Using the purified genomic DNA, the draft genome of M. rhizophilum CL-YJ9 T was generated at the DOE-JGI using the Illumina technology [24]. An Illumina standard shotgun library was constructed and sequenced using the Illumina HiSeq 2000 platform which generated 7,253,734 reads totaling 1088.1 Mbp. All general aspects of library construction and sequencing performed at the JGI can be found at the JGI website. All raw Illumina sequence data was passed through DUK, a filtering program developed at JGI, which removes known Illumina sequencing and library-preparation artifacts [25]. The following steps were then performed for assembly: (1) filtered 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 (https://github.com/lh3/wgsim), (3) Illumina reads were assembled with simulated read pairs using Allpaths–LG (version r41043) [27]. Parameters for assembly steps were exactly same as in Choi et al. [28]. The final draft assembly contained 68 contigs in 58 scaffolds. The total size of the genome is 5.4 Mbp and the final assembly is based on 638.1 Mbp of Illumina data, which provides an average 119.1X coverage of the genome.

Genome annotation

As described in Choi et al. [28], identification of genes was performed using Prodigal [29] as part of the DOE-JGI Annotation pipeline [30, 31]. After translation of the predicted CDSs, they were used to search the databases, such as National Center for Biotechnology Information non-redundant database, UniProt, TIGRFam, Pfam, PRIAM, KEGG, COG, and InterPro databases. Additional analysis and functional annotation were performed within the Integrated Microbial Genomes [32].

Genome properties

The genome is 5,364,574 bp long and comprises 58 scaffolds ranging 1097 to 401,958 bp, with an overall G + C content of 58.5% (Table 3). Of the 4853 genes predicted, 4762 were protein coding genes, and 91 were RNA genes. A total of 3878 genes (79.9%) 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)

5,364,574

100

DNA coding (bp)

4,619,007

86.10

DNA G + C (bp)

3,136,815

58.47

DNA scaffolds

58

100

Total genes

4853

100

Protein coding genes

4762

98.12

RNA genes

91

1.88

Pseudo genes

0

 

Genes in internal clusters

642

13.23

Genes with functional prediction

3878

79.91

Genes assigned to COGs

3433

70.74

Genes with Pfam domains

4066

83.78

Genes with signal peptides

386

7.95

Genes with transmembrane helices

1137

23.43

CRISPR repeats

1

 

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

232

6.01

Translation, ribosomal structure and biogenesis

A

1

0.03

RNA processing and modification

K

289

7.48

Transcription

L

103

2.67

Replication, recombination and repair

B

2

0.05

Chromatin structure and dynamics

D

41

1.06

Cell cycle control, cell division, chromosome partitioning

V

72

1.86

Defense mechanisms

T

182

4.71

Signal transduction mechanisms

M

213

5.52

Cell wall/membrane/envelope biogenesis

N

71

1.84

Cell motility

U

58

1.50

Intracellular trafficking, secretion, and vesicular transport

O

162

4.19

Post-translational modification, protein turnover, chaperones

C

296

7.66

Energy production and conversion

G

334

8.65

Carbohydrate transport and metabolism

E

407

10.54

Amino acid transport and metabolism

F

102

2.64

Nucleotide transport and metabolism

H

211

5.46

Coenzyme transport and metabolism

I

179

4.63

Lipid transport and metabolism

P

186

4.82

Inorganic ion transport and metabolism

Q

134

3.47

Secondary metabolites biosynthesis, transport and catabolism

R

335

8.67

General function prediction only

S

209

5.41

Function unknown

1420

29.26

Not in COGs

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

Insights from the genome sequence

To cope with osmotically varying conditions in tidal flat (e.g., exposure to heavy rainfalls or desiccation during low tides), M. rhizophilum CL-YJ9T seems to display diverse mechanisms of adaption. For instance, the strain can synthesize compatible solutes such as betaine, ectoine and 5-hydroxyectoine. The strain has two kind of genes (choline dehydrogenases and betaine aldehyde dehydrogenase; Table 5) participating in glycine-betaine biosynthesis from choline, which is found in Gram-negative bacteria [33]. The strain also has essential genes participating in the ectoine biosynthesis and the 5-hydroxyectoine biosynthesis (five enzymes for the steps from aspartate to ectoine as well as ectoine hydroxylase, respectively; Table 5) [34]. In addition, the strain seems to uptake osmolytes by transport from the external environment. In the genomic analysis, the glycine betaine/L-proline ABC transporter system known as proU, which is an operon that encodes a high-affinity ABC transporter system consisting of three proteins (ProV, ProW and ProX; F451DRAFT_00884, F451DRAFT_00885, F451DRAFT_00886, respectively) is found in the strain. Further, the homologue of the TRAP transporter (F451DRAFT_00922) involved in transport of external ectoine and hydroxyectoine is found in M. rhizophilum . Function of the TRAP transporter is elucidated in both Halomonas elongata DSM 2581 [35] and Silicibacter pomeroyi DSS-3 [36]. Ectoine/5-hydroxyectoine-binding periplasmic protein in M. rhizophilum showed amino acids sequence similarity of 35.1% and 33.8% with those of H. elongata (TeaA) and S. pomeroyi (UehA), respectively. The transported ectoine is used as the sole carbon and nitrogen source in S. pomeroyi , but H. elongata can use it as a compatible solute. Considering that ectoine can be de novo produced in M. rhizophilum as well as actively transported from the environment, the role of the TRAP transporter in M. rhizophilum could be thought to recover endogenously synthesized ectoine that has leaked through the membrane as known in H. elongata [35].
Table 5

