Open Access

Complete genome sequence of Paludibacter propionicigenes type strain (WB4T)

  • Sabine Gronow1,
  • Christine Munk2, 3,
  • Alla Lapidus2,
  • Matt Nolan2,
  • Susan Lucas2,
  • Nancy Hammon2,
  • Shweta Deshpande2,
  • Jan-Fang Cheng2,
  • Roxane Tapia2, 3,
  • Cliff Han2, 3,
  • Lynne Goodwin2, 3,
  • Sam Pitluck2,
  • Konstantinos Liolios2,
  • Natalia Ivanova2,
  • Konstantinos Mavromatis2,
  • Natalia Mikhailova2,
  • Amrita Pati2,
  • Amy Chen4,
  • Krishna Palaniappan4,
  • Miriam Land2, 5,
  • Loren Hauser2, 5,
  • Yun-Juan Chang2, 5,
  • Cynthia D. Jeffries2, 5,
  • Evelyne Brambilla1,
  • Manfred Rohde6,
  • Markus Göker1,
  • John C. Detter2, 3,
  • Tanja Woyke2,
  • James Bristow2,
  • Jonathan A. Eisen2, 7,
  • Victor Markowitz4,
  • Philip Hugenholtz2, 8,
  • Nikos C. Kyrpides2 and
  • Hans-Peter Klenk1
Standards in Genomic Sciences20114:4010036

DOI: 10.4056/sigs.1503846

Published: 4 March 2011

Abstract

Paludibacter propionicigenes Ueki et al. 2006 is the type species of the genus Paludibacter, which belongs to the family Porphyromonadaceae. The species is of interest because of the position it occupies in the tree of life where it can be found in close proximity to members of the genus Dysgonomonas. This is the first completed genome sequence of a member of the genus Paludibacter and the third sequence from the family Porphyromonadaceae. The 3,685,504 bp long genome with its 3,054 protein-coding and 64 RNA genes consists of one circular chromosome and is a part of the Genomic Encyclopedia of Bacteria and Archaea project.

Keywords

strictly anaerobic nonmotile Gram-negative anoxic rice-field soil mesophilic chemoorganotrophic Porphyromonadaceae GEBA

Introduction

Strain WB4T (= DSM 17365 = CCUG 53888 = JCM 13257) is the type strain of P. propionicigenes, which is the type species of the genus Paludibacter [12]. Currently, there is only one species placed in the genus Paludibacter [1]. The generic name derives from the Latin noun palusudis meaning swamp or marsh and the Neo-Latin word bacter meaning a rod, referring to a rod living in swamps [2]. The species epithet is derived from the Neo-Latin word acidum propionicum meaning propionic acid and the Greek verb gennao meaning to produce, referring to the metabolic property of the species [2]. P. propionicigenes strain WB4T was isolated together with a number of other strains from rice plant residues in an anoxic rice-field soil in Yamagata, Japan, and described for the first time by Akasaka et al. in 2003 [3]. In 2006 the species was formally described by Ueki et al. and the genus Paludibacter was introduced [2]. No further isolates have been obtained for P. propionicigenes, however, cultivation-independent 16S rRNA-dependent molecular investigations showed the presence of P. propionicigenes in the rumen of sheep [4]. Here we present a summary classification and a set of features for P. propionicigenes WB4T, together with the description of the complete genomic sequencing and annotation.

Classification and features

A representative genomic 16S rRNA sequence of strain WB4T was compared using NCBI BLAST under default values (e.g., considering only the best 250 hits) with the most recent release of the Greengenes database [5] and the relative frequencies, of taxa and keywords (reduced to their stems [6]) were determined, weighted by BLAST scores. The most frequently occurring genus was Dysgonomonas (100%) (8 hits in total). Among all other species, the one yielding the highest score was Dysgonomonas capnocytophagoides, which corresponded to an identity of 91.9% and a HSP coverage of 83.6%. The highest-scoring environmental sequence was AY212569 (‘water 10 m downstream manure clone 118ds10’), which showed an identity of 99.6% and a HSP coverage of 100.1%. The five most frequent keywords within the labels of environmental samples which yielded hits were ‘digest’ (11.7%), ‘anaerob’ (6.2%), ‘sludge’ (6.1%), ‘wastewater’ (6.0%) and ‘mesophile’ (5.9%) (241 hits in total). The single most frequent keyword within the labels of environmental samples which yielded hits of a higher score than the highest scoring species was ‘downstream/manure/water’ (33.3%) (1 hit in total).

