International Journal of Systematic and Evolutionary Microbiology (2010), 60, 1999–2005
DOI 10.1099/ijs.0.019323-0
Weissella fabaria sp. nov., from a Ghanaian cocoa
fermentation
Katrien De Bruyne,13 Nicholas Camu,2 Luc De Vuyst2
and Peter Vandamme1
Correspondence
1
Katrien De Bruyne
2
katrien_debruyne@
applied-maths.com
Laboratory of Microbiology, Ghent University, Ledeganckstraat 35, B-9000 Ghent, Belgium
Research Group of Industrial Microbiology and Food Biotechnology (IMDO), Department of
Applied Biological Sciences and Engineering, Vrije Universiteit Brussel, Pleinlaan 2, B-1050
Brussels, Belgium
Two lactic acid bacteria, strains 257T and 252, were isolated from traditional heap fermentations of
Ghanaian cocoa beans. 16S rRNA gene sequence analysis of these strains allocated them to the
genus Weissella, showing 99.5 % 16S rRNA gene sequence similarity towards Weissella
ghanensis LMG 24286T. Whole-cell protein electrophoresis, fluorescent amplified fragment length
polymorphism fingerprinting of whole genomes and biochemical tests confirmed their unique
taxonomic position. DNA–DNA hybridization experiments towards their nearest phylogenetic
neighbour demonstrated that the two strains represent a novel species, for which we propose the
name Weissella fabaria sp. nov., with strain 257T (5LMG 24289T 5DSM 21416T) as the type
strain. Additional sequence analysis using pheS gene sequences proved useful for identification of
all Weissella–Leuconostoc–Oenococcus species and for the recognition of the novel species.
During the main crop of 2004 (October–November 2004),
the microbiota of four spontaneously fermented cocoa
bean heaps in Ghana was studied (Camu et al., 2007, 2008).
Culture-dependent analysis resulted in the isolation of 538
potential lactic acid bacterial (LAB) isolates; subsequent
characterization using both phenotypic and genotypic
methods resulted in 382 LAB. DNA from each isolate
was prepared by alkaline lysis (Coenye et al., 2002) and the
DNA solutions were stored at 220 uC. Dereplication and
preliminary identification of all isolates was achieved by
rep-PCR using the (GTG)5 primer (De Vuyst et al., 2008).
In this analysis, four main clusters of LAB were revealed:
Lactobacillus plantarum, Lactobacillus fermentum, Leuconostoc
pseudomesenteroides and Enterococcus casseliflavus (Camu
et al., 2007). (GTG)5-primed rep-PCR fingerprints revealed
three LAB isolates with fingerprints that differed from those
3Present address: Applied Maths NV, Keistraat 120, B-9830 SintMartens-Latem, Belgium.
Abbreviations: FAFLP, fluorescent amplified fragment length polymorphism; LAB, lactic acid bacteria.
The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene
sequences of strains 257T and 252 are FM179678 and FM179679,
respectively. The accession numbers for the pheS sequences reported in
this paper are FM202093–FM202127, as detailed in Supplementary
Table S1.
16S rRNA gene sequence-based neighbour-joining and maximumlikelihood trees, results of SDS-PAGE profile cluster analysis and details
of strains used in pheS sequencing are available as supplementary
material with the online version of this paper.
019323 G 2010 IUMS
of all known LAB species; these isolates were described
previously as Weissella ghanensis (De Bruyne et al., 2008).
Another two isolates, 257T and 252, occupied a distinct
position in the (GTG)5 fingerprint dendrogram. The clonality
of the two isolates was investigated by RAPD fingerprinting using primers RAPD-270 (59-TGCGCGCGGG-39) and
RAPD-272 (59-AGCGGGCCAA-39), as described previously
(Mahenthiralingam et al., 1996); the fingerprints indicated
that isolates 257T and 252 were genetically different (not
shown), and thus represent two distinct strains.
The taxonomic position of strains 257T and 252 was
investigated by 16S rRNA gene sequence analysis, as
described by De Bruyne et al. (2007). Since the 16S rRNA
gene sequence similarity between the two strains was 100 %,
only the sequence of strain 257T was used for further analysis.