Enzymes and gene-loci participating in selected pathways identified in the draft genome of M. rhizophilum CL-YJ9T. Gene-loci are from the IMG/MER database

Pathways

Enzymes

Gene-loci

Glycine betaine biosynthesis

Choline dehydrogenase

F451DRAFT_01661

F451DRAFT_03441

F451DRAFT_04658

Betaine aldehyde dehydrogenase

F451DRAFT_00114

Ectoine and 5-hydroxyectoine biosynthesis

Aspartate kinase

F451DRAFT_00077

F451DRAFT_02577

Aspartate semialdehyde dehydrogenase

F451DRAFT_01139

F451DRAFT_01140

Diaminobutyrate aminotransferase apoenzyme

F451DRAFT_00080

Diaminobutyrate acetyltransferase

F451DRAFT_00081

Ectoine synthase

F451DRAFT_00079

Ectoine hydroxylase

F451DRAFT_00078

Molybdopterin biosynthesis

Cyclic pyranopterin monophosphate synthase

F451DRAFT_03412

F451DRAFT_01249

Molybdopterin synthase

F451DRAFT_04784

F451DRAFT_03411

F451DRAFT_01222

In the rhizosphere of tidal flat, oxygen tension varies in a wide range due to temperature change, repetitive exposure to atmosphere and seawater during tidal cycle and oxygen release from the roots of plants. Further, M. rhizophilum has a molybdopterin biosynthesis pathway (Table 5) and molybdoenzymes that use molydopterin as cofactor or prosthetic group such as formate dehydrogenase (F451DRAFT_01667, F451DRAFT_01668, F451DRAFT_01669, F451DRAFT_01665) and arsenate reductase (F451DRAFT_01068). ROS can be generated during the molybdopterin metabolism. Thus, defense mechanisms to ROS are required. Alteromonas sp. SN2, isolated from marine tidal flat, increased the number of oxidative stress tolerance genes to deal with ROS [37]. Similarly, many genes encoding ROS defense mechanisms are present in M. rhizophilum , including catalase-peroxidae (F451DRAFT_01727, F451DRAFT_04596), superoxide dismutase (F451DRAFT_03202), alkyl hydroperoxide reductase (F451DRAFT_02876, F451DRAFT_01413, F451DRAFT_00847), glutathione peroxidase (F451DRAFT_01603) and glutaredoxin (F451DRAFT_00578, F451DRAFT_01573, F451DRAFT_04005) as direct ROS scavengers. This line of data indicates a lifestyle of M. rhizophilum closely associated with the rhizosphere where substantial amounts of oxygen might be released from the roots of a well-adapted tidal-flat plant, Suaeda japonica . On the contrary, truncated bacterial hemoglobins (F451DRAFT_00578, F451DRAFT_01573, F451DRAFT_04005) involved in protection from oxidative stress and enhanced respiration under hypoxic conditions are present, indicating M. rhizophilum is adapted to the hypoxic rhizosphere in tidal-flat sediments, too.

The presence of motility by means of monopolar flagella was reported in a previous report [4]. Consistently, a number of genes encoding flagellar basal body proteins, flagellar hook-associated proteins and flagellar biosynthesis proteins are found in the genomic analyses, suggesting that M. rhizophilum could explore more favorable microenvironments using flagella in the rhizosphere. In contrast to a recent study that genes encoding steroid catabolism were identified in Marinobacterium stanieri S30 [38], most of these genes were not identified in the M. rhizophilum .

Conclusions

The genome of a representative of the genus Marinobacterium from the Proteobacteria phylum is reported here for the first time. In addition to detailed information on genome sequencing and annotation, genetic adaptation in environmental conditions closely associated with rhizosphere of a tidal flat plant such as salinity change and oxygen stress could be understood on the basis of genomic analyses.

Abbreviations

GEBA: 

Genomic Encyclopedia of Bacteria and Archaea

GOLD: 

Genomes OnLine Database

JGI: 

Joint Genome Institute

KMG: 

One thousand microbial genomes

ROS: 

Reactive oxygen species

TRAP: 

Tripartite ATP-independent periplasmic

Declarations

Acknowledgements

We acknowledge the technical assistance of Andrea Schütze and Evelyn Brambilla, both at DSMZ, in cultivation of DSM 18822T and subsequent DNA production, respectively.

Funding

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 (PE99513) of the Korea Institute of Ocean Science and Technology (KIOST) and by an East Asian Seas Time series-1 (EAST-1) funded by the Ministry of Oceans and Fisheries, Korea, and the BK21+ project of the Korean Government.

Authors’ contributions

DHC, GIJ and BCC drafted the manuscript. AL, AC, TBKR, SM, MH, NV, NI, MP, BJT and TW sequenced, assembled and annotated the genome. NCK, MG, HPK designed the KMG study and selected the strain for sequencing. All authors read and approved the final manuscript.

Competing interests

The authors declare that they have no competing interests. Authors Kyrpides and Klenk are editorial board members of the Standards in Genomic Sciences.

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Authors’ Affiliations

(1)
Marine Ecosystem and Biological Research Center, 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)
Centre for Algorithmic Biotechnology, St. Petersburg State University
(4)
Department of Cytology and Histology, St. Petersburg Academic University
(5)
Department of Energy Joint Genome Institute
(6)
Biological Data Management and Technology Center, Lawrence Berkeley National Laboratory
(7)
Leibniz Institute DSMZ – German Collection of Microorganisms and Cell Cultures
(8)
School of Biology, Newcastle University

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