Open Access

High-quality permanent draft genome sequence of the Parapiptadenia rigida-nodulating Burkholderia sp. strain UYPR1.413

  • Sofie E. De Meyer1,
  • Elena Fabiano2,
  • Rui Tian1,
  • Peter Van Berkum3,
  • Rekha Seshadri4,
  • TBK Reddy4,
  • Victor Markowitz5,
  • Natalia Ivanova4,
  • Amrita Pati4,
  • Tanja Woyke4,
  • John Howieson1,
  • Nikos Kyrpides4, 6 and
  • Wayne Reeve1Email author
Standards in Genomic Sciences201510:31

DOI: 10.1186/s40793-015-0018-9

Received: 19 November 2014

Accepted: 13 May 2015

Published: 4 June 2015

Abstract

Burkholderia sp. strain UYPR1.413 is an aerobic, motile, Gram-negative, non-spore-forming rod that was isolated from a root nodule of Parapiptadenia rigida collected at the Angico plantation, Mandiyu, Uruguay, in December 2006. A survey of symbionts of P. rigida in Uruguay demonstrated that this species is nodulated predominantly by Burkholderia microsymbionts. Moreover, Burkholderia sp. strain UYPR1.413 is a highly efficient nitrogen fixing symbiont with this host. Currently, the only other sequenced isolate to fix with this host is Cupriavidus sp. UYPR2.512. Therefore, Burkholderia sp. strain UYPR1.413 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 GEBA-RNB project. Here we describe the features of Burkholderia sp. strain UYPR1.413, together with sequence and annotation. The 10,373,764 bp high-quality permanent draft genome is arranged in 336 scaffolds of 342 contigs, contains 9759 protein-coding genes and 77 RNA-only encoding genes.

Keywords

Root-nodule bacteria Nitrogen fixation Rhizobia Betaproteobacteria GEBA-RNB

Introduction

Rhizobia are soil bacteria that have acquired the ability to establish symbiotic associations with plants, mainly from the Fabaceae family, and carry out the Biological Nitrogen Fixation (BNF) process. BNF is catalyzed by the rhizobial nitrogenase complex, whereby N2 is reduced to ammonium.

Well-known and studied rhizobia are those belonging to the α-proteobacteria (eg. Azorhizobium , Bradyrhizobium , Ensifer , Mesorhizobium and Rhizobium ). In 2001 symbiotic nitrogen fixing bacteria belonging to the group of Betaproteobacteria were reported as root nodule bacteria, introducing the term of Alpha and Beta-rhizobia to differentiate both groups of rhizobia [1, 2]. The Beta-rhizobia identified so far belong to only two genera: Burkholderia and Cupriavidus and the association seem to be mainly with plants from the Mimosoideae subfamily [3]. Additionally, studies indicate that the South American Mimosa genus is preferentially nodulated by Beta-rhizobia [4]. Different Beta-rhizobia species have been described belonging to the Burkholderia genus (eg. B. caballeronis , B. caribensis , B. diazotrophica , B. dilworthii , B. mimosarum , B. nodosa , B. phymatum , B. rhynchosiae , B. sabiae , B. sprentiae , B. symbiotica and B. tuberum ) but only two in the Cupriavidus genus ( C. taiwanensis and C. necator ) [2, 517].

Burkholderia sp. UYPR1.413 strain has been isolated from a root nodule of Parapiptadenia rigida (Benth.) Brenan found in an angico plantation in Artigas, Uruguay [18]. P. rigida belongs to the Mimosoideae subfamily and is a woody species, which can reach 30 m in height and a diameter of 60 to 80 cm [19]. The wood is of excellent quality, heavy, elastic, very hard and quite durable, rich in tannins and has medicinal properties [20]. There are six different species of Parapiptadenia in the Americas of which only P. rigida is present in Uruguay. A survey of symbionts of P. rigida in Uruguay demonstrated that this species is nodulated by rhizobia belonging to the genera Burkholderia , Cupriavidus and Rhizobium , of which the Burkholderia microsymbionts predominated [18]. Burkholderia sp. UYPR1.413 strain belongs to a group of microsymbionts that were able to nodulate and fix nitrogen with P. rigida [18]. In this work we present the description of the Burkholderia sp. UYPR1.413 high-quality permanent draft genome sequence and its annotation.

