Open Access

Complete genome sequence of Kosakonia oryzae type strain Ola 51T

Contributed equally
Standards in Genomic Sciences201712:28

https://doi.org/10.1186/s40793-017-0240-8

Received: 1 September 2016

Accepted: 7 April 2017

Published: 17 April 2017

Abstract

Strain Ola 51T (=LMG 24251T = CGMCC 1.7012T) is the type strain of the species Kosakonia oryzae and was isolated from surface-sterilized roots of the wild rice species Oryza latifolia grown in Guangdong, China. Here we summarize the features of the strain Ola 51T and describe its complete genome sequence. The genome contains one circular chromosome of 5,303,342 nucleotides with 54.01% GC content, 4773 protein-coding genes, 16 rRNA genes, 76 tRNA genes, 13 ncRNA genes, 48 pseudo genes, and 1 CRISPR array.

Keywords

Endophyte Kosakonia Nitrogen fixationPlant growth-promoting bacteria

Introduction

Enterobacter cowanii [1], E. radicincitans [2], E. oryzae [3], E. arachidis [4], E. sacchari [5], E. oryziphilus [6, 7], and E. oryzendophyticus [6, 7] have been transferred into the novel genus Kosakonia of the family “ Enterobacteriaceae ” [810]. A novel species “Kosakonia pseudosacchari” [11] closely related to K. sacchari was recently proposed. With the exception of the type species K. cowanii , which was originally obtained from clinical samples [1], the other members of the genus Kosakonia are nitrogen-fixing bacteria associated with plants [26, 11] and commonly occur in the nitrogen-fixing bacterial community of some non-legume crops, such as rice [6] and sugarcane [12]. Some nitrogen-fixing Kosakonia strains are able to promote crop growth [1214].

Strain Ola 51T (=LMG 24251 T=CGMCC 1.7012 T) is the type strain of the species Kosakonia oryzae and was isolated from surface-sterilized roots of the wild rice species Oryza latifolia grown in Guangdong, China [3]. Here we present the summary of the features of the K. oryzae type strain Ola 51T and its complete genome sequence, which provides a reference for resolving the phylogeny and taxonomy of closely related strains and the genetic information to study its plant growth-promoting potential and its plant-associated life style.

Organism information

Classification and features

K. oryzae strain Ola 51T is a Gram-negative, non-spore-forming, motile rod with peritrichous flagella (Fig. 1). It grows aerobically but reduces N2 to NH3 at a low pO2. It forms circular, convex, smooth colonies with entire margins on nutrient agar [3, 8]. It grows best around 30 °C and pH 7 (Table 1) [3]. K. oryzae Ola 51T has the typical biochemical phenotypes of the genus Kosakonia : positive for acetoin production (Voges-Proskauer test) while negative for indole production; positive for β-galactosidase and arginine dihydrolase while negative for lysine decarboxylase; positive for oxidation of arabinose, cellobiose, citrate, fructose, galactose, gluconate, glucose, glycerol, lactose, malate, maltose, mannitol, mannose, sorbitol, sucrose and trehalose (Table 1) [3, 8].
Fig. 1

Cell morphology of the Kosakonia oryzae type strain Ola 51T. The bacterium was stained by uranyl acetate and observed by a transmission electron microscope

Table 1

Classification and general features of Kosakonia oryzae strain Ola 51T according to the MIGS recommendations [15]

MIGS ID

Property

Term

Evidence codea

 

Classification

Domain Bacteria

TAS [34]

Phylum Proteobacteria

TAS [35]

Class Gammaproteobacteria

TAS [36, 37]

Order “Enterobacteriales

TAS [38]

Family Enterobacteriaceae

TAS [39, 40]

Genus Kosakonia

TAS [8]

Species Kosakonia oryzae

TAS [3, 8]

Type strain: Ola 51T

TAS [3]

 

Gram stain

Negative

TAS [3]

 

Cell shape

Rod

TAS [3]

 

Motility

Motile

TAS [3]

 

Sporulation

Non-sporulating

TAS [3]

 

Temperature range

10–40 °C

TAS [3]

 

Optimum temperature

28–37 °C

TAS [3]

 

pH range; Optimum Carbon source

3.5–10; 6.0–8.0

Arabinose, cellobiose, citrate, fructose, galactose, gluconate, glucose, glycerol, lactose, malate, maltose, mannitol, mannose, sorbitol, sucrose & trehalose

