Food Research International 40 (2007) 539–558

www.elsevier.com/locate/foodres

Review

Lactobacilli in sourdough fermentation

Aldo Corsetti *, Luca Settanni
Dipartimento di Scienze degli Alimenti, Sezione di Microbiologia Agro-Alimentare ed Ambientale,
Università degli Studi di Teramo, V.C.R. Lerici 1, 64023 Mosciano Sant’Angelo (TE), Italy

Received 1 August 2006; accepted 5 November 2006

Abstract

Sourdough technology is widely used; it is employed in bread making and for the production of cakes. Sourdough is characterized by
a complex microbial ecosystem, mainly represented by lactic acid bacteria and yeasts, whose fermentation confers to the resulting bread
its characteristic features such as palatability and high sensory quality. Investigation of the microbial composition of sourdough is rel-
evant in order to determine the potential activities of sourdough microorganisms. This review focuses on the role of the most important
group of sourdough fermenting bacteria that consists of lactobacilli; species that belong to the Lactobacillus genus are the main respon-
sible of flavor development, improvement of nutritional quality as well as stability over consecutive refreshments of sourdough. Lacto-
bacilli also establish some durable microbial associations. An overview of the tools for monitoring predominant species is also reported.
 2006 Elsevier Ltd. All rights reserved.

Keywords: Antimicrobial substances; Healthy aspects; Lactobacillus; Microbial monitoring; Nutritional quality; Sourdough

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 540
2. Sourdough fermenting microorganisms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 540
2.1. Dominating lactobacilli in sourdough . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 542
2.2. Microbial interactions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 544
3. Useful propreties of sourdough lactobacilli . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 545
3.1. Contribution of lactobacilli to flavour development . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 545
3.2. Contribution of lactobacilli to dough structure . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 546
3.3. Lactobacilli as organisms to improve nutritional quality and healthy aspects of sourdough . . . . . . . . . . . . . . . . . . 546
3.3.1. Reduction of antinutritional factors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 547
3.3.2. Conversion of toxic compounds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 547
3.4. Antimicrobial substances produced by sourdough lactobacilli . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 548
3.4.1. Bacteriocins. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 548
3.4.2. Antifungal compounds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 549
3.4.3. Other antimicrobial compounds. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 550
4. Monitoring of lactobacilli dynamics during sourdough fermentation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 550
5. Concluding remarks . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 552
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 552

*
Corresponding author. Tel.: +39 (0) 861 266896; fax: +39 (0) 85 8071509.
E-mail address: acorsetti@unite.it (A. Corsetti).

0963-9969/$ - see front matter  2006 Elsevier Ltd. All rights reserved.
doi:10.1016/j.foodres.2006.11.001
540 A. Corsetti, L. Settanni / Food Research International 40 (2007) 539–558
1. Introduction
Dry cereals can only be eaten after grinding and mixing
with water (Salovaara, 1998). Such a mixture, resulting in
the formation of a dough characterized by sour aroma
when left on its own for a while, may have been the first
example of fermented food employed by mankind (Ham-
mes & Gänzle, 1998). The first evidence of baking of leav-
ened dough are dated at around 1500 BC by mural
Egyptian paintings (von Stokar, 1956), although sour-
dough bread was already part of the European diet 5000
years ago (Währen, 1985). Sourdough was used as a lea-
vening agent in bread production until it was replaced by
baker’s yeast in the 19th century; from then on its use
was reduced to artisan and rye bread. Nowadays, sour-
dough is employed in the manufacture of a variety of prod-
ucts such as breads, cakes and crackers, with its application
still being on the increase (De Vuyst & Gänzle, 2005;
Foschino, Terraneo, Mora, & Galli, 1999; Ottogalli, Galli,
& Foschino, 1996; Vogel et al., 1999) while being applied to
a large variety of cereal flours throughout the world. Wheat
sourdough is used in more than 30% of Italian bakery
products (Ottogalli et al., 1996), including more than 200
different types of sourdough breads (INSOR, 2000). Some
regions of southern Italy, such as Apulia, produces sour-
dough breads mostly from wheat flour species Triticum
durum instead of the common species Triticum aestivum
used in several other Italian regions (Corsetti et al.,
2001). Rye as cereal for bread making is widely used in
Germany, Poland, Russia and Scandinavian countries
(Bushuk, 2001).
Study of sourdough from a microbiological point of
view barely started a hundred years ago (Salovaara,
1998). Sourdough is reported to be a dough whose typical
characteristics are mainly due to its microflora, basically
represented by lactic acid bacteria (LAB) and yeasts.
Thanks to its microbial community such a dough is meta-
bolically active and can be reactivated. Sourdough micro-
organisms ensure acid production and leavening upon
addition of flour and water (Anon., 1994). Since flour can-
not be subjected to heat-sterilization, the occurrence and
number of certain types of microorganisms will strictly
depend on a combination of available substrates and spe-
cific technological parameters (Salovaara, 1998). Sour-
doughs, on the basis of the technology applied, have been
grouped into three types (Böcker, Stolz, & Hammes,
1995): type I, type II and type III (Fig. 1). Type I sour-
doughs are produced with traditional techniques and are
characterized by continuous, daily refreshments to keep
the microorganisms in an active state. Type II sourdoughs,
often used as dough-souring supplements during bread
preparation, are semi-fluid silo preparations characterized
by long fermentation periods (from 2 up to 5 days) and fer-
mentation temperature sometimes >30 C to speed up the
process (Böcker et al., 1995; Hammes & Gänzle, 1998).
Type III sourdoughs are dried preparations containing
LAB resistant to the drying process (Hammes & Gänzle,
Type I Type II Type III
Traditional proces
process Industrial process Industrial process
Flour, H2O, Sourdough, (NaCl, sugar)
mixing Liquid Dried
fermentation at RT
final pH ca. 4.0
Pugliese, Toscano,
and Altamura bread
Italian Panettone, Pandoro
and Colomba
San Francisco sourdough
French bread
Fig. 1. Scheme of sourdough production processes.
1998). Unlike type I sourdoughs, doughs of types II and
III require the addition of baker’s yeast (Saccharomyces
cerevisiae) as leavening agent.
The modern biotechnology of baked goods largely uses
sourdough as a natural leavening agent because of the
many advantages it offers over baker’s yeast, e.g. in the
development of the characteristic flavour of bread, result-
ing in a final product with high sensory quality (Hansen
& Hansen, 1996). Many inherent properties of sourdough
rely on the metabolic activities of its resident LAB: lactic
fermentation, proteolysis, synthesis of volatile compounds,
anti-mould and antiropiness are among the most important
activities during sourdough fermentation (Gobbetti, 1998;
Hammes & Gänzle, 1998). Moreover, endogenous factors
in cereal products (carbohydrates, nitrogen sources, miner-
als, lipids and free fatty acids, and enzyme activities) and
process parameters (temperature, dough yield, oxygen, fer-
mentation time and number of sourdough propagation
steps) markedly influence the microflora of sourdough
and the features of leavened baked goods (Hammes &
Gänzle, 1998).
2. Sourdough fermenting microorganisms
In contrast to the use of mostly homofermentative spe-
cies of LAB in the majority of (fermented) food applica-
tions, heterofermentative species play a major role in
sourdough fermentation (Salovaara, 1998), especially when
sourdoughs are prepared in a traditional manner (Corsetti
et al., 2003; Corsetti et al., 2001). So far, a few less than 50
different species of LAB isolated from sourdough have
been reported (Hammes et al., 2005), some of which, e.g.
Lactobacillus reuteri and Lactobacillus acidophilus, may
be of intestinal origin and, due to cross-contamination,
are found in sourdoughs (Gänzle, oral communication).
 A. Corsetti, L. Settanni / Food Research International 40 (2007) 539–558 541