A BLAST search showed 99.5 % 16S rRNA gene sequence
similarity towards two Weissella strains isolated from the
same study and previously described as W. ghanensis (De
Bruyne et al., 2008). 16S rRNA gene sequence similarities
towards other Weissella strains were below 92.2 %. The 16S
rRNA gene sequence obtained (1536 bp) and sequences of
type strains of all established Weissella species were aligned
using the BioNumerics software package, version 5.10
(Applied Maths). Using the maximum-parsimony treebuilding method (Fig. 1), W. ghanensis and strains 257T
and 252 represent a distinct lineage peripheral to the genus
Weissella. The same topology was obtained using neighbourjoining analysis (Supplementary Fig. S1, available in IJSEM
Online). The maximum-likelihood tree (Supplementary
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1999
K. De Bruyne and others
Fig. 1. Maximum-parsimony tree based on
16S rRNA gene sequences showing the
phylogenetic relationships of strain 257T
among other strains of the Leuconostoc–
Weissella–Oenococcus clade. The sequence
of Lactobacillus delbrueckii subsp. delbrueckii
ATCC 9649T was used as the outgroup.
Bootstrap values (%) based on 200 tree
replications are shown at branch points. Bar,
2 % sequence divergence.
Fig. S2) revealed an aberrant topology, placing W. ghanensis
and strains 257T and 252 on a separate clade originating
before the differentiating node that separates the genera
Leuconostoc and Weissella. At present, no explanation has
been found for these distinct topologies. The statistical
reliability of tree topologies was evaluated by bootstrapping
analysis based on 200 tree replications. Because of the high
16S rRNA gene sequence similarity of 99.5 % of strains 257T
and 252 towards W. ghanensis LMG 24285T, DNA–DNA
hybridizations were needed to recognize these strains as a
separate species.
In the present study, another gene phylogeny was studied in
addition to the ambiguous 16S rRNA gene sequence
phylogenies. pheS gene sequences of 29 Weissella and six
Oenococcus strains (Supplementary Table S1) were determined. Amplification and sequencing were performed as
described by De Bruyne et al. (2007). The strength of the use
of pheS gene sequences, i.e. the large discriminatory power
compared with 16S rRNA gene sequences, was confirmed
for members of the Weissella–Leuconostoc–Oenococcus clade.
This is illustrated using the TaxonGap software (Slabbinck et
al., 2008) (Fig. 2), an improved visual method that supports
optimal comparison of different biomarkers. It is clear that
for all species, except for the subspecies of Leuconostoc
mesenteroides (De Bruyne et al., 2007), the interspecies
variation for the pheS gene (represented as dark-grey bars) is
much greater than for the 16S rRNA gene. The name of the
closest neighbour is presented to the right of each dark-grey
bar; in addition, the intraspecies variation (light-grey bars) is
shown for each taxon and biomarker. From this representation, it is clear that subspecies identification for Leuconostoc
2000
mesenteroides strains cannot be achieved through pheS gene
sequence analysis.
In the pheS gene sequence analysis, strains 257T and 252 and
W. ghanensis strains appeared as the most divergent lineage
within Weissella (Fig. 3), confirming the 16S rRNA gene
phylogenies obtained using maximum-parsimony and neighbour-joining analysis. Oenococcus species appeared as an
outgroup to both Leuconostoc and Weissella (Fig. 3). The same
outgroup was found for the majority of gene phylogenies
studied by Chelo et al. (2007). From that study, it was
concluded that Weissella kandleri represents a line that results
from the first divergence within this genus. This conclusion
was based on gene analysis of only six Weissella species. From
the results of the present study, it is demonstrated that strains
257T and 252 and W. ghanensis should be seen as the result of
the first divergent line within the genus Weissella, from both
16S rRNA and pheS gene sequence analyses.
Strains belonging to the same Weissella species shared a pheS
gene sequence similarity of at least 96.8 %, except for
Weissella viridescens strains. To cover the heterogeneity of
this species, four typical W. viridescens strains (LMG 3507T,
LMG 13093, LMG 12021 and LMG 11497) and one
phenotypically and genotypically aberrant strain, 58 (5LMG
23120), confirmed as W. viridescens by DNA–DNA hybridizations by Koort et al. (2006), were included in the study.
Whereas the pheS gene sequence divergence for the restricted
set of four typical W. viridescens strains was minimal (0.7 %),
the sequence similarity of this group towards the pheS gene
sequence of strain LMG 23120 was only 88.8 % (Fig. 3). This
subdivision into two W. viridescens clusters based on pheS
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Weissella fabaria sp. nov.
