Open Access

High-quality permanent draft genome sequence of the Parapiptadenia rigida-nodulating Cupriavidus sp. strain UYPR2.512

  • Sofie E De Meyer1,
  • Elena Fabiano2,
  • Rui Tian1,
  • Peter Van Berkum3,
  • Rekha Seshadri4,
  • TBK Reddy4,
  • Victor Markowitz5,
  • Natalia N Ivanova4,
  • Amrita Pati4,
  • Tanja Woyke4,
  • John Howieson1,
  • Nikos C Kyrpides4, 6 and
  • Wayne Reeve1Email author
Standards in Genomic Sciences201510:13

https://doi.org/10.1186/1944-3277-10-13

Received: 26 November 2014

Accepted: 5 December 2014

Published: 11 April 2015

Abstract

Cupriavidus sp. strain UYPR2.512 is an aerobic, motile, Gram-negative, non-spore-forming rod that was isolated from a root nodule of Parapiptadenia rigida grown in soils from a native forest of Uruguay. Here we describe the features of Cupriavidus sp. strain UYPR2.512, together with sequence and annotation. The 7,858,949 bp high-quality permanent draft genome is arranged in 365 scaffolds of 369 contigs, contains 7,411 protein-coding genes and 76 RNA-only encoding genes, and is part of the GEBA-RNB project proposal.

Keywords

Root-nodule bacteria Nitrogen fixation Rhizobia Betaproteobacteria GEBA-RNB

Introduction

Legumes establish symbiotic associations with a group of soil bacteria, rhizobia, able to fix atmospheric nitrogen (N2). Rhizobia elicit the formation of a symbiotic organ called a nodule comprising differentiated plant and bacterial cells. Differentiated rhizobia within nodules are termed bacteroids, and acquire the ability to fix nitrogen. Rhizobia are phylogenetically diverse including genera from the Alphaproteobacteria (Allorhizobium, Azorhizobium, Bradyrhizobium, Ensifer, Mesorhizobium, Rhizobium, etc.) as well as from the Betaproteobacteria (Burkholderia, Cupriavidus) [1, 2].

The biological nitrogen fixation process significantly contributes to the development of sustainable agriculture reducing the use of supplies dependent on fuel and alleviating environmental impacts produced by the addition of chemical fertilizer [3]. Moreover, forestation with leguminous trees associated with rhizobia, “nitrogen-fixing trees”, has been successfully used for recovering degraded soils [4].

Parapiptadenia rigida (Benth.) Brenan, is a “nitrogen-fixing tree” belonging to the Piptadenia group from the Mimosoideae subfamily [5]. It is a multipurpose tree, very appreciated because of its timber and therefore used in high quality furniture and construction. It is also used for gums, tannins and essential oil extraction, has medicinal properties and is included in agroforestry and reforestation programs [4, 6, 7]. Taulé et al.[8] demonstrated that this species could be nodulated either by Alpha-rhizobia (Rhizobium) or by Beta-rhizobia (Burkholderia and Cupriavidus) with Burkholderia being the preferred natural symbiont of this legume. In the case of Cupriavidus sp. UYPR2.512, this strain was isolated from a nodule of a P. rigida plant grown in soils collected from Mandiyú native forest in Artigas, Uruguay. Isolated bacterial colonies of Cupriavidus sp. UYPR2.512 were able to nodulate and to promote the growth of P. rigida, as well as Mimosa pudica plants [8].

To our knowledge, the only published sequenced genome of a Beta-rhizobia belonging to the Cupriavidus genus so far is that of C. taiwanensis LMG 19424T[9]. Interestingly, the closest relative of Cupriavidus sp. UYPR2.512 is C. necator ATCC 43291T[8]. Here, we present the description of the Cupriavidus sp. UYPR2.512 high-quality permanent draft genome sequence and its annotation.

Organism information

Classification and features

Cupriavidus sp. strain UYPR2.512 is a motile, Gram-negative, non-spore-forming rod (Figure 1 Left, Center) in the order Burkholderiales of the class Betaproteobacteria. The rod-shaped form varies in size with dimensions of 0.5-0.7 μm in width and 0.9-1.2 μm in length (Figure 1 Left). It is fast growing, forming 0.5-0.8 mm diameter colonies after 24 h when grown on TY [10] at 28°C. Colonies on TY are white-opaque, slightly domed, moderately mucoid with smooth margins (Figure 1 Right).
Figure 1

Images of Cupriavidus sp. strain UYPR2.512 using scanning (Left) and transmission (Center) electron microscopy and the appearance of colony morphology on solid media (Right).