TAS [3]

TAS [3, 8]

MIGS-6

Habitat

Plants

TAS [3]

MIGS-6.3

Salinity

0 – 5% NaCl (w/v)

TAS [3]

MIGS-22

Oxygen requirement

Facultatively anaerobic

TAS [3]

MIGS-15

Biotic relationship

Free-living, endophytic

TAS [3]

MIGS-14

Pathogenicity

Not reported

 

MIGS-4

Geographic location

Guangzhou, Guangdong, China

TAS [3]

MIGS-5

Sample collection

September 12, 2005

TAS [3]

MIGS-4.1 MIGS-4.2

Latitude

23.1634171311 °N

NAS

Longitude

113.3534469581°E

NAS

MIGS-4.3

Depth

0.2 – 0.3 m below the surface

TAS [3]

MIGS-4.4

Altitude

20 m

NAS

a 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 [41]

The 16S rRNA gene sequence of K. oryzae Ola 51T was deposited in GenBank under the accession number EF488759 [3]. A phylogenetic analysis of the 16S rRNA gene sequences from the strains belonging to the genus Kosakonia and Escherichia coli ATCC11775 T (the type strain of the type species of the type genus of the family Enterobacteriaceae ) showed that K. oryzae Ola 51T is most closely related to the strains belonging to the species K. radicincitans (Fig. 2) [3, 811].
Fig. 2

Phylogenetic tree based on the 16S rRNA gene sequences showing the phylogenetic position of the Kosakonia oryzae type strain Ola 51T () and other strains belonging to the genus Kosakonia. The sequences were aligned using the SINA (SILVA Incremental Aligner) Alignment Service [42] and were constructed to the phylogenetic tree with the neighbor-joining algorithm and the Kimura 2-parameter model integrated in the MEGA 5.2 program [43]. Bootstrap values (>50%) of 1,000 tests are shown at the nodes. The tree was rooted on the outgroup Escherichia coli ATCC 11775T. The GenBank accession numbers of the sequences are indicated in brackets; * indicates the accession number of a contig of the whole genome sequence. The scale bar indicates 0.1% substitutions per site

Chemotaxonomic data

Whole-cell fatty acids were extracted from cells grown aerobically at 28 °C for 24 h on the TSA medium according to the recommendations of the Microbial Identification System (MIDI Inc., Delaware USA). The whole-cell fatty acid composition was determined using a 6890 N gas chromatograph (Agilent Technologies, Santa Clara, USA) and the peaks of the profiles were identified using the TSBA50 identification library version 5.0 (MIDI). K. oryzae Ola 51T shows the typical cell fatty acid profile of the genus Kosakonia [8]. The major fatty acids are C16:0, C18:1 ω7c, C16:1 ω7c/15:0 iso 2OH, C17:0 cyclo and C14:0 3OH/16:1 iso I [8, 11].

Genome sequencing information

Genome project history

K. oryzae Ola 51T was selected for sequencing based on its taxonomic significance. The genome sequence is deposited in GenBank under the accession number CP014007. A summary of the genome sequencing project information and its association with MIGS version 2.0 [15] is shown in Table 2.
Table 2

Genome sequencing project information for Kosakonia oryzae strain Ola 51T

MIGS ID

Property

Term

MIGS 31

Finishing quality

Finished

MIGS-28

Libraries used

PacBio 8 –11 Kb library

MIGS 29

Sequencing platforms

PacBio RS II

MIGS 31.2

Fold coverage

PacBio 128 ×

MIGS 30

Assemblers

HGAP Assembly.3 in SMRT analysis-2.3.0

MIGS 32

Gene calling method

GeneMarkS+

 

Locus Tag

AWR26

 

Genbank ID

CP014007

 

GenBank Date of Release

June 6, 2016

 

GOLD ID

Gp0154734

 

BIOPROJECT

PRJNA309028

MIGS 13

Source Material Identifier

LMG 24251T = CGMCC 1.7012T

 

Project relevance

Taxonomy, agriculture, plant-microbe interactions

Growth conditions and genomic DNA preparation

K. oryzae Ola 51T was grown aerobically in liquid Luria-Bertani medium at 30 °C until early stationary phase. The genome DNA was extracted from the cells by using a TIANamp bacterial DNA kit (Tiangen Biotech, Beijing, China). DNA quality (OD260/OD280 = 1.8) and quantity (22 μg) were determined with a Nanodrop spectrometer (Thermo Scientific, Wilmington, USA).