Although species belonging to Leuconostoc, Weissella, Ped- Table 1

iococcus, Lactococcus, Enterococcus and Streptococcus gen- Lactobacillus species generally associated with sourdough fermentation or
found in fermented sourdough
era have been isolated from sourdough, Lactobacillus strains
are the most frequently observed bacteria in this ecosys- Obligately Facultatively Obligately
heterofermentative heterofermentative homofermentative
tems. The recently described species Lactobacillus frumenti
(Müller, Ehrmann, & Vogel, 2000a), Lactobacillus minden- Lb. acidifarinae Lb. plantarum Lb. amylovorus
Lb. brevis Lb. pentosus Lb. acidophilus
sis (Ehrmann, Müller, & Vogel, 2003), Lactobacillus paral- Lb. buchneri Lb. alimentarius Lb. delbrueckii subsp.
imentarius (Cai, Okada, Mori, Benno, & Nakase, 1999), delbrueckii
Lactobacillus spicheri (Meroth, Hammes, & Hertel, 2004), Lb. fermentum Lb. paralimentarius Lb. farciminis
Lactobacillus rossiae [formerly Lactobacillus rossii (Corsetti Lb. fructivorans Lb. casei Lb. mindensis
et al., 2005)], Lactobacillus acidifarinae, Lactobacillus Lb. frumenti Lb. crispatus
Lb. hilgardii Lb. johnsonii
zymae (Vancanneyt et al., 2005), Lactobacillus hammesii Lb. panis Lb. amylolyticus
(Valcheva et al., 2005), Lactobacillus nantensis (Valcheva Lb. pontis
et al., 2006) and Lactobacillus siliginis (Aslam et al., Lb. reuteri
2006) were first isolated from sourdough matrices. A selec- Lb. rossiae
tion occurs during propagation that leads to the establish- Lb. sanfranciscensis
Lb. siliginis
ment of, usually, one or two Lactobacillus species at Lb. spicheri
numbers that are three or four orders of magnitude above Lb. zymae
those of the adventitious microbial flora (Hammes & Gän-
zle, 1998; Hammes, Stolz, & Gänzle, 1996).
Sourdough lactobacilli, consisting of obligately and fac-
FRUCTOSE
ultatively heterofermentative, and obligately homofermen-
tative species (Table 1) are associated with type I, type II, NADH + H+ mannitol dehydrogenase
type III sourdough and with type 0 dough. Type 0 dough, NAD+

for which baker’s yeast is the main fermenting agent, is not MANNITOL
made with sourdough technology. However, yeast prepara-
tions often contain LAB, especially lactobacilli rather than
Pediococcus, Lactococcus and Leuconostoc spp. (Jenson, MALATE CITRATE
1998), which in this case contributes only to a small degree
to the acidification and aroma development of dough citrate lyase
CO2
because of the short processing time (Rothe & Ruttloff, Acetate

1983). Starting from glucose, homofermentative LAB LACTATE OXALACETATE

lactate-dehydrogenase
mainly produce lactic acid through glycolysis (homolactic oxaloacetate-decarboxylase
NADH + H+
fermentation) while heterofermentative LAB produce, NAD+ CO2
besides lactic acid, CO2, acetic acid and/or ethanol
(depending on the presence of additional substrates acting PYRUVATE
PYRUVATE
as electron acceptors, as reported in Fig. 2 for Lactobacillus
sanfranciscensis) through 6-phosphogluconate/phosphoke- O2
tolase (6-PG/PK) pathway (heterolactic fermentation). 2 NADH + 2 H+ NADH-oxidase
Hexoses other than glucose enter these major pathways 2 NAD+
at the level of glucose-6-phosphate or fructose-6-phosphate
after isomerization and/or phosphorylation (Axelsson, 2 H 2O
1998). Disaccharides are split by specific hydrolyses and/ Fig. 2. Fate of potential electron acceptors upon carbohydrates fermen-
or phosphohydrolases to monosaccharides which then tation by Lb. sanfranciscensis.
enter the major pathways. Pentoses are phosphorylated
and converted to ribulose-5-phosphate or xylulose-5-phos-
phate by epimerases or isomerases and subsequently tive heterofermentative LAB is induced by the available
metabolized through the lower half of the 6-PG/PK path- pentose sugar (Hammes & Vogel, 1995). Fermentation of
way (Axelsson, 1998). Utilization of pentoses is not pentoses results in the production of equimolar amounts
restricted to LAB species which possess a constitutive of lactic and acetic acid; no CO2 is formed and since no
phosphoketolase, the key enzyme of the 6-PG/PK pathway dehydrogenation steps are necessary to reach the interme-
(obligately heterofermentative); facultative heterofermen- diate xylulose-5-phosphate, acetyl phosphate is used by
tative LAB, which ferment hexose through glycolysis acetate kinase in a substrate level phosphorylation step
because they possess a constitutive fructose-1,6-diphos- yielding acetate and ATP. Obligately homofermentative
phate aldolase (key enzyme of glycolysis), ferment pentoses LAB do not ferment pentoses (Axelsson, 1998). So far,
in the same way as obligately heterofermentative species. some studies have been aimed to the sequencing of com-
Under such circumstances, the phosphoketolase of faculta- plete genome of lactobacilli, including Lactobacillus brevis
542 A. Corsetti, L. Settanni / Food Research International 40 (2007) 539–558
(Makarova et al., 2006), Lactobacillus plantarum (Kleereb-
ezem et al., 2004) and Lb. reuteri (unpublished results), that
are also found in sourdough. Furthermore, some papers
dealing with investigation on their genome size, performed
by pulsed field gel electrophoresis, (Ehrmann & Vogel,
2005; Zapparoli, Torriani, & Dellaglio, 1998) showed that
genomes of Lb. sanfranciscensis, Lactobacillus pontis and
Lb. reuteri are about 1.5 Mbp, thus indicating that the met-
abolic potential and adaptation to several niches of these
species may be limited.
Yeasts are also often associated with LAB in sourdough
and yeasts/LAB ratio is generally 1:100 (Gobbetti, Cor-
setti, Rossi, La Rosa, & De Vincenzi, 1994a; Ottogalli