Figure 2 shows the phylogenetic relationship of Cupriavidus sp. strain UYPR2.512 in a 16S rRNA gene sequence based tree. This strain is the most similar to Cupriavidus necator ATCC 43291T, Cupriavidus oxalaticus DSM 1105T and Cupriavidus taiwanensis LMG 19424T based on the 16S rRNA gene alignment with sequence identities of 99.32%, 98.49% and 98.42%, respectively, as determined using the EzTaxon-e server [11]. Cupriavidus necator ATCC 43291T has been isolated from soil and is a non-obligate predator causing lysis of various Gram-positive and Gram-negative bacteria in the soil [12]. Cupriavidus taiwanensis LMG 19424T is a plant symbiont and was isolated from root nodules of Mimosa pudica collected from three fields at Ping-Tung Country in the southern part of Taiwan [1]. Minimum Information about the Genome Sequence (MIGS) is provided in Table 1 and Additional file 1: Table S1.
Figure 2

Phylogenetic tree highlighting the position of Cupriavidus sp. strain UYPR2.512 (shown in blue print) relative to other type and non-type strains in the Cupriavidus genus using a 1,034 bp internal region of the 16S rRNA gene. Several Alpha-rhizobia sequences were used as an outgroup. All sites were informative and there were no gap-containing sites. Phylogenetic analyses were performed using MEGA, version 5.05 [13]. The tree was built using the maximum likelihood method with the General Time Reversible model. Bootstrap analysis with 500 replicates was performed to assess the support of the clusters. Type strains are indicated with a superscript T. Strains with a genome sequencing project registered in GOLD [14] are shown in bold and have the GOLD ID mentioned after the strain number, otherwise the NCBI accession number has been provided. Finished genomes are designated with an asterisk.

Table 1

Classification and general features of Cupriavidus sp. strain UYPR2.512 in accordance with the MIGS recommendations [15] published by the Genome Standards Consortium [16]

MIGS ID

Property

Term

Evidence code

 

Current classification

Domain Bacteria

TAS [17]

Phylum Proteobacteria

TAS [18, 19]

Class Betaproteobacteria

TAS [20]

Order Burkholderiales

TAS [21]

Family Burkholderiaceae

TAS [22]

Genus Cupriavidus

TAS [23]

Species Cupriavidus sp.

IDA

 

Gram stain

Negative

IDA [23]

 

Cell shape

Rod

IDA

 

Motility

Motile

IDA

 

Sporulation

Non-sporulating

IDA [23]

 

Temperature range

mesophile

IDA [23]

 

Optimum temperature

28°C

IDA

 

pH range; Optimum

Not reported

 
 

Carbon source

Not reported

 

MIGS-6

Habitat

Soil, root nodule on host

IDA

MIGS-6.3

Salinity

Not reported

 

MIGS-22

Oxygen requirement

aerobic

IDA

MIGS-15

Biotic relationship

Symbiotic

IDA

MIGS-14

Pathogenicity

Non-pathogenic

NAS

MIGS-4

Geographic location

Uruguay

IDA

MIGS-5

Nodule collection date

2006

IDA

MIGS-4.1

Latitude

-30.507

IDA

MIGS-4.2

Longitude

-57.71

IDA

MIGS-4.4

Altitude

58 m

IDA

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 [24].

Symbiotaxonomy

Cupriavidus sp. strain UYPR2.512 was isolated from Parapiptadenia rigida, a Mimosoideae legume native to Uruguay [8]. This tree is native to South America, including south Brazil, Argentina, Paraguay, and Uruguay, and used by locals for timber and as a source of gums, tannins and essential oils [8]. Cupriavidus sp. strain UYPR2.512 is able to renodulate its original host and is highly efficient in fixing nitrogen with this host [8]. A selection of other host plants, including Trifolium repens, Medicago sativa, Peltophorum dubium and Mimosa pudica were tested for their ability to nodulate with UYPR2.512. Of these plants, strain UYPR2.512 was only able to nodulate and fix nitrogen effectively with M. pudica[8].