Genome sequencing and assembly

The genomic DNA of K. oryzae Ola 51T was constructed into 8 – 11 kb insert libraries and sequenced using PacBio SMRT sequencing technology [16] at the Duke University Genome Sequencing & Analysis Core Resource. Sequencing was run on two SMRT cells and resulted in 124,997 high-quality filtered reads with an average length of 8,260 bp. High-quality reads were assembled by the RS_HGAP_Assembly.3 in the SMRT analysis v2.3.0. The final assembly produced 128-fold coverage of the genome.

Genome annotation

Automated genome annotation was done using the NCBI Prokaryotic Genome Annotation Pipeline [17]. Functional annotations were done by searching against the KEGG [18], InterPro [19], and COG [20] databases. Genes with signal peptides were predicted using SignalP [21]. Genes with transmembrane helices were predicted using TMHMM [22].

Genome properties

The genome of K. oryzae Ola 51T contains one circular chromosome (Fig. 3). The chromosome contains 5,303,342 nucleotides with 54.0% G + C content. The genome contains 4,926 predicted genes, 4773 protein-coding genes, 105 RNA genes (16 rRNA genes, 76 tRNA genes, and 13 ncRNA genes), 48 pseudo genes, and 1 CRISPR repeats. Among the 4,773 protein-coding genes, 3,765 genes (78.88%) have been assigned functions, while 1008 genes (21.12%) have been annotated as hypothetical or unknown proteins (Table 3). The distribution of genes into COG functional categories is presented in Table 4 and Fig. 3.
Fig. 3

Circular map of the chromosome of the Kosakonia oryzae strain Ola 51T. From outside to the center: CDS on forward strand colored according to their COG categories (oranges/reds: information storage and processing; greens/yellows: cellular processes and signaling; blues/purples: metabolism; grays: pooly characterized), CDS and RNA genes on forward strand, CDS and RNA genes on reverse strand, CDS on reverse strand colored according to their COG categories, GC content, and GC skew. The circular map was generated by CGView [44]

Table 3

Genome statistics

Attribute

Value

% of Total

Genome size (bp)

5,303,342

100

DNA coding (bp)

4,613,400

86.99

DNA G + C (bp)

2,864,594

54.01

DNA scaffolds

1

100

Total genes

4,926

100

Protein-coding genes

4,773

96.89

RNA genes

105

2.13

Pseudo genes

48

0.97

Genes in internal clusters

ND

 

