Open Access

High-quality permanent draft genome sequence of the Mimosa asperata - nodulating Cupriavidus sp. strain AMP6

  • Sofie E. De Meyer1,
  • Matthew Parker2,
  • Peter Van Berkum3,
  • Rui Tian1,
  • Rekha Seshadri4,
  • T.B.K. Reddy4,
  • Victor Markowitz5,
  • Natalia Ivanova4,
  • Amrita Pati4,
  • Tanja Woyke4,
  • Nikos Kyrpides4,
  • John Howieson1 and
  • Wayne Reeve1Email author
Standards in Genomic Sciences201510:80

DOI: 10.1186/s40793-015-0074-1

Received: 26 November 2014

Accepted: 8 October 2015

Published: 16 October 2015

Abstract

Cupriavidus sp. strain AMP6 is an aerobic, motile, Gram-negative, non-spore-forming rod that was isolated from a root nodule of Mimosa asperata collected in Santa Ana National Wildlife Refuge, Texas, in 2005. Mimosa asperata is the only legume described so far to exclusively associates with Cupriavidus symbionts. Moreover, strain AMP6 represents an early-diverging lineage within the symbiotic Cupriavidus group and has the capacity to develop an effective nitrogen-fixing symbiosis with three other species of Mimosa. Therefore, the genome of Cupriavidus sp. strain AMP6 enables comparative analyses of symbiotic trait evolution in this genus and here we describe the general features, together with sequence and annotation. The 7,579,563 bp high-quality permanent draft genome is arranged in 260 scaffolds of 262 contigs, contains 7,033 protein-coding genes and 97 RNA-only encoding genes, and is part of the GEBA-RNB project proposal.

Keywords

Root-nodule bacteria Nitrogen fixation Betaproteobacteria Texas Mimosa asperata GEBA-RNB

Introduction

Cupriavidus is one of two known genera of Betaproteobacteria that include legume root-nodule symbionts [1]. The other genus, Burkholderia , has multiple species associated with diverse legume host plants indigenous to North and South America, South Africa and Australia [28]. Cupriavidus , by contrast, has only been isolated from four species in two legume genera in the tribe Mimoseae ( Mimosa , Parapiptadenia), at a few locations in the native geographic ranges of their host plants (south Texas, the Caribbean, central America, French Guiana, and Uruguay; [2, 912]). However, both Cupriavidus and Burkholderia have now spread to many new regions along with species of Mimosa that are invasive weeds [10, 1317]. In South America, Cupriavidus was uncommon in French Guiana and Uruguay (3-10 % of nodule isolates; [9, 11]), and was not detected at all in extensive surveys of Mimosa in central Brazil [5, 6]. However, it has been isolated from two cultivated legumes in Minas Gerais, Brazil [18]. This suggests that further surveys in South America may discover additional wild legume hosts that utilize Cupriavidus symbionts.

The only legume studied to date that is exclusively associated with Cupriavidus nodule symbionts is Mimosa asperata , from which Cupriavidus strain AMP6 was isolated in 2005 [12]. The range of M. asperata is centered in Mexico and extends slightly into south Texas, Cuba, and northern Central America [19]. Based on both housekeeping loci and symbiotic loci, strain AMP6 represents an early-diverging lineage of nodule-symbiotic Cupriavidus [10, 12], whose genome may provide insights about how legume nodule symbiosis became established in this group.

Strain AMP6 was collected at the Santa Ana National Wildlife Refuge in Hidalgo County, Texas. Cupriavidus nodule bacteria resembling strain AMP6 are currently known only from M. asperata populations in the lower Rio Grande valley of Texas, and have not been detected in surveys of Mimosa species in other geographic locations [2, 911]. Nevertheless, inoculation tests have indicated that Cupriavidus strain AMP6 has the capacity to develop an effective nitrogen-fixing symbiosis with three other species of Mimosa [12]. M. asperata occurs mainly along the margins of seasonally flooded wetlands [20], a habitat characterized by heavy silt/clay soils with neutral to moderately alkaline pH (pH 7.0 - 8.4; [21]).

The first completed genome for a betaproteobacterial legume symbiont was that of Cupriavidus taiwanensis LMG 19424T [22]. Here we provide an analysis of the high-quality permanent draft genome sequence of Cupriavidus strain AMP6, enabling comparative analyses of symbiotic trait evolution in this genus.