et al., 1996). Yeasts found in sourdoughs belong to more
than 20 species (Gullo, Romano, Pulvirenti, & Giudici,
2002; Rossi, 1996; Stolz, 1999). The frequently dominant
S. cerevisiae (Corsetti et al., 2001; Gobbetti et al., 1994a;
Vernocchi et al., 2004a; Vernocchi et al., 2004b) is often
introduced through the addition of baker’s yeast (Corsetti
et al., 2001). Typical yeasts associated with LAB in sour-
doughs are Saccharomyces exiguus, Candida humilis (for-
merly described as Candida milleri) and Issatchenkia
orientalis (Candida krusei) (Gobbetti et al., 1994a; Spicher
& Schröder, 1978; Succi et al., 2003; Sugihara, Kline, &
Miller, 1971; Vernocchi et al., 2004a; Vernocchi et al.,
2004b). Other yeast species detected in sourdough ecosys-
tem are: Pichia anomala (as Hansenula anomala), Saturnis-
pora saitoi (as Pichia saitoi), Torulaspora delbrueckii,
Debaryomyces hansenii and Pichia membranifaciens
(Foschino & Galli, 1997; Gobbetti et al., 1994a; Succi
et al., 2003). The extensive variability in the number and
type of species found depends on several factors, including
degree of dough hydration [dough yield (DY) = weight of
dough/weight of flour ·100], type of cereal used, leavening
temperature, and sourdough maintenance temperature
(Gobbetti et al., 1994a).
LAB, both homofermentative and heterofermentative
species, contribute most to the process of dough acidificat-
ion, while yeasts are primarily responsible for the leaven-
ing. Nevertheless, heterofermentative LAB are also
known to partly contribute to the leavening process (Gobb-
etti et al., 1995a; Spicher, 1983).
2.1. Dominating lactobacilli in sourdough
A phylogram based on 16S rRNA gene sequences of
sourdough lactobacilli is reported in Fig. 3. A total of 41
species are included in the tree, even though, probably
due to their misidentification, some of them have been
rarely or just once reported to be found in sourdough, as
an example could be cited Lactobacillus rhamnosus (Spicher
& Lönner, 1985) detected before molecular techniques
being available. About 30 species (Table 1) are effectively
considered to be typical of sourdough environments (Ham-
mes et al., 2005).
Lactobacillus sanfranciscensis, Lb. brevis and Lb. planta-
rum are the most frequently lactobacilli isolated from sour-
doughs (Böcker, Vogel, & Hammes, 1990; Corsetti et al.,
2003; Corsetti et al., 2001; Gobbetti, 1998; Valmorri
et al., 2006). However, some strains, initially classified as
Lb. plantarum may actually belong to Lactobacillus para-
plantarum or Lactobacillus pentosus species, since both
phenotypic determination tools, such as carbohydrate fer-
mentation patterns, and genetic methods, such as 16S
rRNA gene sequence analysis, are not able to distinguish
among Lb. plantarum group species. For a reliable identifi-
cation of these species, a multiplex PCR with recA
gene-derived primers was developed (Torriani, Felis, &
Dellaglio, 2001). Traditional production by various stages
of continuous propagation and production by commercial
starter cultures allow the predominance of Lb. sanfrancisc-
ensis which is considered to be the key sourdough LAB
(Gobbetti & Corsetti, 1997). Lactobacillus sanfranciscensis
dominates type I sourdough fermentations; this observed
predominance of Lb. sanfranciscensis strains is possibly
the result of the selective pressures that arise through the
environmental conditions pertinent to the applied sour-
dough fermentation technology (Böcker et al., 1995; Cor-
setti et al., 2001; Foschino et al., 1999; Kline & Sugihara,
1971). In general, the competitiveness of heterofermenta-
tive lactobacilli in sourdoughs mainly relies on their com-
bined use of maltose and electron acceptors (Gobbetti &
Corsetti, 1996; Gobbetti & Corsetti, 1997; Gobbetti et al.,
1995a; Vogel, Ehrmann, & Gänzle, 2002). The majority
of Lb. sanfranciscensis strains only ferment glucose and
maltose (Corsetti et al., 2001). However, sucrose, raffinose,
galactose, melibiose, ribose and fructose can be fermented
by some Lb. sanfranciscensis strains (Hammes & Gänzle,
1998); in this case, fructose is used, under certain condi-
tions, as external electron acceptor (Gobbetti & Corsetti,
1997; Stolz, Böcker, Hammes, & Vogel, 1995a) since virtu-
ally all strains display mannitol dehydrogenase activity and
reduce fructose to mannitol (Gänzle, Vermeulen, & Vogel,
2007).
Gobbetti (1998) reported on the Lb. sanfranciscensis/
Lb. plantarum association in Italian wheat sourdough.
Lb. plantarum may be superseded by another facultative
heterofermentative species: Lactobacillus alimentarius in
its association with Lb. sanfranciscensis in sourdough made
from durum wheat (Corsetti et al., 2001). Lactobacillus ali-
mentarius is capable of fermenting all four flour soluble
carbohydrates (maltose, sucrose, glucose and fructose)
and it is possible that this reduces direct metabolic compe-
tition with Lb. sanfranciscensis. Most of the Lb. alimentar-
ius strains, due to a phenotypical misidentification,
probably belong to Lb. paralimentarius, a facultatively het-
erofermentative species first isolated from Japanese sour-
dough (Cai et al., 1999). Lactobacillus brevis and Lb.
plantarum have generally been found associated with Lac-
tobacillus fermentum in Russian sourdoughs (Kazanskaya,
Afanasyeva, & Patt, 1983) and Lb. fermentum dominates
Swedish sourdoughs (Spicher & Lönner, 1985) and Ger-
man type II sourdoughs, although, in the latter case, it
was demonstrated that it originated from the baker’s yeast
 A. Corsetti, L. Settanni / Food Research International 40 (2007) 539–558 543