Genes with function prediction

3765

76.43

Genes assigned to COGs

4237

86.01

Genes with Pfam domains

4416

89.65

Genes with signal peptides

432

8.77

Genes with transmembrane helices

1179

23.93

CRISPR repeats

1

0.02

Table 4

Number of genes associated with general COG functional categories

Code

Value

%age

Description

J

194

4.06

Translation, ribosomal structure and biogenesis

A

1

0.02

RNA processing and modification

K

414

8.67

Transcription

L

140

2.93

Replication, recombination and repair

B

0

0

Chromatin structure and dynamics

D

35

0.73

Cell cycle control, Cell division, chromosome partitioning

V

60

1.26

Defense mechanisms

T

278

5.82

Signal transduction mechanisms

M

270

5.66

Cell wall/membrane biogenesis

N

163

3.42

Cell motility

U

123

2.58

Intracellular trafficking and secretion

O

154

3.23

Posttranslational modification, protein turnover, chaperones

C

287

6.01

Energy production and conversion

G

428

8.97

Carbohydrate transport and metabolism

E

476

9.97

Amino acid transport and metabolism

F

93

1.95

Nucleotide transport and metabolism

H

188

3.94

Coenzyme transport and metabolism

I

152

3.18

Lipid transport and metabolism

P

293

6.14

Inorganic ion transport and metabolism

Q

98

2.05

Secondary metabolites biosynthesis, transport and catabolism

R

502

10.52

General function prediction only

S

422

8.84

Function unknown

-

536

11.23

Not in COGs

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

Insights from the genome sequence

The genome sequences of K. cowanii JCM 10956 T, K. radicincitans DSM 16656 T (=D5/23T) [23], K. radicincitans UMEnt01/12 [24], K. radicincitans YD4 [25], K. sacchari SP1T [26], “K. pseudosacchari” JM-387T [11], K. oryzae KO348 [27], and Enterobacter sp. R4-368 [28] which was close to K. sacchari SP1T [26] had been deposited in the GenBank database. The genome ANIs (Additional file 1: Table S1) between Ola 51T and the other strains belonging to the genus Kosakonia were calculated using the Orthologous Average Nucleotide Identity tool [29]. The cut-off ANI value for species boundary was set at 95% - 96% [30]. The ANI value (95.85%) between K. oryzae Ola 51T and K. radicincitans DSM 16656 T is in the fuzzy zone 95% - 96%. The digital DDH value between Ola 51T and DSM 16656 T calculated by the Genome-to-Genome Distance Calculator [31] with the Formula 2 is 66.2%, below the 70% cut-off value for species boundary. Moreover, Ola 51T and DSM 16656 T were differentiated by metabolic phenotypes [3, 11] and ribosomal protein mass profiles [5]. Therefore, K. oryzae and K. radicincitans are closely related sister species.

Strain YD4 was closer to K. radicincitans DSM 16656 T than K. oryzae Ola 51T on the phylogenetic tree based on the 16S rRNA genes (Fig. 2). However, the ANI value and the digital DDH value between YD4 and K. radicincitans DSM 16656 T is 95.56% and 64.4%, respectively, while between YD4 and K. oryzae Ola 51T is 97.04% and 74.3%, respectively. Therefore, the strain YD4 belongs to K. oryzae but not K. radicincitans .

Strain KO348 was grouped with K. sacchari SP1T, Enterobacter sp. R4-368, and “K. pseudosacchari” JM-387T on the phylogenetic tree based on the 16S rRNA genes (Fig. 2). The ANI value between KO348 and K. oryzae Ola 51T is 84.04%. The strain KO348 thus does not belong to K. oryzae . The ANI value between KO348 and Enterobacter sp. R4-368 [27], K. sacchari SP1T, or “K. pseudosacchari” JM-387T is 98.80%, 94.56%, or 94.05%, respectively. Therefore, KO348 and R4-368 belong to the same species, likely a novel species closely related to K. sacchari and “K. pseudosacchari”.

K. oryzae Ola 51T and YD4, K. radicincitans DSM 16656 T and UMEnt01/12, K. sacchari SP1T, “K. pseudosacchari” JM-387T, and Kosakonia sp. KO348 and R4-368 were all isolated from plants. Their genomes contain genes encoding multiple enzymes degrading plant cell wall polysaccharides and removing reactive oxygen species, likely facilitating endophytic colonization [32]. They all contain genes encoding the regulatory protein (Fha1) and structural proteins (Lip, IcmF, DotU and ClpV) and secreted proteins (VgrG and Hcp) of the type VI secretion system, which may play a role in the plant-associated lifestyle [32]. Except K. radicincitans DSM 16656 T and UMEnt01/12, these strains contain the most structural proteins (YscCJRSTUVN) of the type III secretion system, which is not widespread among the previously studied endophytic bacteria [32].

These plant-associated Kosakonia strains contain genes contributing to multiple plant growth-promoting activities. They all contain the nif gene cluster (nifJHDKTYENXUSVWZMFLABQ) for the Mo-Fe nitrogenase-dependent nitrogen fixation, the genes encoding indole-3-acetaldehyde dehydrogenase, aspartate aminotransferase, aromatic amino acid aminotransferase and phenylpyruvate decarboxylase for producing the phytohormone auxin, and the budABC genes for producing volatile acetoin and 2,3-butanediol which induce plant systemic resistance to pathogens [33]. In addition, K. oryzae Ola 51T and YD4, and K. radicincitans DSM 16656 T and UMEnt01/12 also contain the anf gene cluster (anfHDGK) for the Fe-Fe nitrogenase-dependent nitrogen fixation. In contrast, the clinical strain K. cowanii JCM 10956 T does not contain the nif gene cluster.