Genome sequencing information

Genome project history

This organism was selected for sequencing on the basis of its environmental and agricultural relevance to issues in global carbon cycling, alternative energy production, and biogeochemical importance, and is part of the Genomic Encyclopedia of Bacteria and Archaea, The Root Nodulating Bacteria chapter (GEBA-RNB) project at the U.S. Department of Energy, Joint Genome Institute [25]. The genome project is deposited in the Genomes OnLine Database [14] and the high-quality permanent draft genome sequence in IMG [26]. Sequencing, finishing and annotation were performed by the JGI using state of the art sequencing technology [27]. A summary of the project information is shown in Table 2.
Table 2

Genome sequencing project information for Cupriavidus sp. strain UYPR2.512

MIGS ID

Property

Term

MIGS-31

Finishing quality

Permanent-draft

MIGS-28

Libraries used

Illumina Std PE

MIGS-29

Sequencing platforms

Illumina HiSeq 2000

MIGS-31.2

Fold coverage

106.8 X Illumina

MIGS-30

Assemblers

Velvet 1.1.04, ALLPATHS-LG V.r41043

MIGS-32

Gene calling methods

Prodigal 1.4

 

Locus Tag

A3A5

 

Genbank ID

ARBE00000000

 

Genbank Date of Release

September 16, 2013

 

GOLD ID

Gp0009663 [28]

 

BIOPROJECT

PRJNA165301

MIGS-13

Source Material Identifier

UYPR2.512

 

Project relevance

Symbiotic N2fixation, agriculture

Growth conditions and DNA isolation

Cupriavidus sp. strain UYPR2.512 was grown to mid logarithmic phase in TY rich media [10] on a gyratory shaker at 28°C. DNA was isolated from 60 mL of cells using a CTAB (Cetyl trimethyl ammonium bromide) bacterial genomic DNA isolation method [29].

Genome sequencing and assembly

The draft genome of Cupriavidus sp. UYPR2.512 was generated at the DOE Joint Genome Institute [27]. An Illumina Std shotgun library was constructed and sequenced using the Illumina HiSeq 2000 platform which generated 29,312,424 reads totaling 4,396.9 Mbp [30]. All general aspects of library construction and sequencing performed at the JGI can be found at the JGI web site [31]. 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. unpublished). Artifact filtered sequence data was then screened and trimmed according to the k–mers present in the dataset. 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 (>30x average k–mer depth) were normalized to an average depth of 30x. Reads with an average kmer depth of less than 2x were removed. Following steps were then performed for assembly: (1) normalized Illumina reads were assembled using Velvet version 1.1.04 [32] (2) 1–3 Kbp simulated paired end reads were created from Velvet contigs using wgsim [33] (3) normalized Illumina reads were assembled with simulated read pairs using Allpaths–LG (version r41043)[34]. 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 369 contigs in 365 scaffolds. The total size of the genome is 7.9 Mbp and the final assembly is based on 839.6 Mbp of Illumina data, which provides an average of 106.8x coverage.

Genome annotation

Genes were identified using Prodigal [35], as part of the DOE-JGI genome annotation pipeline [36, 37] followed by a round of manual curation using GenePRIMP [38] for finished genomes and Draft genomes in fewer than 10 scaffolds. The predicted CDSs were translated and used to search the National Center for Biotechnology Information (NCBI) non-redundant database, UniProt, TIGRFam, Pfam, KEGG, COG, and InterPro databases. The tRNAScanSE tool [39] was used to find tRNA genes, whereas ribosomal RNA genes were found by searches against models of the ribosomal RNA genes built from SILVA [40]. Other non–coding RNAs such as the RNA components of the protein secretion complex and the RNase P were identified by searching the genome for the corresponding Rfam profiles using INFERNAL [41]. Additional gene prediction analysis and manual functional annotation was performed within the Integrated Microbial Genomes-Expert Review (IMG-ER) system [42] developed by the Joint Genome Institute, Walnut Creek, CA, USA.

Genome properties

The genome is 7,858,949 nucleotides with 65.25% GC content (Table 3) and comprised of 365 scaffolds and 369 contigs (Figure 3). From a total of 7,487 genes, 7,411 were protein encoding and 76 RNA only encoding genes. The majority of genes (75.64%) were assigned a putative function whilst the remaining genes were annotated as hypothetical. The distribution of genes into COG functional categories is presented in Table 4.
Table 3

Genome statistics for Cupriavidus sp. strain UYPR2.512

Attribute

Value

% of total

Genome size (bp)

7,858,949

100

DNA coding (bp)

6,709,332

85.37

DNA G + C (bp)

5,128,158

65.25

DNA scaffolds

365

 

Total genes

7,487

100

Protein coding genes

7,411

98.98

RNA genes

76

1.02

Pseudo genes

0

0

Genes in internal clusters

419

5.6

Genes with function prediction

5,663

75.64

Genes assigned to COGs

4,807

64.20

Genes with Pfam domains

5,959

79.59

Genes with signal peptides

696

9.30

Genes with transmembrane helices

1,545

20.64

CRISPR repeats

1

 
Figure 3

Graphical map of the four largest scaffolds of the genome of Cupriavidus sp. strain UYPR2.512. From the bottom to the top of each scaffold: Genes on forward strand (color by COG categories as denoted by the IMG platform), Genes on reverse strand (color by COG categories), RNA genes (tRNAs green, sRNAs red, other RNAs black), GC content, GC skew.