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Fig. 3. Phylogenetic tree of Lactobacillus species commonly associated to or found in sourdough products based on 16S rRNA gene sequences. Sequence
alignment was performed with CLUSTALX (Thompson et al., 1997). Sequence and alignment manipulations and calculation of similarity values and
nucleotide compositions of sequences were performed with GeneDoc program version 2.5.000 (Nicholas and Nicholas, unpublished data). Positions
available for analysis were ca. 1160 bp. Phylogenetic and molecular evolutionary analyses were conducted using MEGA version 3.1 (Kumar et al., 2004).
The bar indicates the number of nucleotide substitutions per site.

used (Meroth, Walter, Hertel, Brandt, & Hammes, 2003). doughs of southern and central Italy (Settanni, Van Sind-
Furthermore, Gobbetti et al. (1994a) reported that Lb. aci- eren, Rossi, & Corsetti, 2005a). From preliminary
dophilus is common in Umbrian (Italian region) sour- observations, Lb. rossiae is often associated with the key-
doughs, even though it is rarely isolated from sourdoughs sourdough Lb. sanfranciscensis (data not published). More-
of different origin (Infantes & Tourneur, 1991; Salovaara over, Lb. rossiae has been found in environments other
& Katunpää, 1984; Spicher, 1984). Recently, Corsetti and than sourdough (pig feaces) (De Angelis et al., 2006a),
coworkers (2005), described a new sourdough associated while no other habitat is known for Lb. sanfranciscensis
species, Lb. rossiae, that seems to be wide diffused in sour- (Hammes et al., 2005).
544 A. Corsetti, L. Settanni / Food Research International 40 (2007) 539–558
2.2. Microbial interactions
Knowledge to exploit and improve the stability of asso-
ciated sourdough LAB and yeasts are necessary in order to
prevent the loss of variety of regional specialities while
simultaneously trying to meet consumer and industry
demands (Gobbetti, 1998). Stable co-metabolism between
LAB and yeasts is common in many foods, enabling the
utilization of substrates that are otherwise non-fermentable
(for example starch) by individual microorganisms and,
thus, increasing the microbial adaptability to complex food
ecosystems (De Vuyst & Neysen, 2005; Gobbetti, Corsetti,
& Rossi, 1994b; Gobbetti & Corsetti, 1997; Stolz, Böcker,
Vogel, & Hammes, 1995b). San Francisco French bread
and Panettone are characterised by a unique and strict
association between Lb. sanfranciscensis and S. exiguus
(Foschino et al., 1999; Gobbetti et al., 1994a; Sugihara,
Kline, & McGgready, 1970; Sugihara et al., 1971). This
association, optimal in continuously operating sourdough
fermentation systems (Vollmar & Meuser, 1992), has been
found in sourdoughs from different countries (Spicher,
Rabe, Sommer, & Stephan, 1982; Wlodarczyk, 1985) as
well as in gluten-free baked goods (Wlodarczyk, Jezynska,
& Warzywoda, 1993). Soluble carbohydrates are present in
low amounts in rye and especially wheat flours and their
concentration varies with the type of flour (Salovaara &
Valjakka, 1987) and with the level of amylase activity on
the damaged starch granules (Oura, Suomalainen, & Visk-
ari, 1982). Wheat flour contains 1.55–1.85% soluble carbo-
hydrates depending on the balance between starch
hydrolysis by the flour and microbial enzymes and micro-
bial consumption (Martinez-Anaya, 1996). Lactobacillus
sanfranciscensis hydrolyzes maltose by a maltose phos-
phorylase which produces a molecule of glucose-1-phos-
phate that is metabolized further, and a molecule of
glucose, which is excreted outside the cell to avoid intracel-
lular accumulation (Fig. 4) (Ehrmann & Vogel, 1998; Stolz,
Hammes, & Vogel, 1996). Maltose phosphorylase acts
without the expenditure of ATP. Inside the Lb. sanfrancisc-
amylases
STARCH MALTOSE
maltose-H+ symport
ate/
lucon
6-P-g pathway MALTOSE
las e
P-keto maltose phosphorylase
GLUCOSE-1-P + GLUCOSE
maltose-inducible
glucose uniport
GLUCOSE
Fig. 4. Utilization of maltose by Lb. sanfranciscensis.
ensis cell cytoplasm, glucose-1-P is converted into glucose-
6-P by the action of phosphoglucomutase and then further
metabolized through the 6-phosphogluconate/phosphoke-
tolase pathway. As long as there is plenty of maltose in
sourdough, Lb. sanfranciscensis uses such an energetically
more favourable pathway in which it is releasing glucose
(Salovaara, 1998). Maltose-negative yeasts (e.g. S. exiguus)
may in turn utilize such excreted glucose. The lack of com-
petition for maltose (Sugihara et al., 1970) possibly
explains the observed stimulation of S. exiguus by Lb. san-
franciscensis. Saccharomyces exiguus preferentially uses
glucose or sucrose and shows a high tolerance to the acetic
acid produced by heterofermentative microorganisms (Sui-
hko & Mäkinen, 1984). Such an association presents
ecological advantages to both Lb. sanfranciscensis and
S. exiguus. However, maltose utilization by maltose-posi-
tive yeasts only begins when available glucose and fructose
are depleted (Barber, Baguena, Benedito de Barber, &
Martinez-Anaya, 1991). Amino acid production by yeasts
stimulates Lb. sanfranciscensis growth even though syn-
thetic medium is deficient of essential amino acids such
as valine and isoleucine (Gobbetti, Corsetti, & Rossi,
1994c). Sour Dough Bacteria (SDB) broth (Kline & Sugi-
hara, 1971) is an optimal medium for the growth of Lb.
sanfranciscensis. It is made with freshly-prepared yeast
extract which contains a small peptide (Asp-Cys-Glu-Gly-
Lys) identified as a growth stimulant factor for Lb. sanfran-
ciscensis (Berg, Sandine, & Anderson, 1981); fresh yeast
extract cannot be substituted by commercial yeast extracts,
liver or protein hydrolysates (Sugihara & Kline, 1975).
Gobbetti et al. (1994b) observed a decrease in Lb. san-
franciscensis metabolism when associated with S. cerevi-
siae, a phenomenon which apparently is due to a faster
consumption of maltose and in particular of glucose by
the yeast. In contrast, Meignen et al. (2001) reported a
reduction of S. cerevisiae growth when it was mixed with
Lb. brevis. The disappearance of S. cerevisiae from the
microbial population of sourdough during consecutive fer-
mentations is related to the repression of the genes involved
in maltose fermentation, as a consequence of which malt-
ose cannot be utilized (Nout & Creemers-Molenaar,
1987). This causes a rapid depletion of sucrose and a
decline of particularly sensitive S. cerevisiae strains as a
result of acetic acid produced by heterofermentative LAB
that, at sourdough pH (4.0–4.5), is in the undissociated
lipophilic and membrane-diffusable form, thus exhibiting
its highest inhibitory activity (Blom & Mörtvedt, 1991).
In agreement with Hansen, Lund, and Lewis (1989a),
who demonstrated a greater adaptability of yeasts to grow
in association with homofermentative rather than hetero-
fermentative LAB, S. cerevisiae fermentation was posi-
tively influenced by Lb. plantarum, especially regarding
the production of CO2 that resulted increased compared
to the CO2 produced by the association S. cerevisiae/Lb.
sanfranciscensis (Gobbetti et al., 1995a).
Interactions among sourdough LAB depend on several
mechanisms in which some competitive advantages are
 A. Corsetti, L. Settanni / Food Research International 40 (2007) 539–558
provided by bacteriocin whose discussion is reported below
(Section 3.4.1).
3. Useful propreties of sourdough lactobacilli
3.1. Contribution of lactobacilli to flavour development
Taste and smell of bread or any other cereal based
baked product are the main characteristics taken into
account by consumers to determine its quality. The flavour
of wheat bread is assumed to be influenced by the nature of
the raw materials as well as the conditions of the fermenta-
tion and baking process (Hansen, Lund, & Lewis, 1989b).
Czerny and Schieberle (2002) found high odour activities in
wholemeal and white wheat flours. In general, the baking
process influences the typical aroma of bread crust, while
dough fermentation is fundamental for the development