Conclusions

The phylogeny of the members of the genus Kosakonia based on the 16S rRNA gene sequences is roughly in agreement with their overall genome relatedness. The complete genome sequence of K. oryzae Ola 51T provides the reference genome for genomic identification of strains belonging to K. oryzae . Analyses of the overall genome relatedness indices (ANI and digital DDH values), easily and reliably show that K. oryzae and K. radicincitans are closely related sister species and that the strain YD4, which shows close 16S rRNA gene-based phylogeney to K. radicincitans and was classified into K. radicincitans , belongs to K. oryzae . As well as YD4, which is able to promote growth of the yerba mate plants in low-fertility soils [14], K. oryzae Ola 51T contains both the nif gene cluster and the anf gene cluster for nitrogen fixation and genes contributing to production of auxin and volatile acetoin and 2,3-butanediol. Therefore, K. oryzae Ola 51T may be able to promote plant growth. Genomic analyses also show that K. oryzae Ola 51T and YD4 may have the type III and VI secretion systems and thus motivate us to study the functions of the type III and VI secretion systems in the interactions between beneficial Kosakonia bacteria and plants.

Abbreviations

ANI: 

Average nucleotide identity

DDH: 

DNA-DNA hybridization

SMRT: 

Single Molecule Real-Time

Declarations

Funding

This work was supported by the National Natural Science Foundation of China (31171504, 31370052 and 31471449), Zhejiang Provincial Natural Science Foundation of China (LY14C010002), Science and Technology Planning Project of Guangdong Province (2014A030313459 and 2014A050503058), and the State Key Laboratory of Rice Biology, China.

Authors’ contributions

YL, SL and MC assembled the sequencing data and completed the genome analysis; GP did the microbiological studies and obtained the organism information; ZT and QA designed the study and wrote the manuscript. All authors read and approved the final manuscript.

Competing interests

The authors declare that they have no competing interests.

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Authors’ Affiliations

(1)
State Key Laboratory of Rice Biology, Institute of Biotechnology, Zhejiang University
(2)
College of Natural Resources and Environment, South China Agricultural University
(3)
College of Agriculture, South China Agricultural University