Fig. 2. TaxonGap output for the Leuconostoc–Weissella–Oenococcus clade, indicating the discriminatory power of the 16S
rRNA and pheS gene sequences. Bars represent intraspecies (light grey) and interspecies (dark grey) variability. For each taxon
and biomarker, the closest neighbour is given on the right. The 16S rRNA gene sequence tree on the left was calculated using
the neighbour-joining algorithm. Bar, 1 % sequence divergence. The biomarker scale represents percentage sequence
variability. L., Leuconostoc; L. mes., Leuconostoc mesenteroides.
gene sequences (Fig. 3) was confirmed by Koort et al. (2006)
with ribotyping results using HindIII.
Genomic DNA of strain 257T and W. ghanensis LMG
24285T was isolated as described by Stackebrandt &
Kandler (1979). DNA–DNA hybridizations were performed using the microplate method, with photobiotin
for labelling of the DNA (Ezaki et al., 1989), as modified by
Goris et al. (1998). The DNA–DNA hybridization between
strain 257T and W. ghanensis LMG 24285T was 41 %,
confirming that strain 257T represents a distinct species.
The G+C content was determined according to the
enzymic DNA degradation method of Mesbah et al.
(1989), using a Waters Breeze HPLC system and XBridge
Shield RP18 column. The solvent used was 0.02 M
NH4H2PO4 (pH 4.0)/1.5 % (v/v) acetonitrile. Non-methylated lambda phage DNA (Sigma) was used as a calibration
reference and Escherichia coli LMG 2093 DNA was included
as a control. The G+C content of strain 257T was
38.2 mol%, which was consistent with the G+C values
observed in the genus Weissella (37–47 mol%) (Björkroth
et al., 2002; Choi et al., 2002; Collins et al., 1993; Lee et al.,
2002; Magnusson et al., 2002; Tanasupawat et al., 2000).
The cell-wall composition was determined as described by
Schleifer (1985), Schleifer & Kandler (1972) and MacKenzie
(1987) with the modification that TLC on cellulose was
applied instead of paper chromatography. The peptidoglycan
structure of strain 257T was determined as L-Lys–L-Ala–L-Ser.
http://ijs.sgmjournals.org
SDS-PAGE of whole-cell proteins (Pot et al., 1994) and
fluorescent amplified fragment length polymorphism
(FAFLP) analysis (Franz et al., 2006) were also performed
to study the proteomic and genetic relatedness of strains
257T and 252 with their nearest neighbours. Data for
reference strains of established species were available from
previous studies (Björkroth et al., 2002; De Bruyne et al.,
2008). The whole-cell protein profile of strain 257T was
different from those of W. ghanensis strains, its nearest
phylogenetic neighbour, and from those of other Weissella
species (Supplementary Fig. S3). Similarly, the unique
taxonomic status of strains 257T and 252 was confirmed by
FAFLP analysis (Fig. 4).
Cell and colony morphology were investigated after
growth on MRS agar (pH 5.4; Oxoid) and 48 h of aerobic
incubation at 28 uC, unless stated otherwise. Conventional biochemical and growth characteristics, carbohydrate fermentation tests and enzyme activities were tested
as described by De Bruyne et al. (2008). For detection of
glucose metabolites and the proportion of D- and Llactate, strains were grown at 30 uC in MRS broth
(pH 5.4; Oxoid) for 24 h. The production of dextran
was observed on MRS agar in which glucose had been
replaced with 5 % sucrose. The results are given in the
species description. Characteristics that differentiate strain
257T and 252 from other Weissella species are summarized
in Table 1.
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K. De Bruyne and others
Fig. 3. Phylogenetic neighbour-joining tree
based on pheS gene sequences showing the
phylogenetic relationships of strains 257T and
252 among other strains of the Leuconostoc–
Weissella–Oenococcus clade. Individual sequences for Weissella and Oenococcus
strains are presented whereas, for Leuconostoc
strains, sequences are grouped in species
clusters. See De Bruyne et al. (2007) for
accession numbers of sequences from
Leuconostoc strains. The Oenococcus strains
were used as an outgroup. Bar, 5 % sequence
divergence.
The results from the present study demonstrate that strains
257T and 252 are closely related to W. ghanensis strains
(99.5 % 16S rRNA gene sequence similarity) but that they
can be distinguished from W. ghanensis and other Weissella
species by DNA–DNA hybridization, SDS-PAGE of wholecell proteins, AFLP analysis, pheS gene sequence analysis and
biochemical characteristics. Although the phylogenetic
analyses were not unambiguous, we describe the novel
species represented by strains 257T and 252 as the nearest
neighbour of W. ghanensis, the two representing a peripheral
position in 16S rRNA gene sequence-based maximumparsimony (Fig. 1) and neighbour-joining (Supplementary
Fig. S1) trees. Because of the close relationship between W.
ghanensis strains and strains 257T and 252, the latter would
be expected to meet the characteristics of the genus. The
2002
heterofermentative metabolism of the strains, their colony
and cell morphology, motility, catalase activity, arginine
hydrolysis and G+C content are in agreement with the
description of the genus Weissella (Collins et al., 1993). Based
on these biochemical characteristics and 16S rRNA and pheS
gene sequence analysis, the assignment of these strains to a
novel Weissella species is justified. Therefore, we propose to
classify the two strains as strains of Weissella fabaria sp. nov.