of crumb flavour. Furthermore, the recipe and geographi-
cal origin make the difference in the aroma of breads
consumed in different geographical areas (Hansen & Schi-
eberle, 2005).
The largest amounts of aroma substances are undoubt-
edly formed during baking (Schieberle, 1996; Spicher,
1983), e.g. the roasty aroma of wheat bread is due to the
formation of compounds such as 2-acetyl-1-pyrrolin, giv-
ing the typical scent of wheat bread in the crust (Schieberle,
1996). Because of its lack in gluten proteins, rye flour has to
be prefermented before bread can be manufactured from
such rye-based dough and this procedure is one of the main
reasons for the differences in the overall aromas between
wheat and rye breads (Kirchhoff & Schieberle, 2001). Nev-
ertheless, sourdough fermentation is essential to achieve an
acceptable flavour, since a comparison between chemically
acidified bread and sourdough bread showed that the latter
possessed a superior sensory quality (Kirchhoff & Schi-
eberle, 2002; Rothe & Ruttloff, 1983). The ratio between
lactic and acetic acid, defined as the fermentation quotient
(FQ), is an important factor that might affect the aroma
profile, although it is also relevant for the structure of final
products. Acetic acid, produced by heterofermentative
LAB, is responsible for a shorter and harder gluten while
lactic acid can gradually account for a more elastic gluten
structure (Lorenz, 1983). Regarding whole rye sourdough
bread, optimal FQ drops into the range of 1.5–4.0 (Spicher,
1983). The attention towards the increasing of acetic acid
content is also due to its antimicrobial effect on the rope-
producing Bacillus and antimould effect (Rosenquist &
Hansen, 1998).
Compounds strongly affecting bread flavour are mainly
organic acids, alcohols, esters and carbonyls (Barber, Tor-
ner, Martinez-Anaya, & Benedito de Barber, 1989; Czerny
& Schieberle, 2002; Hansen & Lund, 1987; Hansen et al.,
1989a; Hoffmann & Schieberle, 2000; Kirchhoff & Schi-
eberle, 2002; Lund, Hansen, & Lewis, 1989; Röcken, Rick,
& Reinkemeier, 1992). In order to generate sufficient
amounts of volatile compounds, the generation process
needs multiple steps of about 12–24 h; when baker’s yeast
545
is used the fermentation is completed within a few hours
(Hansen & Schieberle, 2005). Bacterial proteolysis during
sourdough fermentation was shown to contribute much
more to the development of typical sourdough flavours
of baked breads when compared to breads produced from
chemically acidified or yeasted doughs (Hansen et al.,
1989b). Several works have reported on the importance
of amino acid conversion to flavour volatile compounds
(Gao, Mooberry, & Steele, 1998; Juillard, Guillot, Le Bars,
& Gripon, 1998; Smacchi & Gobbetti, 1998; Smit, Verheul,
van Kranenburg, Siezen, & Engels, 2000; Tamman, Wil-
liams, Novle, & Lloyd, 2000; Zotta, Piraino, Ricciardi,
McSweeney, & Parente, 2006). Furthermore, addition of
amino acids (e.g. ornithine, leucine and phenylalanine) to
doughs resulted in an enhanced conversion to flavour com-
pounds (Gassenmeier & Schieberle, 1995; Schieberle,
1990). At this proposal, proteolytic strains of sourdough
LAB may affect amino acids level in doughs, but there is
substantial evidence that the activation of cereal proteases
is a major driving force for protein degradation in sour-
doughs (Loponen, Mikola, Katina, Sontag-Strohm, & Sal-
ovaara, 2004; Thiele, Gänzle, & Vogel, 2002, 2003; Thiele,
Grassl, & Gänzle, 2004; Vermuelen, Pavlovic, Ehrmann,
Gänzle, & Vogel, 2005). The key degradation reaction of
amino acids during fermentation is the Ehrlich pathway
leading to aldehydes or the corresponding alcohols (Schi-
eberle, 1996), while during baking takes place the Strecker
reaction which also leads to aldehydes, but also to the cor-
responding acids (Hoffmann & Schieberle, 2000).
Differences other than acetic acid production, in the
overall aroma profile of final bread, are due to the type
of dominating lactobacilli. Ethyl acetate content was
higher in firm wheat (Damiani et al., 1996) and rye sour-
doughs (Lund et al., 1989) fermented with heterofermenta-
tive LAB compared to sourdoughs fermented with
homofermentative LAB. The same trend was observed
for hexyl acetate in firm rye sourdough, while the content
of aldehydes was higher in rye sourdoughs fermented with
homofermentative cultures (Lund et al., 1989). Regarding
diacetyl, it has been found that its content was higher in
sourdough manufactured with homofermentative com-
pared to heterofermentative cultures (Damiani et al.,
1996; Hansen et al., 1989b; Lund et al., 1989). However,
due to evaporation during baking, the amounts of alcohols,
esters and diacetyl in sourdough bread are much lower
than in the corresponding sourdough (Hansen & Hansen,
1996; Lund et al., 1989).
Contribution of metabolites produced by yeasts in
imparting taste and flavour to foods and, in particular to
sourdough, is well documented (Brauman, Keleke, Mal-
onga, Miambi, & Ampe, 1996; Czerny, Brandt, Hammes,
& Schieberle, 2004; Halm, Lillie, Sørensen, & Jakobsen,
1993). Sourdoughs made with both LAB and yeasts
resulted in more aroma compounds as compared to sour-
doughs made from single starter based either on LAB
(e.g. Lb. brevis) or yeast (e.g. S. cerevisiae) (Meignen
et al., 2001). Sourdoughs with a higher relative percentage
546 A. Corsetti, L. Settanni / Food Research International 40 (2007) 539–558
of yeast-derived fermentation products are produced if a
combination of S. cerevisiae with Lb. sanfranciscensis and
Lb. plantarum is used during the sourdough fermentation
process (Gobbetti, Corsetti, & Rossi, 1995b). This observed
increased production of aroma compounds in a mixed-star-
ter process appears to be related to the proteolytic activity
of LAB.
The arginine metabolism by Lb. pontis (Thiele et al.,
2002) and Lb. sanfranciscensis (De Angelis et al., 2002)
has been demonstrated to have a defined impact on bread
flavour. Recently, Gerez, Rollán, and De Valdez (2006)
reported that gluten breakdown of lactobacilli and pedio-
cocci, besides reducing gluten-allergen compounds, also
increased the basic amino acid concentration in broth cul-
tures, mainly due to an increase in the amount of ornithine,
which is considered to be the key flavour precursor in
wheat bread (Gassenmeier & Schieberle, 1995), generating
2-acetyl-1-pyrrolin (Thiele et al., 2002). Phenylalanine
metabolism, as studied in Lb. plantarum and Lb. sanfran-
ciscensis, besides producing phenyllactic acid (PLA) and
its 4-hydroxy derivative (OH-PLA), whose antifungal
activities are reported below (Section 3.3.2), also generate
flavour volatiles (Vermeulen, Gänzle, & Vogel, 2006).
Czerny and Schieberle (2002) reported that fermentation
of suspensions of wholemeal and white wheat flours LAB
did not generate new odorants than those present in raw
materials, but they demonstrated that many compounds,
such as acetic acid or 3-methylbutanal, were increased,
whereas aldehydes (formed from the degradation of unsat-
urated fatty acids) were decreased. The authors concluded
that the odorant concentrations present before and after
fermentation gave evidence that the main influence of the
microorganisms on sourdough aroma is to either enhance
or decrease specific volatiles already present in the flour.
Therefore, careful selection of starter cultures is pivotal
to modify the aroma of flour-based products (Vogel
et al., 2002).
3.2. Contribution of lactobacilli to dough structure
Essentially, cereal grains contain starch and non-starch
polysaccharides, the latter composed of glucose (b-glucan),
fructose (polyfructan), xylose and arabinose (arabinoxy-
lan) (Belitz & Grosh, 1999). Starch is partially digestible
while some of the other polysaccharides, such as arabin-
oxylan, would represent dietary fibres. Wheat and rye
flours contain, in addition to polyfructan, also nystose, kes-
tose and other fructooligosacchaides of the inulin type
(Campbell et al., 1997) whose prebiotic effect is well docu-
mented (Van Loo et al., 1999). Bacterial polysaccharides