Figure 1 shows the phylogenetic neighborhood of P. propionicigenes WB4T in a 16S rRNA based tree. The three identical 16S rRNA sequences in the genome differ by one nucleotide from the previously published 16S rRNA sequence (AB078842).
Figure 1.

Phylogenetic tree highlighting the position of P. propionicigenes relative to the other type strains within the family Porphyromonadaceae. The tree was inferred from 1,400 aligned characters [78] of the 16S rRNA gene sequence under the maximum likelihood criterion [9] and rooted in accordance with the current taxonomy. The branches are scaled in terms of the expected number of substitutions per site. Numbers above branches are support values from 300 bootstrap replicates [10] if larger than 60%. Lineages with type strain genome sequencing projects registered in GOLD [11] are shown in blue, published genomes in bold [1213].

The cells of P. propionicigenes are generally rod-shaped (0.5–0.6 εm × 1.3–1.7 µm) with ends that are round or slightly tapered [2]. Elongated cells can also be seen, either as single cells or in short chains (Figure 2). P. propionicigenes is a Gram-negative and non spore-forming bacterium (Table 1). The organism is described to be nonmotile; only eight genes associated with motility were identified in the genome. The organism is strictly anaerobic and chemoorganotrophic [23]. The temperature range for growth is between 15°C and 35°C, with an optimum at 30°C [2]. The organism does not grow at 37°C [2]. The pH range for growth is 5.0–7.6 with an optimum at pH 6.6 [2]. NaCl concentrations from 0–0.5% (w/v) are tolerated. P. propionicigenes is able to utilize arabinose, glucose, fructose, xylose, cellobiose, galactose, mannose, maltose, melibiose, glycogen and soluble starch as growth substrates [2]. The organism does not utilize ribose, lactose, sucrose, melezitose, raffinose, sorbose, rhamnose, trehalose, cellulose, xylan, salicin, dulcitol, inositol, mannitol, sorbitol, ethanol, glycerol, fumarate, malate, lactate, succinate or pyruvate [2]. Glucose is fermented to propionate and acetate in a molar ratio of 2:1 as major products and succinate as a minor product [2]. The organism does not reduce nitrate, it does not hydrolyze gelatin or urea and does not produce indole or hydrogen sulfide [2]. P. propionicigenes does not grow in the presence of bile salts. Catalase and oxidase are not present in the organism [2].
Figure 2.

Scanning electron micrograph of P. propionicigenes WB4T

Table 1.

Classification and general features of P. propionicigenes WB4T according to the MIGS recommendations [14].

MIGS ID

Property

Term

Evidence code

 

Current classification

Domain Bacteria

TAS [15]

 

Phylum Bacteroidetes

TAS [16]

 

Class Bacteroidia

TAS [16,17]

 

Order Bacteroidales

TAS [16]

 

Family Porphyromonadaceae

TAS [16]

 

Genus Paludibacter

TAS [2]

 

Species Paludibacter propionicigenes

TAS [2]

 

Type strain WB4

TAS [2]

 

Gram stain

negative

TAS [3]

 

Cell shape

rod-shaped

TAS [3]

 

Motility

non-motile

TAS [2]

 

Sporulation

none

TAS [3]

 

Temperature range

15°C to 35°C

TAS [3]

 

Optimum temperature

30°C

TAS [2]

 

Salinity

normal

NAS

MIGS-22

Oxygen requirement

strictly anaerobic

TAS [3]

 

Carbon source

carbohydrates

TAS [3]

 

Energy source

chemoorganotroph

TAS [3]

MIGS-6

Habitat

soil

TAS [3]

MIGS-15

Biotic relationship

free-living

NAS

MIGS-14

Pathogenicity

none

NAS

 

Biosafety level

1

TAS [18]

 

Isolation

rice plant residue in anoxic rice-field soil

TAS [3]

MIGS-4

Geographic location

Yamagata, Japan

TAS [3]

MIGS-5

Sample collection time

1994

TAS [3]

MIGS-4.1

Latitude

38.25

NAS

MIGS-4.2

Longitude

140.34

NAS

MIGS-4.3

Depth

not reported

 

MIGS-4.4

Altitude

not reported

 

Evidence codes - IDA: Inferred from Direct Assay (first time in publication); 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 of the Gene Ontology project [19]. If the evidence code is IDA, then the property was directly observed by one of the authors or an expert mentioned in the acknowledgements.