Table 4

Number of protein coding genes of Cupriavidus sp. strain UYPR2.512 associated with the general COG functional categories

Code

Value

% of total (5,426)

COG Category

J

183

3.37

Translation, ribosomal structure and biogenesis

A

1

0.02

RNA processing and modification

K

526

9.69

Transcription

L

192

3.54

Replication, recombination and repair

B

3

0.06

Chromatin structure and dynamics

D

35

0.65

Cell cycle control, Cell division, chromosome partitioning

Y

0

0.00

Nuclear structure

V

56

1.03

Defense mechanisms

T

210

3.87

Signal transduction mechanisms

M

277

5.11

Cell wall/membrane/envelope biogenesis

N

99

1.82

Cell motility

Z

0

0.00

Cytoskeleton

W

0

0.00

Extracellular structures

U

140

2.58

Intracellular trafficking, secretion, and vesicular transport

O

181

3.34

Posttranslational modification, protein turnover, chaperones

C

434

8.00

Energy production and conversion

G

268

4.94

Carbohydrate transport and metabolism

E

487

8.98

Amino acid transport and metabolism

F

89

1.64

Nucleotide transport and metabolism

H

194

3.58

Coenzyme transport and metabolism

I

337

6.21

Lipid transport and metabolism

P

272

5.01

Inorganic ion transport and metabolism

Q

236

4.35

Secondary metabolite biosynthesis, transport and catabolism

R

661

12.18

General function prediction only

S

545

10.04

Function unknown

-

2680

35.80

Not in COGS

Conclusion

Cupriavidus sp. UYPR2.512 belongs to a group of Beta-rhizobia isolated from Parapiptadenia rigida, a native tree from Uruguay belonging to the Mimosoideae legume group [8]. This tree is also native to the south of Brazil, Argentina and Paraguay [8]. Greenhouse experiments from previous studies have shown that Cupriavidus sp. UYPR2.512 is also able to nodulate and fix nitrogen with Mimosa pudica, an invasive species in many regions around the world [8]. Phylogenetic analysis revealed that UYPR2.512 is the most closely related to Cupriavidus necator ATCC 43291T, Cupriavidus oxalaticus DSM 1105T and Cupriavidus taiwanensis LMG 19424T . In contrast to the other two strains, Cupriavidus taiwanensis LMG 19424T is a microsymbiont that is able to nodulate and fix nitrogen in association with Mimosa species [43]. In total five Cupriavidus strains (AMP6, LMG 19424T, STM6018, STM6070 and UYPR2.512), which can form a symbiotic association have now been sequenced. A comparison of these strains reveals that UYPR2.512 has the largest genome (7.9 Mbp), with the highest KOG count (1398), the lowest G + C (65.25%) and signal peptide (9.3%) percentages in this group. All of these genomes share the nitrogenase-RXN MetaCyc pathway catalyzed by a multiprotein nitrogenase complex. Out of five Cupriavidus strains (AMP6, LMG 19424T, STM6018, STM6070 and UYPR2.512), which contain the N-fixation pathway, only Cupriavidus sp. UYPR2.512 has been shown to nodulate and fix effectively with Parapiptadenia rigida. The genome attributes of Cupriavidus sp. UYPR2.512 will therefore be important for ongoing molecular analysis of the plant microbe interactions required for the establishment of leguminous tree symbioses with this host.

Declarations

Acknowledgements

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, Lawrence Livermore National Laboratory under Contract No. DE-AC52-07NA27344, and Los Alamos National Laboratory under contract No. DE-AC02-06NA25396.

Authors’ Affiliations

(1)
Centre for Rhizobium Studies, Murdoch University
(2)
Instituto de Investigaciones Biológicas Clemente Estable
(3)
Soybean Genomics and improvement laboratory Bldg 006, BARC-West USDA ARS
(4)
DOE Joint Genome Institute
(5)
Biological Data Management and Technology Center, Lawrence Berkeley National Laboratory
(6)
Department of Biological Sciences, King Abdulaziz University

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