Open Access

Complete genome sequence of Leuconostoc suionicum DSM 20241T provides insights into its functional and metabolic features

  • Byung Hee Chun1,
  • Se Hee Lee2,
  • Hye Hee Jeon1,
  • Dong-Woon Kim3 and
  • Che Ok Jeon1Email author
Contributed equally
Standards in Genomic Sciences201712:38

https://doi.org/10.1186/s40793-017-0256-0

Received: 11 May 2017

Accepted: 12 July 2017

Published: 17 July 2017

Abstract

The genome of Leuconostoc suionicum DSM 20241T (=ATCC 9135T = LMG 8159T = NCIMB 6992T) was completely sequenced and its fermentative metabolic pathways were reconstructed to investigate the fermentative properties and metabolites of strain DSM 20241T during fermentation. The genome of L. suionicum DSM 20241T consists of a circular chromosome (2026.8 Kb) and a circular plasmid (21.9 Kb) with 37.58% G + C content, encoding 997 proteins, 12 rRNAs, and 72 tRNAs. Analysis of the metabolic pathways of L. suionicum DSM 20241T revealed that strain DSM 20241T performs heterolactic acid fermentation and can metabolize diverse organic compounds including glucose, fructose, galactose, cellobiose, mannose, sucrose, trehalose, arbutin, salcin, xylose, arabinose and ribose.

Keywords

Leuconostoc suionicum Complete genome Lactic acid bacteria KEGG Fermentative metabolic pathway

Introduction

The genus Leuconostoc comprises Gram-positive, facultatively anaerobic, intrinsically vancomycin-resistant, catalase-negative, spherical heterofermentative lactic acid bacteria which are involved in the fermentation of plant materials (such as kimchi), dairy products, meats, vegetable sausages and beverages [17]. Strain DSM 20241 T (=ATCC 9135 T =LMG 8159 T =NCIMB 6992 T) of the genus Leuconostoc was isolated in Sweden in 1972. It was originally classified as a subspecies of L. mesenteroides , but was recently reclassified as a novel species – L. suionicum –based on its whole genome sequence [4]. Here, we present the taxonomic and genomic features of L. suionicum DSM 20241 T. In addition, we investigated the metabolic properties of L. suionicum DSM 20241 T and reconstructed the metabolic pathways of organic compounds to estimate the fermentative metabolites in L. suionicum DSM 20241 T.

Organism information

Classification and features

L. suionicum DSM 20241 T belongs to the family Leuconostocaceae , order Lactobacillales , class Bacilli and phylum Firmicutes . Strain DSM 20241 T is a Gram-positive, facultatively anaerobic, non-motile, non-sporulating, catalase-negative coccus, with a diameter of 0.5–0.7 μm (Fig. 1). It can be grown in MRS broth at 10–40 °C, with an optimal growth temperature of 30 °C [4]. Strain DSM 20241 T ferments a wide variety of carbon sources including d-glucose, arbutin, melibiose, sucrose, turanose, N-acetylglucosamine, cellobiose, galactose, gentiobiose, amygdalin, l-arabinose, esculin, ferric citrate, d-fructose, d-mannose, lactose, maltose, methyl α-d-glucopyranoside, salicin, trehalose, d-xylose, potassium 5-ketogluconate, mannitol and ribose to produce gas and acids (Table 1); however, it does not ferment glycerol, erythritol, d-arabinose, l-xylose, d-adonitol, methyl β-d-xylopyranoside, l-sorbose, methyl α-d-mannopyranoside, l-rhamnose, dulcitol, inositol, d-sorbitol, inulin, d-melezitose, starch, glycogen, xylitol, d-lyxose, d-tagatose, fucose, d-arabitol, l-arabitol, potassium gluconate, potassium 2-ketogluconate or raffinose [4, 8].
Fig. 1

Transmission electron micrograph showing the general cell morphology of Leuconostoc suionicum DSM 20241T. The bacterial cells were stained by uranyl acetate and examined using transmission electron microscopy (JEM-1010; JEOL)