that are secreted into the environment are termed exopoly-
saccharides (EPS). Two classes of EPS from LAB can be
distinguished, extracellularly synthesised homopolysaccha-
rides (HoPS), composed of only one type of monosaccha-
ride and are synthesised by extracellular glucan- and
fructosyltransferases (glycosyltransferases) using sucrose
as the glycosyl donor, and heteropolysaccharides (HePS)
with (ir)regular repeating units. The repeating units of
HePS are composed of 3–8 carbohydrate moieties that
are synthesised intracellularly from sugar nucleotide pre-
cursors (De Vuyst, De Vin, Vaningelgem, & Degeest,
2001). HePS application is currently limited to ‘ropy’ dairy
starter cultures employed to improve the texture of yoghurt
and other fermented milk products (Laws & Marshall,
2001), while HoPS are generally applied to improve struc-
tural characteristics of baked goods. Sourdough lactoba-
cilli have not been found to produce HePS while the
secretion of alternan, dextran, fructan, inulin, levan, mutan
and reutaran is known (see Tieking & Gänzle, 2005 for a
review).
One of the key sourdough LAB, Lb. sanfranciscensis,
has been well characterized for its contribution to the
enhancement of polysaccharide content of sourdough due
to the production of EPS (Korakli, Gänzle, & Vogel,
2002; Korakli, Pavlovic, Gänzle, & Vogel, 2003; Korakli,
Rossman, Gänzle, & Vogel, 2001; Tieking & Gänzle,
2005; Tieking, Korakli, Ehrmann, Gänzle, & Vogel,
2003). Formation of EPS is a well accepted characteristic
of sourdough LAB, since this feature influences the viscos-
ity of sourdough (Vogel et al., 2002). Furthermore, fructan
produced by two strains of Lb. sanfranciscensis has been
shown to stimulate bifidobacterial growth (Dal Bello, Wal-
ter, Hertel, & Hammes, 2001), thus acting as a prebiotic or
in this case as a bifidogenic factor. Modler (1994) reported
that the application of prebiotics increases both the occur-
rence and the number of faecal bifidobacteria which are
among the most prominent bacteria found in the jejunum
with widely accepted probiotic properties (Salminen,
Deighton, Benno, & Gorbach, 1998). Also certain LAB
strains are reported to possess health-promoting activities
(Lee & Salminen, 1995). Among such probiotic LAB
strains are those that have been isolated from cereal-based
fermented food being capable of adhering to human intes-
tinal cells (Müller et al., 1998). From this is clear that bifid-
ogenic substrates produced by LAB (which are generally
recognized as safe) and resistant to low pH (not degraded
during fermentation) and high temperature (still available
after baking) may be acceptable in foods as a possible pre-
biotic component of that food. Furthermore, species such
as Lb. pontis, Lactobacillus panis, Lactobacillus mucosae,
Lb. reuteri, Lactobacillus oris, Lb. acidophilus (Roos, Kar-
ner, Axelsson, & Jonsson, 2000; Simpson, McCracken,
Gaskins, & Mackie, 2000; Vogel et al., 2002), and recently
Lb. rossiae (De Angelis et al., 2006a), have been found both
in human and animal intestine and feaces, as well as in
sourdoughs, and their possible probiotic activity merits
further investigation (Vogel et al., 2002).
3.3. Lactobacilli as organisms to improve nutritional
quality and healthy aspects of sourdough
Although optimal sensory characteristics represent the
basis for any successful fermented food, consumers are
particularly sensitive to its nutritional value and healthy
 A. Corsetti, L. Settanni / Food Research International 40 (2007) 539–558
aspects. Cereal-based products are utilized in the human
feeding throughout the world, thus it is worth considering
their potential as products fulfilling such criteria.
3.3.1. Reduction of antinutritional factors
Cereal grains are important sources of minerals such as
iron, potassium, magnesium and zinc, but also contain
phytic acid or myo-inositol hexakiphosphate (IP6) (1–4%
of dry weight) (Pandey, Szakacs, Soccol, Rodriguez-Leon,
& Soccol, 2001), which is considered to be an anti-nutri-
tional factor for humans (Lopez et al., 2000; Minihane &
Rimbach, 2002) and animals. Its anti-nutritional property
is due to the central hexaphosphate ring, known to be
the storage form of phosphorus in seeds, which being
highly charged (six anionic groups) acts as a chelator of
dietary minerals (Nolan & Duffin, 1987) preventing their
absorption and thus reducing their bioavailability (Lönner-
dal, 2002). Phytic acid complexes basic amino acid group
of proteins, resulting in a their subsequent reduced bio-
availability (Dvorakova, 1998; Wodzinski & Ullah, 1996).
Lower inositol phosphate derivatives showed health bene-
fits in the protection of coronary heart, arteriosclerosis
and neural tissue diseases (Fisher, Novak, & Agranoff,
2002; Jariwalla, Sabin, Lawson, & Herman, 1990).
Phytases, hydrolysing phytic acid, are enzymes that play
a pivotal role in upgrading the nutritional quality of phy-
tate-rich foods and feeds (Martinez et al., 1996). Moreover,
insoluble protein-phytate complexes are formed at low pH,
as found in the stomach of monogastric animals, and pro-
tein digestibility is reduced. Dietary phytase supplementa-
tion has been shown to prevent the formation of such
complexes or to aid in dissolving them faster, thus phytases
may improve protein digestibility (Kies, De Jonge, Kemme,
& Jongbloed, 2006).
Phytases are widely present in plant materials such as
wheat and rye flours, whose level depends on variety and
crop year, but generally reported to be insufficient to signif-
icantly decrease the amount of phytic acid (Cossa, Oloffs,
Kluge, Drauschke, & Jeroch, 2000). However, it has been
recently published that a moderate decrease of pH by sour-
dough fermentation is sufficient to reduce phytate content
of whole wheat flour through endogenous phytase activity
(Leenhardt, Levrat-Verny, Chanliaud, & Remesy, 2005).
Phytases are also produced by a multitude of microorgan-
isms among which yeasts (Turk, Sandberg, Carlsson, &
Andlid, 2000) and sourdough LAB (De Angelis et al.,
2003; Lopez et al., 2000; Reale et al., 2004).
Phytases whose activity is optimal at sourdough pH (ca.
4.5) (Fretzdorff & Brümmer, 1992), hydrolyze IP6 into IP5
and then into lower myo-inositol phosphate esters (IP4-IP1)
which are less likely to bind minerals and form weaker min-
eral complexes (Sandberg et al., 1999). Reale et al. (2004)
reported on the reduction of IP6 of about 80–90% in a
dough prepared with a mixed starter culture (Lb. planta-
rum, Lb. brevis, Lactobacillus curvatus) compared to the
control dough, after 12 h fermentation; similar percentages
of IP6 level reduction were reported by De Angelis et al.
547
(2003) who showed that Lb. sanfranciscensis CB1, used to
ferment a dough for 8 h, was able to decrease the Na-phy-
tate concentration till 64–74% compared to the unstarted
sourdough. A study on the characterization of phytase
activity of sourdough microorganisms showed that com-
bining selected yeasts and LAB it is possible to reach high
level of phytate biodegradation and the best combination
was S. cerevisiae/Lb. plantarum/Leuconostoc mesenteroides
(Chaoui, Fais, & Belhcen, 2003). These results emphasize
microbial potential in improving the nutritional quality
of cereal-based products.
3.3.2. Conversion of toxic compounds
Sourdough bread owes its popularity to its naturalness
and tradition, however, due to its gluten content, it is toxic
to people affected by celiac sprue (CS), also known as glu-
ten-sensitive enteropathy, an autoimmune disease of the
small intestinal mucosa. Ingestion of gluten causes self-per-
petuating mucosal inflammation and subsequent loss of
absorptive villi and hyperplasia of the crypts. Proteolytic
enzymes of the endoluminal tract acting on prolamins of
wheat (a-, b-, c-, and x-gliadin), rye (secalin) and barley
(hordein), produce proline- and glycine-rich polypeptides
that are responsible for the disease (Silano & De Vincenzi,
1999). The list of proteins that liberate toxic peptides also
includes high molecular weight glutenins (Dewar et al.,