References

  1. Inoue K, Sugiyama K, Kosako Y, Sakazaki R, Yamai S. Enterobacter cowanii sp. nov., a new species of the family Enterobacteriaceae. Curr Microbiol. 2000;41:417–20. PubMedhttp://dx.doi.org/10.1007/s002840010160.View ArticlePubMedGoogle Scholar
  2. Kämpfer P, Ruppel S, Remus R. Enterobacter radicincitans sp. nov., a plant growth promoting species of the family Enterobacteriaceae. Syst Appl Microbiol. 2005;28:213–21. PubMed http://dx.doi.org/10.1016/j.syapm.2004.12.007.View ArticlePubMedGoogle Scholar
  3. Peng G, Zhang W, Luo H, Xie H, Lai W, Tan Z. Enterobacter oryzae sp. nov, a nitrogen-fixing bacterium isolated from the wild rice species Oryza latifolia. Int J Syst Evol Microbiol. 2009;59:1650–5. PubMed http://dx.doi.org/10.1099/ijs.0.65484-0.View ArticlePubMedGoogle Scholar
  4. Madhaiyan M, Poonguzhali S, Lee J-S, Saravanan VS, Lee K-C, Santhanakrishnan P. Enterobacter arachidis sp. nov., a plant-growth-promoting diazotrophic bacterium isolated from rhizosphere soil of groundnut. Int J Syst Evol Microbiol. 2010;60:1559–64. PubMedhttp://dx.doi.org/10.1099/ijs.0.013664-0.View ArticlePubMedGoogle Scholar
  5. Zhu B, Zhou Q, Lin L, Hu C, Shen P, Yang L, An Q, Xie G, Li Y. Enterobacter sacchari sp. nov., a nitrogen-fixing bacterium associated with sugar cane (Saccharum officinarum L.). Int J Syst Evol Microbiol. 2013;63:2577–82. PubMed http://dx.doi.org/10.1099/ijs.0.045500-0.View ArticlePubMedGoogle Scholar
  6. Hardoim PR, Nazir R, Sessitsch A, Elhottová D, Korenblum E, van Overbeek LS, van Elsas JD. The new species Enterobacter oryziphilus sp. nov. and Enterobacter oryzendophyticus sp. nov. are key inhabitants of the endosphere of rice. BMC Microbiol. 2013;13:164. PubMed http://dx.doi.org/10.1186/1471-2180-13-164.View ArticlePubMedPubMed CentralGoogle Scholar
  7. Oren A, Garrity GM. Validation list no. 166. Int J Syst Evol Microbiol. 2015;65:3763–7. PubMed http://dx.doi.org/10.1099/ijsem.0.000632.View ArticlePubMedGoogle Scholar
  8. Brady C, Cleenwerck I, Venter S, Coutinho T, De Vos P. Taxonomic evaluation of the genus Enterobacter based on multilocus sequence analysis (MLSA): proposal to reclassify E. nimipressuralis and E. amnigenus into Lelliottia gen. nov. as Lelliottia nimipressuralis comb. nov. and Lelliottia amnigena comb. nov., respectively, E. gergoviae and E. pyrinus into Pluralibacter gen. nov. as Pluralibacter gergoviae comb. nov. and Pluralibacter pyrinus comb. nov., respectively, E. cowanii, E. radicincitans, E. oryzae and E. arachidis into Kosakonia gen. nov. as Kosakonia cowanii comb. nov., Kosakonia radicincitans comb. nov., Kosakonia oryzae comb. nov. and Kosakonia arachidis comb. nov., respectively, and E. turicensis, E. helveticus and E. pulveris into Cronobacter as Cronobacter zurichensis nom. nov., Cronobacter helveticus comb. nov. and Cronobacter pulveris comb. nov., respectively, and emended description of the genera Enterobacter and Cronobacter. Syst Appl Microbiol. 2013;36:309-19. PubMed http://dx.doi.org/10.1016/j.syapm.2013.03.005.
  9. Gu CT, Li CY, Yang LJ, Huo GC. Enterobacter xiangfangensis sp. nov., isolated from Chinese traditional sourdough, and reclassification of Enterobacter sacchari. Int J Syst Evol Microbiol. 2014;64:2650–6. PubMed http://dx.doi.org/10.1099/ijs.0.064709-0.View ArticlePubMedGoogle Scholar
  10. Li CY, Zhou YL, Ji J, Gu CT. Reclassification of Enterobacter oryziphilus and Enterobacter oryzendophyticus as Kosakonia oryziphila comb. nov. and Kosakonia oryzendophytica comb. nov. Int J Syst Evol Microbiol. 2016. PubMed http://dx.doi.org/10.1099/ijsem.0.001054.
  11. Kämpfer P, McInroy JA, Doijad S, Chakraborty T, Glaeser SP. Kosakonia pseudosacchari sp. nov., an endophyte of Zea mays. Syst Appl Microbiol. 2016;39:1–7. PubMed http://dx.doi.org/10.1016/j.syapm.2015.09.004.View ArticlePubMedGoogle Scholar