Organism information

Classification and features

Cupriavidus sp. strain AMP6 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 0.4-0.6 μm in width and 1.2-1.7 μm in length (Fig. 1 Left). It is fast growing, forming 1.2-1.6 mm diameter colonies after 24 h when grown on YMA [23] at 28 °C. Colonies on YMA are white-opaque, slightly domed, moderately mucoid with smooth margins (Fig. 1 Right).
Fig. 1

Images of Cupriavidus sp. strain AMP6 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 AMP6 in a 16S rRNA gene sequence based tree. This strain is phylogenetically most related to Cupriavidus taiwanensis LMG 19424T , Cupriavidus alkaliphilus ASC-732T and Cupriavidus necator N-1T (deposited as ATCC43291T ) with sequence identities to the AMP6 16S rRNA gene sequence of 99.11 %, 99.04 % and 98.69 %, respectively, as determined using the EzTaxon-e server [24]. 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 [25]. Both ASC-732T and N-1T are soil bacteria that are not able to nodulate or fix nitrogen with legumes [26, 27]. Minimum Information about the Genome Sequence (MIGS) [28] of AMP6 is provided in Table 1.
Fig. 2

Phylogenetic tree highlighting the position of Cupriavidus sp. strain AMP6 (shown in blue print) relative to other type and non-type strains in the Cupriavidus genus using a 1,024 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 [46]. The tree was build 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 mentioned after the strain number, otherwise the NCBI accession number is provided. Finished genomes are designated with an asterisk

Table 1

Classification and general features of Cupriavidus sp. strain AMP6 in accordance with the MIGS recommendations [28] published by the Genome Standards Consortium [47]

MIGS ID

Property

Term

Evidence code

 

Classification

Domain Bacteria

TAS [48]

  

Phylum Proteobacteria

TAS [49, 50]

  

Class Betaproteobacteria

TAS [51]

  

Order Burkholderiales

TAS [52]

  

Family Burkholderiaceae

TAS [53]

  

Genus Cupriavidus

TAS [54]

  

Species Cupriavidus sp.

TAS [12]

  

(Type) strain AMP6

TAS [12]

 

Gram stain

Negative

TAS [54]

 

Cell shape

Rod

IDA

 

Motility

Motile

IDA

 

Sporulation

Non-sporulating

TAS [54]

 

Temperature range

Mesophile

TAS [54]

 

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

Texas, USA

TAS [12]

MIGS-5

Nodule collection date

2005

TAS [12]

MIGS-4.1

Longitude

−98.138

TAS [12]

MIGS-4.2

Latitude

26.0794

TAS [12]

MIGS-4.4

Altitude

30 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 [55]

Symbiotaxonomy

Cupriavidus sp. strain AMP6 was isolated from Mimosa asperata nodules collected at the Santa Ana National Wildlife Refuge in Hidalgo County, Texas [12]. Cupriavidus sp. strain AMP6 was assessed for nodulation and nitrogen fixation on five mimosa species, including M. pigra, M. pudica, M. invisia, M. strigillosa and M. quadrivalvis [12]. Strain AMP6 could nodulate all hosts apart from M. quadrivalvis [12]. Additional acetylene reduction assays provided information on the nitrogenase activity of strain AMP6 on those hosts. These test showed substantial nitrogenase activity with M. pudica and M. invisia but only a small amount with M. pigra [12]. The absence of nodule nitrogenase activity was also observed for M. strigillosa and M. quadrivalvis [12].

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 project at the U.S. Department of Energy, Joint Genome Institute [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 Cupriavidus sp. strain AMP6

MIGS ID

Property

Term

MIGS-31

Finishing quality

High-quality permanent draft

MIGS-28

Libraries used

Illumina Std PE

MIGS-29

Sequencing platforms

Illumina HiSeq 2000

MIGS-31.2

Fold coverage

117.0x Illumina

MIGS-30

Assemblers

Velvet 1.1.04, ALLPATHS V.r42328

MIGS-32

Gene calling methods

Prodigal 1.4

 

Locus Tag

K309

 

Genbank ID

AUFE00000000

 

Genbank Date of Release

December 12, 2013

 

GOLD ID

Gp0009812

 

BIOPROJECT

PRJNA195776

MIGS-13

Source Material Identifier

AMP6

 

Project relevance

Symbiotic N2fixation, agriculture

Growth conditions and genomic DNA preparation

Cupriavidus sp. strain AMP6 was grown on YMA solid medium [23] for 3 days, a single colony was selected and used to inoculate 5 ml TY broth medium. The culture was grown for 48 h on a gyratory shaker (200 rpm) at 28 °C. Subsequently 1 ml was used to inoculate 60 ml TY broth medium and grown on a gyratory shaker (200 rpm) at 28 °C until OD 0.6 was reached. DNA was isolated from 60 mL of cells using a CTAB bacterial genomic DNA isolation method [33]. Final concentration of the DNA was 0.6 mg/ml.