Description of Weissella fabaria sp. nov.
Weissella fabaria (fa.ba9ri.a. L. fem. adj. fabaria of or
belonging to beans).
Cells are Gram-stain-positive, catalase-negative, facultatively anaerobic and non-motile. The cells are coccoid,
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Weissella fabaria sp. nov.
Fig. 4. FAFLP patterns and dendrogram based on UPGMA linkage of Dice coefficients of strain 257T and reference strains
from all established Weissella species.
approximately 1.0 mm wide and 1.5 mm long, and occur
singly, in pairs or in short chains. Colonies grown for
2 days on MRS agar at 30 uC are approximately 1 mm in
diameter, beige, opaque, smooth and circular with a low-
convex elevation. Lactic acid, ethanol, acetic acid and
CO2 are detected after growth on glucose, indicating the
heterofermentative character of the strains. Both known
strains produce the D- and L-isomers of lactic acid in a ratio
Table 1. Differential characteristics of Weissella fabaria sp. nov. 257T and other Weissella species
Species: 1, W. fabaria sp. nov.; 2, W. ghanensis; 3, W. halotolerans; 4, W. minor; 5, W. viridescens; 6, W. soli; 7, W. kandleri; 8, W. koreensis; 9, W.
cibaria; 10, W. confusa; 11, W. thailandensis; 12, W. hellenica; 13, W. paramesenteroides. +, 90 % or more strains positive; 2, 90 % or more strains
negative; d, 11–89 % of strains positive; ND, no data available. Data partially adapted from Collins et al. (1993), Tanasupawat et al. (2000), Björkroth
et al. (2002), Lee et al. (2002), Magnusson et al. (2002) and De Bruyne et al. (2008).
Characteristic
Acid from:
Arabinose
Cellobiose
Fructose
Galactose
Maltose
Melibiose
Raffinose
Ribose
Salicin
Sucrose
Trehalose
Xylose
Hydrolysis of aesculin
NH3 from arginine
Dextran formation
Lactic acid configuration
Growth at/in:
15 uC
37 uC
42 uC
6.5 % NaCl
8 % NaCl
10 % NaCl
DNA G+C content (mol%)
http://ijs.sgmjournals.org
1
2
3
4
5
6
7
8
9
10
11
12
13
2
+
+
2
2
2
2
2
2
2
+
2
+
+
+
2
+
+
2
+
2
2
2
+
d
+
2
+
+
+
2
2
+
2
+
2
2
+
2
2
2
2
2
+
2
2
+
2
+
2
2
2
2
d
d
2
2
2
2
2
+
+
2
2
2
+
2
2
2
2
2
+
+
2
2
+
2
+
+
+
+
+
2
+
2
2
2
+
+
2
+
+
+
+
2
+
+
+
+
2
2
+
+
+
2
+
+
+
+
+
2
+
+
+
+
+
+
2
d
d
2
2
2
2
+
2
+
2
+
2
2
2
2
+
+
2
ND
+
2
2
2
+
+
+
+
+
+
+
+
+
+
2
+
2
ND
2
+
+
2
+
2
2
+
2
+
+
2
+
+
2
2
2
d
d
+
+
+
+
d
d
2
+
+
d
d
2
2
DL
DL
DL
DL
DL
D
DL
D
DL
DL
D
D
D
+
+
2
2
2
2
38
+
+
2
2
2
2
40
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
44
44
41–44
43
39
2
2
37
+
+
+
+
2
2
44–45
ND
ND
+
+
2
ND
ND
+
+
2
ND
ND
ND
ND
ND
2
2
2
2
+
ND
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ND
+
2
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
2
45–47
+
38–41
2
39–40
2
37–38
2003
K. De Bruyne and others
of approximately 9 : 1. Growth is observed at 15–37 uC and
at pH 5.0–9.0. No growth is obtained in the presence of
5 % NaCl. Both known strains produce slime from glucose
and hydrolyse arginine. Acid is produced from glucose,
fructose, mannose, mannitol, N-acetylglucosamine, aesculin, cellobiose, trehalose and gentiobiose. Acid is not
produced from glycerol, erythritol, D- or L-arabinose,
ribose, D- or L-xylose, adonitol, methyl b-D-xyloside,
galactose, sorbose, rhamnose, dulcitol, inositol, sorbitol,
methyl a-D-mannoside, methyl a-D-glucoside, amygdalin,
arbutin, salicin, maltose, lactose, melibiose, sucrose, inulin,
melezitose, raffinose, starch, glycogen, xylitol, turanose,
D-lyxose, D-tagatose, D- or L-fucose, D- or L-arabitol,
gluconate, 2-ketogluonate or 5-ketogluconate. The peptidoglycan structure contains L-Lys–L-Ala–L-Ser. The DNA
G+C content of the type strain is 38.2 mol%.