Table 1

Classification and general features of Leuconostoc suionicum DSM 20241T according to MIGS recommendations [9]

MIGS ID

Property

Term

Evidence codea

 

Classification

Domain Bacteria

TAS [31]

  

Phylum Firmicutes

TAS [32, 33]

  

Class Bacilli

TAS [34]

  

Order Lactobacillales

TAS [35]

  

Family Leuconostocaceae

TAS [35]

  

Genus Leuconostoc

TAS [3638]

  

Species Leuconostoc suionicum

TAS [4]

  

Type strain DSM 20241T

TAS [4]

 

Gram stain

Positive

TAS [8]

 

Cell shape

Coccus

TAS [8]

 

Motility

Non-motile

NAS

 

Sporulation

Non-sporulating

TAS [8]

 

Temperature range

10–40 °C

TAS [4]

 

Optimum temperature

30 °C

TAS [4, 8]

 

pH range; Optimum

Not reported

 
 

Carbon source

l-arabinose, ribose, d-xylose, galactose, glucose, fructose, mannose, methyl α-d-glucopyranoside, N-acetylglucosamine, amygdalin, arbutin, aesculin, salicin, cellobiose, maltose, melibiose, sucrose, trehalose, gentiobiose and turanose

TAS [4, 8]

MIGS-6

Habitat

Not reported

 

MIGS-6.3

Salinity

Not reported

 

MIGS-22

Oxygen requirement

Facultatively anaerobic

TAS [8]

MIGS-15

Biotic relationship

Free-living

NAS

MIGS-14

Pathogenicity

Not reported

NAS

MIGS-4

Geographic location

Sweden

TAS [8]

MIGS-5

Sample collection

1972

TAS [8]

MIGS-4.1

Latitude

Not reported

 

MIGS-4.2

Longitude

Not reported

 

MIGS-4.4

Altitude

Not reported

 

aEvidence 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 [cite this reference]

Phylogenetic analysis using the 16S rRNA gene sequences with validated type strains showed that L. suionicum DSM 20241 T is most closely related to the subspecies of the species L. mesenteroides : L. mesenteroides subsp. mesenteroides , L. mesenteroides subsp. jonggajibkimchii , L. mesenteroides subsp. cremoris , and L. mesenteroides subsp. dextranicum with very high 16S rRNA gene sequence similarities (>99.73%; Fig. 2).
Fig. 2

Neighbor-joining tree based on the 16S rRNA gene sequences showing the phylogenetic relationships between Leuconostoc suionicum DSM 20241T (highlighted in bold) and closely related Leuconostoc species. The sequences were aligned using the fast secondary-structure aware Infernal aligner available from the Ribosomal Database Project [28] and the tree was constructed based on the neighbor-joining algorithm using PHYLIP software (ver. 3.68) [29]. Bootstrap values of over 70% are shown on the nodes as percentages of 1000 replicates. Weissella viridescens 1536T (AB023236) was used as an outgroup (not shown). Bar indicates 0.01 changes per nucleotide position

Genome sequencing information

Genome project history

L. suionicum DSM 20241 T was selected owing to its taxonomic significance for the species L. mesenteroides and was obtained from the German Collection of Microorganisms and Cell Cultures. The complete sequences of the chromosome and plasmid of strain DSM 20241 T were deposited in GenBank with the accession numbers CP015247–48. The project information and its association with MIGS version 2.0 [9] are summarized in Table 2.
Table 2

Genome sequencing project information for Leuconostoc suionicum DSM 20241T

MIGS ID

Property

Term

MIGS 31

Finishing quality

Complete

MIGS-28

Libraries used

PacBio 10-kb SMRT-bell library

MIGS 29

Sequencing platforms

PacBio RS SMRT

MIGS 31.2

Fold coverage

50 ×

MIGS 30

Assemblers

RS_HGAP Assembly.3

MIGS 32

Gene calling method

NCBI Prokaryotic Genome, Annotation Pipeline

 