  12. Lin L, Li Z, Hu C, Zhang X, Chang S, Yang L, Li Y, An Q. Plant growth-promoting nitrogen-fixing enterobacteria are in association with sugarcane plants growing in Guangxi. China Microbes Environ. 2012;27:391–8. PubMed http://dx.doi.org/10.1264/jsme2.ME11275.View ArticlePubMedGoogle Scholar
  13. Berger B, Wiesner M, Brock AK, Schreiner M, Ruppel S. K. radicincitans, a beneficial bacteria that promotes radish growth under field conditions. Agron Sustain Dev. 2015;35:1521–8. PubMed http://dx.doi.org/10.1007/s13593-015-0324-z.View ArticleGoogle Scholar
  14. Bergottini VM, Otegui MB, Sosa DA, Zapata PD, Mulot M, Rebord M, Rebord M, Zopfi J, Wiss F, Benrey B, Junier P. Bio-inoculation of yerba mate seedlings (Ilex paraguariensis St. Hill.) with native plant growth-promoting rhizobacteria: a sustainable alternative to improve crop yield. Biol Fertil Soils. 2015;51:749–55. PubMed http://dx.doi.org/10.1007/s00374-015-1012-5.View ArticleGoogle Scholar
  15. Field D, Garrity G, Gray T, Morrison N, Selengut J, Sterk P, Tatusova T, Thomson N, Allen MJ, Angiuoli SV, Ashburner M, Axelrod N, Baldauf S, Ballard S, Boore J, Cochrane G, Cole J, Dawyndt P, De Vos P, dePamphilis C, Edwards R, Faruque N, Feldman R, Gilbert J, Gilna P, Glöckner FO, Goldstein P, Guralnick R, Haft D, Hancock D, et al. Minimum Information about a Genome Sequence (MIGS) specification. Nat Biotechnol. 2008;26:541–7. PubMed http://dx.doi.org/10.1038/nbt1360.View ArticlePubMedPubMed CentralGoogle Scholar
  16. Eid J, Fehr A, Gray J, Luong K, Lyle J, Otto G, Peluso P, Rank D, Baybayan P, Bettman B, Bibillo A, Bjornson K, Chaudhuri B, Christians F, Cicero R, Clark S, Dalal R, de Winter A, Dixon J, Foquet M, Gaertner A, Hardenbol P, Heiner C, Hester K, Holden D, Kearns G, Kong X, Kuse R, Lacroix Y, Lin S, et al. Real-time DNA sequencing from single polymerase molecules. Science. 2009;323:133–8. PubMed http://dx.doi.org/10.1126/science.1162986.View ArticlePubMedGoogle Scholar
  17. Tatusova T, DiCuccio M, Badretdin A, Chetvernin V, Nawrocki EP, Zaslavsky L, Lomsadze A, Pruitt KD, Borodovsky M, Ostell J. NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res. 2016;44:6614–24. PubMed http://dx.doi.org/10.1093/nar/gkw569.View ArticlePubMedPubMed CentralGoogle Scholar
  18. KEGG [http://www.genome.jp/kegg/]. Accessed 9 Apr 2017.
  19. InterPro [http://www.ebi.ac.uk/interpro/scan.html]. Accessed 9 Apr 2017.
  20. COG [http://weizhong-lab.ucsd.edu/metagenomic-analysis/server/cog/]. Accessed 9 Apr 2017.
  21. Bendtsen JD, Nielsen H, von Heijne G, Brunak S. Improved prediction of signal peptides: SignalP 3.0. J Mol Biol. 2004;340:783–95. PubMed http://dx.doi.org/10.1016/j.jmb.2004.05.028.View ArticlePubMedGoogle Scholar
  22. Krogh A, Larsson B, von Heijne G, Sonnhammer ELL. Predicting transmembrane protein topology with a hidden Markov model: Application to complete genomes. J Mol Biol. 2001;305:567–80. PubMed http://dx.doi.org/10.1006/jmbi.2000.4315.View ArticlePubMedGoogle Scholar
  23. Witzel K, Gwinn-Giglio M, Nadendla S, Shefchek K, Ruppel S. Genome sequence of Enterobacter radicincitans DSM16656T, a plant growth-promoting endophyte. J Bacteriol. 2012;194:5469. PubMed http://dx.doi.org/10.1128/JB.01193-12.View ArticlePubMedPubMed CentralGoogle Scholar
  24. Mohd Suhaimi NS, Yap KP, Ajam N, Thong KL. Genome sequence of Kosakonia radicincitans UMEnt01/12, a bacterium associated with bacterial wilt diseased banana plant. FEMS Microbiol Lett. 2014;358:11–3. PubMed http://dx.doi.org/10.1111/1574-6968.12537.View ArticleGoogle Scholar
  25. Bergottini VM, Filippidou S, Junier T, Johnson S, Chain PS, Otegui MB, Zapata PD, Junier P. Genome sequence of Kosakonia radicincitans strain YD4, a plant growth-promoting rhizobacterium isolated from yerba mate (Ilex paraguariensis St. Hill.). Genome Announc. 2015;3:e00239–15. PubMed http://dx.doi.org/10.1128/genomeA.00239-15.View ArticlePubMedPubMed CentralGoogle Scholar
  26. Chen M, Zhu B, Lin L, Yang L, Li Y, An Q. Complete genome sequence of Kosakonia sacchari type strain SP1T. Stand Genomic Sci. 2014;9:1311–8. PubMed http://dx.doi.org/10.4056/sigs.5779977.View ArticlePubMedPubMed CentralGoogle Scholar