2006). Further proteolysis of such toxic peptides is made
difficult by the position and abundance of proline residues
(Andria, Cucchiara, De Vizia, Mazzacca, & Auricchio,
1980; Auricchio, Greco, De Vizia, & Buonocore, 1978;
Hausch, Shan, Santiago, Gray, & Khosla, 2003). For the
above reasons, persons affected by CS cannot ingest glu-
ten-containing products such as bread or pasta. Recently,
a prolyl-endopeptidase produced by Flavobacterium men-
ingosepticum, which is not interesting for breadmaking,
showed hydrolysing effect on a 33-mer peptide, which is
one of the most potent peptides involved in triggering the
disease, and the use of this endopeptidase has been pro-
posed for an oral therapy for CS patients (Shan et al.,
2002). Lactobacilli have been shown to possess an out-
standing potential in decreasing the CS-inducing effects of
gluten. Di Cagno et al. (2002) demonstrated active hydro-
lysis of various Pro-rich peptides, including the 33-mer
peptide mentioned above, by some Lactobacillus species.
This finding has been exploited to produce sourdoughs
containing 30% of wheat flour (CS-inducing) and 70% of
other (non-CS-inducing) (Madara & Trier, 1980; Hardman
& Fry, 1997) flours such as oat, buckwheat and millet,
started with selected lactobacilli and fermented for 24 h.
Following this, the mixed starter composed of Lb. alimen-
tarius, Lb. brevis, Lb. sanfranciscensis and Lactobacillus hil-
gardii was shown to almost completely hydrolize gliadin
fractions and consequently the resulting bread was toler-
ated by CS patients (Di Cagno et al., 2004). With the same
aim was also successfully tested VSL#3 probiotic prepara-
tion (VSL Pharmaceuticals, Gaithesburg, MD) (ca. 450 bil-
lion cells/sachet), containing Streptococcus thermophilus,
548 A. Corsetti, L. Settanni / Food Research International 40 (2007) 539–558
Lb. plantarum, Lb. acidophilus, Lactobacillus casei, Lacto-
bacillus delbrueckii spp. bulgaricus, Bifidobacterium breve,
Bifidobacterium longum and Bifidobacterium infantis (De
Angelis et al., 2006b).
For the above reasons, sourdough fermentation is a rep-
resentative of traditional biotechnology of outstanding
importance with great potential in human diet. However,
the complete suitability of sourdough for production of
gluten free bread from wheat or rye flours is still under
study while at present it has been proved that sourdough
technology improves the sensory properties of gluten free
bread (Arendt, Ryan, & Dal Bello, 2007).
3.4. Antimicrobial substances produced by sourdough
lactobacilli
In general, LAB play a crucial role in the preservation
and microbial safety of fermented foods (Caplice & Fitz-
gerald, 1999), thus promoting the microbial stability of
the final products of fermentation (Mensah, Tomkins, Dra-
sar, & Harrison, 1991). Since LAB naturally occur in var-
ious food products, they have traditionally been used as
natural food biopreservatives; protection of foods is due
to the production of organic acids, carbon dioxide,
ethanol, hydrogen peroxide and diacetyl (Atrih, Rekhif,
Moir, Lebrihi, & Lefebvre, 2001; De Vuyst & Vandamme,
1994a), antifungal compounds such as fatty acids (Corsetti,
Gobbetti, Rossi, & Damiani, 1998) or phenyllactic acid
(Lavermicocca et al., 2000), bacteriocins (De Vuyst &
Vandamme, 1994a) and antibiotics such as reutericyclin
(Höltzel, Gänzle, Nicholson, Hammes, & Jung, 2000).
Messens and De Vuyst (2002) have extensively reviewed
the inhibitory substances produced by sourdough lactoba-
cilli. Fundamental features of an antimicrobial substance
to be active under food conditions is that it is produced
at active concentrations and that the effect is not masked
by food components.
3.4.1. Bacteriocins
Bacteriocins are antimicrobial peptides or small proteins
which inhibit, by a bactericidal or bacteriostatic mode of
action, microorganisms that are usually closely related to
the producer strain (De Vuyst & Vandamme, 1994b; Schil-
linger & Holzapfel, 1996). Bacteriocins from LAB have
been classified in three classes on the basis of common,
mainly structural, characteristics (Nes et al., 1996). Bacteri-
ocins target the cell envelope, and with the exception of the
larger proteins (>20 kDa) that degrade the murein layer
(e.g. lysins and muramidases), use non-enzymatic mecha-
nisms to disrupt the integrity of the target cell membrane
and/or inhibit cell wall synthesis (Twomey, Ross, Ryan,
Meaney, & Hill, 2002).
Microbial growth inhibition is due to a series of phe-
nomena, first of all dissipation of the transmembrane elec-
trical potential Dw. Strong cytotoxic effects presumably
result from proton influx that leads to a drop of the intra-
cellular pH and consequently to the inhibition of many
enzymatic processes (Moll, Konigs, & Driessen, 1999).
Also influx of sodium ions has a cytotoxic effect (Cheng,
Guffanti, & Krulwich, 1997). Pores in the cytoplasmic
membrane clearly affect the energetic status of the cell,
i.e. dissipation of proton motive force causes an arrest of
DpH and Dw dependent (e.g. transport) processes while
certain bacteriocins cause ATP efflux (Moll et al., 1999).
Bacteriocin producer strains are protected against their
own bacteriocins by a protection system referred to as
immunity. Each bacteriocin has its own dedicated protein
conferring immunity, which is expressed concomitantly
with the bacteriocin (Nes et al., 1996).
Bacteriocins may contribute to the competitiveness of
the producing strain in a fermented food ecosystem
(Caplice & Fitzgerald, 1999). Bacteriocins produced by
sourdough LAB have been purified and well characterized
with regards to their in vitro activity. As examples can be
cited plantaricin ST31 produced by Lb. plantarum ST31
(Todorov et al., 1999) and bavaricin A produced by Lacto-
bacillus bavaricus MI401 (previous designation of Lactoba-
cillus sakei) (Larsen, Vogensen, & Josephsen, 1993).
Corsetti, Gobbetti, and Smacchi (1996), Corsetti, Settanni,
and Van Sinderen (2004) reported on the discovery of anti-
microbial molecules produced by sourdough lactobacilli.
Although these activities were not purified to homogeneity,
such antimicrobial compounds displayed characteristics
similar to bacteriocins, and were hence designated as bacte-
riocin-like inhibitory substances (BLIS) (Tagg, 1991). Lb.
pentosus 2MF8 isolated from sourdough (Corsetti et al.,
2004), was the first example of a sourdough-derived Lacto-
bacillus strain that produced an antimicrobial compound
with bacteriocin characteristics and reported to be active
under sourdough conditions. The in situ activity of BLIS
M30 produced by Lactococcus lactis subsp. lactis M30
and isolated from unmalted barley (Hartnett, Vaughan,
& van Sinderen, 2002) was also tested in the sourdough
ecosystem, where it was shown to possess a more potent
inhibitory spectrum and activity than sourdough LAB,
while it did not inhibit certain strains of the key sourdough
bacterium Lb. sanfranciscensis (Corsetti et al., 2004). The
activity of the above BLIS M30, later identified as lacticin
3147-like bacteriocin (Settanni, Massitti, Van Sinderen, &
Corsetti, 2005b), was also followed over a period of 20 days
(corresponding to 20 refreshments) showing a strong influ-
ence on the microbial consortium of sourdough LAB and
its aptitude to support the dominance of insensitive strains
during sourdough fermentation (Fig. 5). De Vuyst et al.
(2004) reported on the application of a bacteriocin-produc-
ing Lactobacillus amylovorus strain isolated from fresh corn
steep liquor (De Vuyst, Callewaert, & Pot, 1996) in type II
cereal fermentation. Lb. amylovorus DCE 471, which pro-
duces amylovorin L471, a class IIa bacteriocin (Klaenham-
mer, 1993) represented the only culture used as starter.
Wheat and rye sourdough were acidified within 15 h to a
final pH below 3.7, which would be in agreement with an
industrial type II rye sourdough containing Lb. amylovorus
at high concentration (Müller, Wolfrum, Stolz, Ehrmann,
 A. Corsetti, L. Settanni / Food Research International 40 (2007) 539–558 549