Locus Tag

A6B45

 

GenBank ID

CP015247-CP015248

 

GenBank Date of Release

14-APR-2017

 

GOLD ID

Ga0151201

 

BIOPROJECT

PRJNA318320

MIGS 13

Source Material Identifier

DSM 20241T/ ATCC 9135T/LMG 8159T/NCIMB 6992T

 

Project relevance

Taxonomy, industry, fermentation

Growth conditions and genomic DNA preparation

L. suionicum DSM 20241 T was cultured in MRS broth (BD Biosciences, CA, USA) at 30 °C for 24 h until the early stationary phase. Genomic DNA was extracted according to a standard phenol-chloroform extraction and ethanol precipitation procedure [10]. DNA quality (OD260/OD280 > 1.8) and concentration were measured using a NanoDrop ND-1000 spectrophotometer (Synergy Mx, Biotek, VT, USA).

Genome sequencing and assembly

The genome of strain DSM 20241 T was sequenced using PacBio RS SMRT technology based on a 10-kb SMRT-bell library at Macrogen (Seoul, Korea) as previously described [10]; 138,738 high-quality reads were generated, with an average length of 7656 bp. De novo assembly of sequencing reads derived from PacBio SMRT sequencing was performed using the hierarchical genome assembly process (HGAP; ver. 3.0) [11], which yielded a circular chromosome (2,026,850 bp) and a circular plasmid (21,983 bp) (Fig. 3).
Fig. 3

Graphical maps of the Leuconostoc suionicum DSM 20241T chromosome and plasmid. The circular maps were set up by the CGView Server [30]. From the outside to the center: Genes on forward strand (colored by COG categories), genes on reverse strand (colored by COG categories), GC content (in black) and GC skews, where green indicates positive values and magenta indicates negative values

Genome annotation

Automated genome annotation of strain DSM 20241 T was performed using Prodigal as part of the Joint Genome Institute’s microbial genome annotation pipeline [12]. In addition, predicted coding sequences were functionally annotated using the NCBI non-redundant database, UniProt, TIGR-Fam, Pfam, PRIAM, Kyoto Encyclopedia of Genes and Genomes, Clusters of Orthologous Groups, and InterPro. Structural RNA genes were identified by using HMMER 3.0rc1 (rRNAs) [13] and tRNAscan-SE 1.23 (tRNAs) [14]. Other non-coding genes were searched using INFERNAL 1.0.2 [15]. Additional annotation was performed within the Integrated Microbial Genomes—Expert Review platform [16].

Genome properties

The complete genome of L. suionicum strain DSM 20241 T consists of a circular chromosome (2,026,850 bp) and a circular plasmid (21,983 bp) with 37.6% and 37.0% G + C contents, respectively (Table 3). The genome contains 1997 protein coding genes and 93 RNA genes (72 tRNAs, 12 rRNAs and 9 other RNAs; Table 4). Additional genome statistics and the distribution of the genes into COG functional categories are presented in Tables 4 and 5, respectively.
Table 3

Sequence features of chromosome and plasmid present in the L. suionicum DSM 20241T genome

Label

Size (bp)

Topology

Coding gene sequences (bp)

G + C content (%)

INSDC identifier

Chromosome

2,026,850

Circular

1,758,165

37.6

CP015247.1

Plasmid

21,983

Circular

14,895

37.0

CP015248.1

Table 4

Genome statistics

Attribute

Value

% of Total

Genome size (bp)

2,048,833

100.00

DNA coding (bp)

1,835,796

89.60

DNA G + C (bp)