Chemotaxonomy

Little chemotaxonomic data are available for strain WB4T. Only the fatty acid composition has been elucidated. The major fatty acids found were anteiso-C15:0 (30.8%), C15:0 (19.0%) and 3-hydroxy anteiso-C17:0 (17.9%) [2]. Also, iso-C17:0 3-OH (6.2%) and C16:0 (4.9%) were detected in intermediate amounts whereas iso-C15:0 3-OH, iso-C16:0 3-OH, C15:0 3-OH, C16:03-OH, iso-C15:0, C14:0, C16:0, and C18:0 were present in minor amounts (1% to 5% of the total fatty acids). Unsaturated fatty acids were not detected [2].

Genome sequencing and annotation

Genome project history

This organism was selected for sequencing on the basis of its phylogenetic position [20], and is part of the Genomic Encyclopedia of Bacteria and Archaea project [21]. The genome project is deposited in the Genomes OnLine Database [11] and the complete genome sequence is deposited in GenBank. Sequencing, finishing and annotation were performed by the DOE Joint Genome Institute (JGI). A summary of the project information is shown in Table 2.
Table 2.

Genome sequencing project information

MIGS ID

Property

Term

MIGS-31

Finishing quality

Finished

MIGS-28

Libraries used

Three genomic libraries: one 454 pyrosequence standard library, one 454 PE library (9 kb insert size), one Illumina library

MIGS-29

Sequencing platforms

Illumina GAii, 454 GS FLX Titanium

MIGS-31.2

Sequencing coverage

337.6 × Illumina; 28.1 × pyrosequence

MIGS-30

Assemblers

Newbler version 2 2.3-PreRelease-10-21-2009-gcc-4.1.2-threads, Velvet, phrap

MIGS-32

Gene calling method

Prodigal 1.4, GenePRIMP

 

INSDC ID

CP002345

 

Genbank Date of Release

December 2, 2010

 

GOLD ID

Gc01549

 

NCBI project ID

694427

 

Database: IMG-GEBA

2503538024

MIGS-13

Source material identifier

DSM 17365

 

Project relevance

Tree of Life, GEBA

Growth conditions and DNA isolation

P. propionicigenes WB4T, DSM 17365, was grown anaerobically in DSMZ medium 104 [22] at 30°C. DNA was isolated from 0.5–1 g of cell paste using a MasterPure Gram-positive DNA purification kit (Epicentre MGP04100) following the standard protocol as recommended by the manufacturer, with modification st/DL for cell lysis as described in Wu et al. [21].

Genome sequencing and assembly

The genome was sequenced using a combination of Illumina and 454 sequencing platforms. All general aspects of library construction and sequencing can be found at the JGI website [23]. Pyrosequencing reads were assembled using the Newbler assembler version 2.3-PreRelease-10-21-2009-gcc-4.1.2-threads (Roche). The initial Newbler assembly consisting of 26 contigs in one scaffold which was converted into a phrap assembly by [24] making fake reads from the consensus, to collect the read pairs in the 454 paired end library. Illumina GAii sequencing data (967 Mb) was assembled with Velvet [25] and the consensus sequences were shredded into 1.5 kb overlapped fake reads and assembled together with the 454 data. The 454 draft assembly was based on 93.4 Mb 454 draft data and all of the 454 paired end data. Newbler parameters are -consed -a 50 -l 350 -g -m -ml 20. The Phred/Phrap/Consed software package was used for sequence assembly and quality assessment in the subsequent finishing process. After the shotgun stage, reads were assembled with parallel phrap (High Performance Software, LLC). Possible mis-assemblies were corrected with gapResolution [23], Dupfinisher, or sequencing cloned bridging PCR fragments with subcloning or transposon bombing (Epicentre Biotechnologies, Madison, WI) [26]. Gaps between contigs were closed by editing in Consed, by PCR and by Bubble PCR primer walks (J.-F.Chang, unpublished). A total of 124 additional reactions and one shatter library were necessary to close the gaps and to raise the quality of the finished sequence. Illumina reads were also used to correct potential base errors and increase consensus quality using a software Polisher developed at JGI [27]. The error rate of the completed genome sequence is less than 1 in 100,000. Together, the combination of the Illumina and 454 sequencing platforms provided 365.7 × coverage of the genome. The final assembly contained 333,397 pyrosequence and 34,564,373 Illumina reads.