  27. Meng X, Bertani I, Abbruscato P, Piffanelli P, Licastro D, Wang C, Venturi V. Draft genome sequence of rice endophyte-associated isolate Kosakonia oryzae KO348. Genome Announc. 2015;3:e00594–15. PubMed http://dx.doi.org/10.1128/genomeA.00594-15.View ArticlePubMedPubMed CentralGoogle Scholar
  28. Madhaiyan M, Peng N, Ji L. Complete genome sequence of Enterobacter sp. strain R4-368, an endophytic N-fixing gammaproteobacterium isolated from surface-sterilized roots of Jatropha curcas L. Genome Announc. 2013;1:e00544–13. PubMed http://dx.doi.org/10.1128/genomeA.00544-13.View ArticlePubMedPubMed CentralGoogle Scholar
  29. Lee I, Kim YO, Park S-C, Chun J. OrthoANI: An improved algorithm and software for calculating average nucleotide identity. Int J Syst Evol Microbiol. 2016;66:1100–3. PubMed http://dx.doi.org/10.1099/ijsem.0.000760.View ArticleGoogle Scholar
  30. Richter M, Rosselló-Móra R. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci U S A. 2009;45:19126–31. PubMed http://dx.doi.org/10.1073/pnas.0906412106.View ArticleGoogle Scholar
  31. GGDC [http://ggdc.dsmz.de/distcalc2.php]. Accessed 9 Apr 2017.
  32. Reinhold-Hurek B, Hurek T. Living inside plants: bacterial endophytes. Curr Opin Plant Biol. 2011;14:435–43. PubMed http://dx.doi.org/10.1016/j.pbi.2011.04.004.View ArticlePubMedGoogle Scholar
  33. Ryu CM, Farag MA, Hu CH, Reddy MS, Wei HX, Paré PW, Kloepper JW. Bacterial volatiles promote growth in Arabidopsis. Proc Natl Acad Sci U S A. 2003;100:4927–32. PubMed http://dx.doi.org/10.1073/pnas.0730845100.View ArticlePubMedPubMed CentralGoogle Scholar
  34. Woese CR, Kandler O, Wheelis ML. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci U S A. 1990;87:4576–9. PubMed http://dx.doi.org/10.1073/pnas.87.12.4576.View ArticlePubMedPubMed CentralGoogle Scholar
  35. Garrity GM, Bell JA, Lilburn T. Phylum XIV. Proteobacteria phyl. nov. In: Garrity GM, Brenner DJ, Krieg NR, Staley JT, editors. Bergey’s Manual of Systematic Bacteriology, Volume 2, Part B. 2nd ed. New York: Springer; 2005. p. 1.View ArticleGoogle Scholar
  36. Garrity GM, Bell JA, Lilburn T. Class III. Gammaproteobacteria class. nov. In: Garrity GM, Brenner DJ, Krieg NR, Staley JT, editors. Bergey’s Manual of Systematic Bacteriology, Volume 2, Part B. 2nd ed. Springer: New York; 2005. p. 1.View ArticleGoogle Scholar
  37. Validation of publication of new names and new combinations previously effectively published outside the IJSEM. List no. 106. Int J Syst Evol Microbiol.2005;55:2235-8. PubMed http://dx.doi.org/10.1099/ijs.0.64108-0.
  38. Garrity GM, Holt JG. Taxonomic Outline of the Archaea and Bacteria. In: Garrity GM, Boone DR, Castenholz RW, editors. Bergey’s Manual of Systematic Bacteriology, Volume 1. 2nd ed. New York: Springer; 2001. p. 155–66.Google Scholar
  39. Rahn O. New principles for the classification of bacteria. Zentralblatt für Bakteriologie, Parasitenkunde, Infektionskrankheiten und Hygiene. Abteilung II. 1937;96:273–86.Google Scholar
  40. Skerman VBD, McGowan V, Sneath PHA. Approved Lists of Bacterial Names. Int J Syst Bacteriol. 1980;30:225–420. PubMed http://dx.doi.org/10.1099/00207713-30-1-225.View ArticleGoogle Scholar
  41. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G. Gene ontology: tool for the unification of biology. Nat Genet. 2000;25:25–9. PubMed http://dx.doi.org/10.1038/75556.View ArticlePubMedPubMed CentralGoogle Scholar
  42. SINA Alignment Service [https://www.arb-silva.de/aligner/]. Accessed 9 Apr 2017.
  43. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011;28:2731–9. PubMed http://dx.doi.org/10.1093/molbev/msr121.View ArticlePubMedPubMed CentralGoogle Scholar
  44. Stothard P, Wishart DS. Circular genome visualization and exploration using CGView. Bioinformatics. 2005;21:537–9. PubMed http://dx.doi.org/10.1093/bioinformatics/bti054.View ArticlePubMedGoogle Scholar

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