769,980

37.58

DNA scaffolds

2

100.00

Total genes

2090

100.00

Protein coding genes

1997

95.55

RNA genes

93

4.45

Pseudo genes

0

Genes in internal clusters

381

18.23

Genes with function prediction

1641

78.52

Genes assigned to COGs

1483

70.96

Genes with Pfam domains

1695

81.10

Genes with signal peptides

31

1.48

Genes with transmembrane helices

592

28.33

CRISPR repeats

0

Table 5

Number of genes associated with general COG functional categories

Code

Value

%age

Description

J

176

7.91

Translation, ribosomal structure and biogenesis

A

0

0.00

RNA processing and modification

K

116

5.21

Transcription

L

83

3.73

Replication, recombination and repair

B

0

0.00

Chromatin structure and dynamics

D

25

1.12

Cell cycle control, Cell division, chromosome partitioning

V

34

1.53

Defense mechanisms

T

53

2.38

Signal transduction mechanisms

M

93

4.18

Cell wall/membrane biogenesis

N

11

0.49

Cell motility

U

14

0.63

Intracellular trafficking and secretion

O

55

2.47

Posttranslational modification, protein turnover, chaperones

C

53

2.38

Energy production and conversion

G

146

6.56

Carbohydrate transport and metabolism

E

179

8.04

Amino acid transport and metabolism

F

85

3.82

Nucleotide transport and metabolism

H

98

4.40

Coenzyme transport and metabolism

I

65

2.92

Lipid transport and metabolism

P

81

3.64

Inorganic ion transport and metabolism

Q

27

1.21

Secondary metabolites biosynthesis, transport and catabolism

R

127

5.71

General function prediction only

S

98

4.40

Function unknown

-

607

27.27

Not in COGs

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

Insights from the genome sequence

KEGG metabolic and regulatory pathways

The KEGG metabolic pathways of L. suionicum DSM 20241 T show that strain DSM 20241 T displays typical heterolactic acid fermentative capabilities, performing pentose phosphate metabolism, fructose and mannose metabolism, galactose metabolism, sucrose metabolism and pyruvate metabolism without the complete tricarboxylic acid cycle (Fig. 4a, see Additional file 1: Table S1) [1719]. In addition, L. suionicum DSM 20241 T harbors genes related to riboflavin metabolism, fatty acid biosynthesis, purine and pyrimidine metabolism and amino acid biosynthesis (Fig. 4a). The regulatory pathways of strain DSM 20241 T indicate that it contains various phospho transferase systems, such as a sucrose-specific EII component (K02808, K02809 and K02810), a β-glucoside β-glucoside-specific EII component (K02755, K02756 and K02757), a cellobiose-specific EII component (K02759, K02760 and K02761), a mannose-specific EII component (K02793, K02794, K02795 and K02796) and an l-ascorbate-specific EII component (K02821, K02822 and K03475) (Fig. 4b), suggesting that strain DSM 20241 T possesses the ability to ferment various carbon sources.
Fig. 4

KEGG metabolic (a) and regulatory (b) pathways of Leuconostoc suionicum DSM 20241T . The pathways were generated using the iPath v2 module based on KEGG Orthology numbers of genes identified from the genome of L. suionicum DSM 20241T