Organism information

Classification and features

Burkholderia sp. strain UYPR1.413 is a motile, Gram-negative, non-spore-forming rod (Fig. 1 Left, Center) in the order Burkholderiales of the class Betaproteobacteria . The rod-shaped form varies in size with dimensions of 0.3–0.5 μm in width and 1.0–2.0 μm in length (Fig. 1 Left). It is fast growing, forming 0.5–1 mm diameter colonies after 24 h when grown on TY [21] at 28 °C. Colonies on TY are white-opaque, slightly domed, moderately mucoid with smooth margins (Fig. 1 Right).
Fig. 1

Images of Burkholderia sp. strain UYPR1.413 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 Burkholderia sp. strain UYPR1.413 in a 16S rRNA gene sequence based tree. This strain is phylogenetically most related to Burkholderia sabiae Br3407T, Burkholderia caribensis MWAP64T and Burkholderia phymatum STM815T with sequence identities to UYPR1.413 16S rRNA gene sequence of 98.96, 98.64 and 98.56 %, respectively, as determined using the EzTaxon-e server [22]. Burkholderia sabiae Br3407T was first isolated from root nodules of Mimosa caesalpiniifolia , a native tree to Brazil [6]. Burkholderia caribensis MWAP64T was first isolated from vertisol in Martinique [5] and related strains have been identified as a plant growth promoting bacteria for grain Amaranth and Mango trees [23, 24] and nitrogen fixing root nodule bacteria for several Mimosa species [25, 26]. Burkholderia phymatum STM815T is also known to nodulate effectively with several Mimosa species [27]. Minimum Information about the Genome Sequence (MIGS) [28] is provided in Table 1.
Fig. 2

Phylogenetic tree highlighting the position of Burkholderia sp. strain UYPR1.413 (shown in blue print) relative to other type and non-type strains in the Burkholderia genus using 1046 bp internal region of the 16S rRNA gene. Several Alpha-rhizobia sequences were used as outgroup. All sites were informative and there were no gap-containing sites. Phylogenetic analyses were performed using MEGA, version 5.05 [47]. 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 [30] have the GOLD ID provided after the strain number. Finished genomes are designated with an asterisk

Table 1

Classification and general features of Burkholderia sp. strain UYPR1.413 in accordance with the MIGS recommendations [28] published by the Genome Standards Consortium [48]

MIGS ID

Property

Term

Evidence code

 

Classification

Domain Bacteria

TAS [49]

Phylum Proteobacteria

TAS [50, 51]

Class Betaproteobacteria

TAS [52]

Order Burkholderiales

TAS [53]

Family Burkholderiaceae

TAS [54]

Genus Burkholderia

TAS [55]

Species Burkholderia sp.

IDA

(Type) strain UYPR1.413

IDA

 

Gram stain

Negative

TAS [55]

 

Cell shape

Rod

IDA

 

Motility

Motile

IDA

 

Sporulation

non-sporulating

TAS [55]

 

Temperature range

Not reported

 
 

Optimum temperature

28 °C

IDA

 

pH range; Optimum

Not reported

 
 

Carbon source

Not reported

 

MIGS-6

Habitat

Soil, root nodule on host

TAS [18]

MIGS-6.3

Salinity

Not reported

 

MIGS-22

Oxygen requirement

Aerobic

IDA

MIGS-15

Biotic relationship

Symbiotic

TAS [18]

MIGS-14

Pathogenicity

Non-pathogenic

NAS

MIGS-4

Geographic location

Uruguay

TAS [18]

MIGS-5

Sample collection

December, 2006

TAS [18]

MIGS-4.1

Latitude

−30.507

TAS [18]

MIGS-4.2

Longitude

−57.702

TAS [18]

MIGS-4.4

Altitude

76 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 [56]

Symbiotaxonomy

Burkholderia sp. strain UYPR1.413 was isolated from Parapiptadenia rigida , a Mimosoideae legume native to Uruguay [18]. 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 [18]. Burkholderia sp. strain UYPR1.413 is able to renodulate its original host and is highly efficient in fixing nitrogen with this host [18]. A selection of host plants, including Trifolium repens , Medicago sativa , Peltophorum dubium and Mimosa pudica were investigated previously for their ability to nodulate with UYPR1.413 and only M. pudica plants were nodulated by UYPR1.413, albeit ineffectively [18].