Coenye, T., Spilker, T., Martin, A. & LiPuma, J. J. (2002). Comparative
assessment of genotyping methods for epidemiologic study of
Burkholderia cepacia genomovar III. J Clin Microbiol 40, 3300–
3307.
Collins, M. D., Samelis, J., Metaxopoulos, J. & Wallbanks, S. (1993).
Taxonomic studies on some Leuconostoc-like organisms from
fermented sausages: description of a new genus Weissella for the
Leuconostoc paramesenteroides group of species. J Appl Bacteriol 75,
595–603.
De Bruyne, K., Schillinger, U., Caroline, L., Boehringer, B.,
Cleenwerck, I., Vancanneyt, M., De Vuyst, L., Franz, C. M. A. P. &
Vandamme, P. (2007). Leuconostoc holzapfelii sp. nov., isolated from
Ethiopian coffee fermentation and assessment of sequence analysis of
housekeeping genes for delineation of Leuconostoc species. Int J Syst
Evol Microbiol 57, 2952–2959.
De Bruyne, K., Camu, N., Lefebvre, K., De Vuyst, L. & Vandamme, P.
(2008). Weissella ghanensis sp. nov., isolated from a Ghanaian cocoa
fermentation. Int J Syst Evol Microbiol 58, 2721–2725.
The type strain, 257T (5LMG 24289T 5DSM 21416T), was
isolated from a Ghanaian cocoa fermentation. The two
known strains originated from a single cocoa heap
fermentation in New Tafo, Ghana, in 2004.
De Vuyst, L., Camu, N., De Winter, T., Vandemeulebroecke, K., Van
de Perre, V., Vancanneyt, M., De Vos, P. & Cleenwerck, I. (2008).
Acknowledgements
Ezaki, T., Hashimoto, Y. & Yabuuchi, E. (1989). Fluorometric
This work was supported by the Federal Research Policy [Action for
the Promotion of and Cooperation with the Belgian Coordinated
Collections of Microorganisms (C3/00/17)], the Research Council of
the Vrije Universiteit Brussel (GOA project), the Institute for the
Promotion of Innovation through Science and Technology in
Flanders (IWT Project 040043) and Barry Callebaut N.V.
The cooperation of the Ghanaian Cocoa Producers’ Alliance
(COCOBOD, Accra, Ghana) and the Cocoa Research Institute of
Ghana is highly appreciated. Approval was obtained from
COCOBOD to cooperate with local farmers.
Validation of the (GTG)5-rep-PCR fingerprinting technique for rapid
classification and identification of acetic acid bacteria, with a focus on
isolates from Ghanaian fermented cocoa beans. Int J Food Microbiol
125, 79–90.
deoxyribonucleic acid-deoxyribonucleic acid hybridization in microdilution wells as an alternative to membrane filter hybridization in
which radioisotopes are used to determine genetic relatedness among
bacterial strains. Int J Syst Bacteriol 39, 224–229.
Franz, C. M. A. P., Vancanneyt, M., Vandemeulebroecke, K., De
Wachter, M., Cleenwerck, I., Hoste, B., Schillinger, U., Holzapfel,
W. H. & Swings, J. (2006). Pediococcus stilesii sp. nov., isolated from
maize grains. Int J Syst Evol Microbiol 56, 329–333.
Goris, J., Suzuki, K., De Vos, P., Nakase, T. & Kersters, K. (1998).
Evaluation of a microplate DNA-DNA hybridization method
compared with the initial renaturation method. Can J Microbiol 44,
1148–1153.
Koort, J., Coenye, T., Santos, E. M., Molinero, C., Jaime, I., Rovira, J.,
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