Carbon metabolic pathways

To investigate the fermentative metabolic properties of L. suionicum DSM 20241 T, metabolic pathways of various carbon sources were reconstructed based on predicted KEGG pathways and BLASTP analysis using reference protein sequences (Fig. 5). The predicted metabolic pathways identified motifs associated with the pentose phosphate pathway, fructose and mannose metabolism, galactose metabolism, sucrose metabolism, pyruvate metabolism, partial TCA cycle and incomplete glycolysis pathway in the genome of L. suionicum DSM20241 T, indicating that this strain performs typical heterolactic acid fermentation to produce lactate, ethanol and carbon dioxide (Fig. 5, Additional file 1: Table S1). It has been reported that mannitol, an important refreshing sweet agent in fermented vegetable foods such as sauerkraut, pickles and kimchi, is synthesized through fructose reduction by mannitol dehydrogenase (EC 1.1.1.67) through the consumption of NADH [20, 21]. The predicted metabolic pathways indicate that L. suionicum DSM 20241 T produces ethanol via the reduction of acetyl phosphate through the consumption of NADH; this strain may also produce acetate instead of ethanol due to the lack of NADH when the strain produces mannitol from fructose [21]. L. suionicum DSM 20241 T harbors genes related to diverse PTSs or permeases that transport various glycosides or sugars including d-glucose, d-fructose, sucrose, d-mannose, trehalose, arbutin, salcin, cellobiose, d-xylose, arabinose, and d-ribose; this indicates that L. suionicum DSM 20241 T has versatile metabolic capabilities. d-lactate and l-lactate are produced from the reduction of pyruvate by d-lactate dehydrogenase (EC 1.1.1.28) and l-lactate dehydrogenase (EC 1.1.1.27), respectively. L. suionicum DSM 20241 T harbors four copies of d-lactate dehydrogenase (locus tags: Ga0151201_111849, Ga0151201_112070, Ga0151201_11385 and Ga0151201_111758) and one copy of l-lactate dehydrogenase (locus tag: Ga0151201_1175), suggesting that L. suionicum DSM 20241 T may produce more d-lactate than l-lactate; this is similar to other members of the genus Leuconostoc , which have been shown to produce more d-lactate than l-lactate under laboratory conditions [4, 2225]. The predicted metabolic pathways show that L. suionicum DSM 20241 T produces diacetyl and acetoin, which are known as butter flavors in dairy products [26, 27]. Acetolactate synthase (EC 2.2.1.6) produces 2-acetolactate from pyruvate and converts it into deacetyl and CO2, which is emitted as a byproduct. Furthermore, 2-acetoin is produced from 2-acetolactate and diacetyl (acetolactate decarboxylase, EC 4.1.1.5; diacetyl reductase, EC 1.1.1.304, respectively); but 2-acetoin is eventually converted to 2,3-butanediol, which lacks the butter flavoring property. In addition, the predicted metabolic pathways show that L. suionicum DSM 20241 T uses dextransucrase (EC 2.4.1.5) to produce dextran, a homopolysaccharide of glucose.
Fig. 5

Predicted fermentative metabolic pathways of various carbon compounds in Leuconostoc suionicum DSM 20241T during fermentation. PTS, phosphotransferase system; UDP, uridine diphosphate

Conclusions

In this study, the complete genome of L. suionicum DSM 20241 T, consisting of a circular chromosome and a circular plasmid, was obtained by whole-genome sequencing using the PacBio SMRT sequencing system and de novo assembly using the HGAP method. In addition, the metabolic pathways of organic compounds in L. suionicum DSM 20241 T were reconstructed to estimate its fermentative properties and metabolites. The metabolic pathways show that strain DSM 20241 T performs typical heterolactic acid fermentations to produce lactate, ethanol and carbon dioxide and contains genes encoding various PTSs, permeases, and other enzymes to metabolize various organic compounds. In addition, strain DSM 20241 T synthesizes mannitol to produce acetate instead of ethanol through heterolactic acid fermentation, and produces butter flavoring compounds. The complete genome and reconstructed metabolic pathways of L. suionicum DSM 20241 T provide important insights into its functional and metabolic features during fermentation.

Notes

Abbreviations

COG: 

Clusters of orthologous groups

KEGG: 

Kyoto Encyclopedia of Genes and Genomes

PTS: 

Phosphotransferase system

SMRT: 

Single molecule real-time

TCA: 

Tricarboxylic acid

Declarations

Funding

This work was supported the “Cooperative Research Program for Agriculture Science & Technology Development (Project No. PJ01090604)” of Rural Development Administration and the World Institute of Kimchi funded by the Ministry of Science, ICT and Future Planning (KE1702–2), Republic of Korea.

Authors’ contributions

BHC and HHJ assembled the sequencing data and completed the genome analysis; SHL and HHJ performed the microbiological studies and obtained the organism information; BHC, SHL and DWK analyzed the genome sequence informatically; BHC and COJ 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)
Department of Life Science, Chung-Ang University
(2)
Microbiology and Functionality Research Group, World Institute of Kimchi
(3)
Animal Nutrition and Physiology Team, National Institute of Animal Science, RDA

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