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 (JGI) for projects of relevance to agency missions [29]. The genome project is deposited in the Genomes OnLine Database [30] and the high-quality permanent draft genome sequence in IMG [31]. Sequencing, finishing and annotation were performed by the JGI using state of the art sequencing technology [32]. A summary of the project information is shown in Table 2.
Table 2

Genome sequencing project information for Burkholderia sp. strain UYPR1.413

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

117.1 × Illumina

MIGS-30

Assemblers

Velvet version 1.1.04, ALLPATHS-LG V.r41043

MIGS-32

Gene calling methods

Prodigal 1.4

 

Locus Tag

A3A7

 

Genbank ID

JAFD01000000

 

Genbank Date of Release

January 23, 2014

 

GOLD ID

Gp0010091

 

BIOPROJECT

PRJNA165303

MIGS-13

Source Material Identifier

UYPR1.413

 

Project relevance

Symbiotic N2fixation, agriculture

Growth conditions and genomic DNA preparation

Burkholderia sp. strain UYPR1.413 was grown to mid logarithmic phase in TY rich media [21] 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 [33].

Genome sequencing and assembly

The draft genome of Burkholderia sp. UYPR1.413 was generated at the DOE Joint genome Institute (JGI) using state of the art technology [32]. An Illumina Std shotgun library was constructed and sequenced using the Illumina HiSeq 2000 platform which generated 23,255,298 reads totaling 3488.3 Mbp. All general aspects of library construction and sequencing performed at the JGI can be found at the JGI web site [34]. 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). The following steps were then performed for assembly: (1) filtered Illumina reads were assembled using Velvet version 1.1.04 [35] (2) 1–3 Kbp simulated paired end reads were created from Velvet contigs using wgsim [36] (3) Illumina reads were assembled with simulated read pairs using Allpaths-LG (version r41043) [37]. 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 342 contigs in 336 scaffolds. The total size of the genome is 10.4 Mbp and the final assembly is based on 1214.2 Mbp of Illumina data, which provides an average of 117.1× coverage of the genome.

Genome annotation

Genes were identified using Prodigal [38], as part of the DOE-JGI genome annotation pipeline [39, 40] followed by a round of manual curation using GenePRIMP [41] 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 [42] was used to find tRNA genes, whereas ribosomal RNA genes were found by searches against models of the ribosomal RNA genes built from SILVA [43]. 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 [44]. Additional gene prediction analysis and manual functional annotation was performed within the Integrated Microbial Genomes-Expert Review (IMG-ER) system [45] developed by the Joint Genome Institute, Walnut Creek, CA, USA.

Genome properties

The genome is 10,373,764 nucleotides with 62.28 % GC content (Table 3) and comprised of 336 scaffolds and 342 contigs (Fig. 3). From a total of 9836 genes, 9759 were protein encoding and 77 RNA only encoding genes. The majority of genes (75.92 %) were assigned a putative function whilst the remaining genes were annotated as hypothetical. The distribution of genes into COGs functional categories is presented in Table 4.
Table 3

Genome statistics for Burkholderia sp. strain UYPR1.413

Attribute

Value

% of total

Genome size (bp)

10,373,764

100

DNA coding (bp)

8,806,315

84.89

DNA G + C (bp)

6,461,024

62.28

DNA scaffolds

336

 

Total genes

9836

100

Protein-coding genes

9759

99.22

RNA genes

77

0.78

Pseudo genes

1

0.01

Genes in internal clusters

471

4.79

Genes with function prediction

7467

75.92

Genes assigned to COGs

6103

62.05

Genes with Pfam domains

7650

77.78

Genes with signal peptides

934

9.50

Genes with transmembrane helices

2097

21.32

CRISPR repeats

1

 
Fig. 3

Graphical map of the four largest scaffolds of the genome of Burkholderia sp. strain UYPR1.413. 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 Burkholderia sp. strain UYPR1.413 associated with the general COG functional categories