Genome sequencing and assembly

The genome of Cupriavidus sp. AMP6 was generated at the DOE Joint genome Institute [32]. An Illumina Std shotgun library was constructed and sequenced using the Illumina HiSeq 2000 platform which generated 15,823,344 reads totaling 2,373.5 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). 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 r42328) [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 262 contigs in 260 scaffolds. The total size of the genome is 7.6 Mbp and the final assembly is based on 886.3 Mbp of Illumina data, which provides an average of 117.0× 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 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 7,579,563 nucleotides with 65.46 % GC content (Table 3) and comprised of 260 scaffolds and 262 contigs. From a total of 7,130 genes, 7,033 were protein encoding and 97 RNA only encoding genes. The majority of genes (80.24 %) 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. AMP6

Attribute

Value

% of Total

Genome size (bp)

7,579,563

100.00

DNA coding (bp)

6,545,489

86.36

DNA G + C (bp)

4,961,426

65.46

DNA scaffolds

260

100.00

Total genes

7,130

100.00

Protein-coding genes

7,033

98.64

RNA genes

97

1.36

Pseudo genes

0

0.00

Genes in internal clusters

538

7.55

Genes with function prediction

5,721

80.24

Genes assigned to COGs

4,791

67.19

Genes with Pfam domains

5,837

81.87

Genes with signal peptides

681

9.55

Genes with transmembrane helices

1,477

20.72

CRISPR repeats

1

 
Table 4

Number of genes associated with general COG functional categories

Code

Value

% age

COG Category

J

182

3.37

Translation, ribosomal structure and biogenesis

A

1

0.02

RNA processing and modification

K

527

9.76

Transcription

L

188

3.48

Replication, recombination and repair

B

4

0.07

Chromatin structure and dynamics

D

32

0.59

Cell cycle control, Cell division, chromosome partitioning

V

59

1.09

Defense mechanisms

T

210

3.89

Signal transduction mechanisms

M

275

5.09

Cell wall/membrane/envelope biogenesis

N

96

1.78

Cell motility

U

119

2.20

Intracellular trafficking, secretion, and vesicular transport

O

164

3.04

Posttranslational modification, protein turnover, chaperones

C

447

8.28

Energy production and conversion

G

256

4.74

Carbohydrate transport and metabolism

E

501

9.28

Amino acid transport and metabolism

F

90

1.67

Nucleotide transport and metabolism

H

185

3.43

Coenzyme transport and metabolism

I

344

6.37

Lipid transport and metabolism

P

272

5.04

Inorganic ion transport and metabolism

Q

235

4.35

Secondary metabolite biosynthesis, transport and catabolism

R

659

12.21

General function prediction only

S

552

10.23

Function unknown

-

2339

32.81

Not in COGS

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

Conclusion

Cupriavidus sp. AMP6 belongs to a group of Beta-rhizobia isolated from Mimosa asperata . Phylogenetic analysis revealed that AMP6 is most closely related to Cupriavidus taiwanensis LMG 19424T , which was isolated from Mimosa pudica , and is able to nodulate and fix nitrogen in association with several Mimosa species [13]. 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 AMP6 has the second largest genome (7.6 Mbp), with the highest KOG count (1398) and the second lowest GC (65.46 %) and signal peptide (9.55 %) percentages in this group. All of these genomes share the nitrogenase-RXN MetaCyc pathway characterized by the 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. AMP6 has been shown to fix effectively with Mimosa asperata . The genome attributes of Cupriavidus sp. AMP6, in conjunction with other Cupriavidus genomes, will be important for ongoing molecular analysis of the plant microbe interactions required for the establishment of Mimosa symbioses.

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

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.

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)
Centre for Rhizobium Studies, Murdoch University
(2)
Binghamton University, State University of New York
(3)
Soybean Genomics and improvement laboratory Bldg 006, BARC-West USDA ARS 10300 Baltimore Blvd
(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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