Genome annotation

Genes were identified using Prodigal [28] as part of the Oak Ridge National Laboratory genome annotation pipeline, followed by a round of manual curation using the JGI GenePRIMP pipeline [29]. The predicted CDSs were translated and used to search the National Center for Biotechnology Information (NCBI) nonredundant database, UniProt, TIGR-Fam, Pfam, PRIAM, KEGG, COG, and InterPro databases. Additional gene prediction analysis and functional annotation was performed within the Integrated Microbial Genomes - Expert Review (IMG-ER) platform [30].

Genome properties

The genome consists of a 3,685,504 bp long chromosome with a GC content of 38.9% (Table 3 and Figure 3). Of the 3,118 genes predicted, 3,054 were protein-coding genes, and 64 RNAs; 34 pseudogenes were also identified. The majority of the protein-coding genes (65.8%) were assigned with a putative function while the remaining ones were annotated as hypothetical proteins. The distribution of genes into COGs functional categories is presented in Table 4.
Figure 3.

Graphical circular map of the chromosome. From outside to the center: Genes on forward strand (color by COG categories), Genes on reverse strand (color by COG categories), RNA genes (tRNAs green, rRNAs red, other RNAs black), GC content, GC skew.

Table 3.

Genome Statistics

Attribute

Value

% of Total

Genome size (bp)

3,685,504

100.00%

DNA coding region (bp)

3,225,817

87.53%

DNA G+C content (bp)

1,432,064

38.86%

Number of replicons

1

 

Extrachromosomal elements

0

 

Total genes

3,118

100.00%

RNA genes

64

2.05%

rRNA operons

3

 

Protein-coding genes

3,054

97.95%

Pseudo genes

34

1.09%

Genes with function prediction

2,051

65.78%

Genes in paralog clusters

325

10.42%

Genes assigned to COGs

2,005

64.30%

Genes assigned Pfam domains

2,205

70.72%

Genes with signal peptides

843

27.04%

Genes with transmembrane helices

784

25.14%

CRISPR repeats

2

 
Table 4.

Number of genes associated with the general COG functional categories

Code

value

%age

Description

J

149

6.8

Translation, ribosomal structure and biogenesis

A

0

0

RNA processing and modification

K

136

6.2

Transcription

L

101

4.6

Replication, recombination and repair

B

0

0

Chromatin structure and dynamics

D

22

1.0

Cell cycle control, cell division, chromosome partitioning

Y

0

0

Nuclear structure

V

48

2.2

Defense mechanisms

T

99

4.5

Signal transduction mechanisms

M

232

10.6

Cell wall/membrane/envelope biogenesis

N

8

0.4

Cell motility

Z

0

0

Cytoskeleton

W

0

0

Extracellular structures

U

40

1.8

Intracellular trafficking, secretion, and vesicular transport

O

80

3.7

Posttranslational modification, protein turnover, chaperones

C

108

5.0

Energy production and conversion

G

172

7.9

Carbohydrate transport and metabolism

E

166

7.6

Amino acid transport and metabolism

F

61

2.8

Nucleotide transport and metabolism

H

128

5.9

Coenzyme transport and metabolism

I

67

3.1

Lipid transport and metabolism

P

131

6.0

Inorganic ion transport and metabolism

Q

24

1.1

Secondary metabolites biosynthesis, transport and catabolism

R

256

11.7

General function prediction only

S

153

7.0

Function unknown

-

1,113

35.7

Not in COGs

Declarations

Acknowledgements

We would like to gratefully acknowledge the help of Sabine Welnitz (DSMZ) for growing P. propionicigenes cultures. This work was performed under the auspices of the US Department of Energy Office of Science, Biological and Environmental Research Program, and by the University of California, Lawrence Berkeley National Laboratory under contract No. DE-AC02-05CH11231, Lawrence Livermore National Laboratory under Contract No. DE-AC52-07NA27344, and Los Alamos National Laboratory under contract No. DE-AC02-06NA25396, UT-Battelle and Oak Ridge National Laboratory under contract DE-AC05-00OR22725, as well as German Research Foundation (DFG) INST 599/1-2.

Authors’ Affiliations

(1)
DSMZ - German Collection of Microorganisms and Cell Cultures GmbH
(2)
DOE Joint Genome Institute
(3)
Bioscience Division, Los Alamos National Laboratory
(4)
Biological Data Management and Technology Center, Lawrence Berkeley National Laboratory
(5)
Oak Ridge National Laboratory
(6)
HZI - Helmholtz Centre for Infection Research
(7)
University of California Davis Genome Center
(8)
Australian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences, The University of Queensland

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Copyright

© The Author(s) 2011