Code

Value

% Age

COG Category

J

193

2.79

Translation, ribosomal structure and biogenesis

A

1

0.01

RNA processing and modification

K

721

10.42

Transcription

L

231

3.34

Replication, recombination and repair

B

4

0.06

Chromatin structure and dynamics

D

36

0.52

Cell cycle control, Cell division, chromosome partitioning

V

67

0.97

Defense mechanisms

T

332

4.80

Signal transduction mechanisms

M

405

5.85

Cell wall/membrane/envelope biogenesis

N

136

1.96

Cell motility

U

200

2.89

Intracellular trafficking, secretion, and vesicular transport

O

196

2.83

Posttranslational modification, protein turnover, chaperones

C

526

7.60

Energy production and conversion

G

527

7.61

Carbohydrate transport and metabolism

E

789

11.40

Amino acid transport and metabolism

F

103

1.49

Nucleotide transport and metabolism

H

220

3.18

Coenzyme transport and metabolism

I

325

4.70

Lipid transport and metabolism

P

308

4.45

Inorganic ion transport and metabolism

Q

248

3.58

Secondary metabolite biosynthesis, transport and catabolism

R

794

11.47

General function prediction only

S

559

8.08

Function unknown

3733

37.95

Not in COGS

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

Conclusion

Burkholderia sp. UYPR1.413 belongs to a group of Beta-rhizobia isolated from Parapiptadenia rigida , a native tree from Uruguay belonging to the Mimosoideae legume group [18]. This tree is also native to the south of Brazil, Argentina and Paraguay [18]. Phylogenetic analysis revealed that UYPR1.413 is most closely related to Burkholderia sabiae Br3407T, Burkholderia caribensis MWAP64T and Burkholderia phymatum STM815T. Interestingly, Br3407T was isolated from nitrogen-fixing nodules on the roots of Mimosa caesalpiniifolia , a legume tree native to Brazil [6]. MWAP64T has not been reported to nodulate legume plants, however B. caribensis TJ182 is able to nodulate and fix nitrogen with Mimosa pigra [7]. STM815T was originally isolated from Macroptilium atropurpureum but could not be authenticated on this host [1]. Additional studies showed that STM815T is instead able to nodulate a wide range of Mimosa species [27]. Glasshouse experiments from previous studies have shown that Burkholderia sp. UYPR1.413 is also able to nodulate Mimosa pudica seedlings, albeit ineffectively [18]. However, it is different from the other microsymbiont in that it can form an effective association with Parapiptadenia rigida . The only other sequenced isolate to fix with this host is Cupriavidus sp. UYPR2.512 [46]. There are in total 13 Burkholderia strains that are known legume symbionts; four (WSM3556T, WSM4176, WSM5005T, STM678T) nodulate South African papilionoid species, in contrast to the other nine (BR3459, CCGE1002, DSM 21604, JPY251, JPY366, LMG 23256T, STM815, STM3621 and UYPR1.413) that are able to nodulate mimosoid species. A comparison of the mimosoid nodulating strains reveals that UYPR1.413 has the largest genome (10.4 Mbp), with the highest KOG count (1670) and the lowest GC (65.28 %) percentage in this group. All 13 of these genomes share the nitrogenase-RXN MetaCyc pathway catalyzed by a multiprotein nitrogenase complex. However, only Burkholderia sp. UYPR1.413 has been shown to fix effectively with Parapiptadenia rigida . The genome attributes of Burkholderia sp. UYPR1.413 will therefore be important for ongoing molecular analysis of the plant microbe interactions required for the establishment of leguminous tree symbioses with this host.

Abbreviations

GEBA-RNB: 

Genomic Encyclopedia of Bacteria and Archaea-Root Nodule Bacteria

JGI: 

Joint Genome Institute

TY: 

Trypton Yeast

CTAB: 

Cetyl trimethyl ammonium bromide

WSM: 

Western Australian Soil Microbiology

BNF: 

Biological Nitrogen Fixation

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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© De Meyer et al. 2015

This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. 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.

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