10

6
Log CFU g-1

0
FT F6h F1T F16h F2T F26h F3 T F36h F4 T F46h F5T F56h F20 T F206h

Step of propagation

10

7
Log CFU g-1

0
GT G6h G1 T G16h G2 T G26h G3 T G36h G4 T G46h G5 T G56h G20 T G206h

Step of propagation

Fig. 5. Persistence of different LAB in sourdoughs started with: (a) Lc. lactis M30 (j), Lb. sanfranciscensis CB1(m) and Lb. plantarum 20 (d); (b) Lc.
lactis Q13 (j), Lb. sanfranciscensis CB1 (m) and Lb. plantarum 20 (d). From Settanni et al. (2005b).

& Vogel, 2001). Lb. amylovorus DCE 471 persistence was
tested over a period of 24 h and it showed the capability
of producing amylovorin L471 under sourdough condi-
tions (De Vuyst et al., 2004) making it a suitable strain
for use in production of type II sourdough.
Although Rosenquist and Hansen (1998) reported that a
variety of bacteriocins from LAB were ineffective to con-
trol the growth of Bacillus spp. in bread, some sourdough
LAB bacteriocins have shown a capability of inhibiting
food-borne pathogens and/or food spoilage bacteria,
including Listeria monocytogenes, Bacillus subtilis and
Staphylococcus aureus, thus their use as food additives or
the application of the producer strains as starter or protec-
tive culture, might contribute to the manufacturing of safer
products. Furthermore, bacteriocins may lead to a reduc-
tion of chemical preservative used by food industry (Mes-
sens & De Vuyst, 2002).
3.4.2. Antifungal compounds
Antimicrobial substances resistant to baking conditions
and active at the physical parameters pertinent to bread,
can control the growth of spoilage organisms (Rosenkvist
& Hansen, 1995). The most frequent cause of spoilage in
baked goods is represented by fungal growth, which may
cause public health concerns relating to mycotoxin produc-
tion (Legan, 1993). Spoiling fungi commonly associated
with bakery losses belong to the genera of Aspergillus, Clad-
osporium, Endomyces, Fusarium, Monilia, Mucor, Penicil-
lium, and Rhizopus (Keshri, Voysey, & Magan, 2002;
Legan, 1993). Besides the common physical methods of food
preservation (heat treatments, cold storage, modified atmo-
sphere storage, drying, freeze-drying) (Farkas, 2001), pro-
tection of baked goods from fungal spoilage is mainly
achieved through the inactivation of contaminating spores
by the use of (1) infrared and microwave radiation; (2) fungal
550 A. Corsetti, L. Settanni / Food Research International 40 (2007) 539–558
inhibitors such as ethanol and propionic, sorbic, benzoic and
acetic acid and some of their salts; (3) suitable packaging
techniques such as modified atmospheres and (4) sourdough
(Brock & Buckel, 2004; Cabo, Braber, & Koenraad, 2002;
Guynot, Marı́n, Sanchis, & Ramos, 2005; Legan, 1993; Röc-
ken, 1996). The last strategy (sourdough addition) seems to
be the best preservation procedure of bread from spoilage,
meeting consumer demands for natural and additive-free
food products (Rosenquist & Hansen, 1998). Extended
shelf-life and improved microbial safety of sourdough bread
is attributed to LAB (Spicher, 1983), whose fungistatic
effects are mainly due to acetic acid rather than lactic acid
production (Röcken, 1996). In this regard, heterofermenta-
tive lactobacilli produce most of the antifungal activity.
Within this group Lb. sanfranciscensis CB1 displays the wid-
est spectrum of antifungal activity due to the production of a
mixture of acetic, caproic, formic, propionic, butyric and
n-valeric acid, among which caproic acid was the organic
acid with the higest antimould activity (Corsetti et al.,
1998). Lavermicocca et al. (2000) purified and characterized
two antifungal compounds produced by Lb. plantarum
ITM21B, identified as phenyllactic and 4-hydroxy-phenyl-
lactic acids, which still retained their fungicidal activities
after baking. Lactobacilli able to produce the above two
antifungal compounds, among which phenyllactic acid is
the most potent one, were shown to delay Aspergillus niger
and Penicillium roqueforti growth for up to 7 days and signif-
icantly prolong the shelf-life of bread (Lavermicocca et al.,
2000; Lavermicocca, Valerio, & Visconti, 2003). Besides
phenyllactic acid, Lactobacillus coryniformis subsp. coryni-
formis Si3 and Lb. plantarum MiLAB14 isolated from plant
material stored under anaerobic conditions were found to
produce a broad-spectrum 3 kDa protein, as well as the
cyclic dipeptides cyclo(L-Phe-L-Pro) and cyclo(L-Phe-trans-
4-OH-L-Pro), all showing antifungal activity at concentra-
tions in the order of mg ml 1 (Magnusson, Ström, Roos,
Sjögren, & Schnürer, 2003; Sjögren, Magnusson, Broberg,
Schnürer, & Kenne, 2003). Lb. plantarum was furthermore
found to produce antifungal hydroxylated fatty acids active
at 10 lg ml 1 (Sjögren et al., 2003).
Recently, Schnürer and Magnusson (2005) published a
summary of the main antifungal compounds produced by
different LAB, they are: lactic and acetic acid, carbon diox-
ide, diacetyl, hydrogen peroxide, caproic acid, 3-hydroxy
fatty acids, phenyllactic acid, cyclic dipeptides, reuterin
and fungicins. The last are reported to be compounds of
proteinaceous nature, since they loose their antifungal
activity after treatment with proteolyitc enzymes. It has
been found that fungicins are produced by strains of Lb.
casei, Lb. pentosus, Lactobacillus paracasei subsp. paracasei
and Lb. coryniformis subsp. coryniformis (Gourama, 1997;
Magnusson & Schnürer, 2001; Okkers, Dicks, Silvester,
Joubert, & Odendaal, 1999).
3.4.3. Other antimicrobial compounds
The natural microflora associated with SER sourdough,
an in house rye sourdough prepared for producing a com-
mercially available baking aid (Böcker et al., 1995), was fol-
lowed over a period of 10 years. Considerable shifts in
microflora composition were observed, apart for what con-
cerned Lb. reuteri LTH2584, a reutericyclin producing strain
first isolated in 1988 from SER. Reutericyclin is a tetrameric
acid derivative with a molecular weight of 349 Da, and active
against a broad range of Gram-positive bacteria including
spoilage organisms and pathogens as St. aureus, Enterococ-
cus faecalis, L. monocytogenes and Bacillus cereus as well as
vegetative cells and spores of rope forming bacilli (Gänzle,
1998). It is produced in active concentrations in dough and
its production is relevant to dough ecology since it was
shown to contribute to the stable persistence of Lb. reuteri
in sourdough over about 50,000 generations of microbial
growth (Gänzle & Vogel, 2003). Some Lb. reuteri strains
were also found to produce reuterin (3-hydroxy-propanal),
an antimicrobial compound representing the main product
of glycerol metabolism that, like reutericyclin, is not classi-
fied as a bacteriocin. Reuterin was shown to be active against
a wide range of Gram-positive as well as Gram-negative bac-
teria (Vogel et al., 2002), yeasts and fungi (Schnürer & Mag-
nusson, 2005) such as Aspergillus and Fusarium (Chung,
Axelsson, Lindgren, & Dobrogosz, 1989).
During bread-making, environmental contamination of
the products may also occur with bacteria such as bacilli
and clostridia, whose growth can be inhibited by acidity
(Voysey & Hammond, 1993). Bacillus spp., especially B.
subtilis and Bacillus licheniformis are spoilage agents of
wheat bread due to rope formation (Kirschner & Von Holy,
1989), while representative strains of both species may also
cause foodborne illness if present at levels over 105 CFU g 1
(Kramer & Gilbert, 1989). Although food-borne illness
related to consumption of ropy bread is considered unlikely
to happen due to the slimy appearance of the crumb, loaves
with high counts of B. subtilis and B. licheniformis, showing
no rope symptoms, may cause diarrhoea and vomiting
(Rosenkvist & Hansen, 1995). Furthermore, Bacillus spores
can survive the baking process where the temperature in the
centre of the crumb remains at maximum of 97–101 C.
However, rope formation occurs principally in wheat
breads that have not been acidified, or in breads with high
concentrations of sugars, fat or fruits (Beuchat & Ryu,
1997). The most natural way to prevent rope formation is
by means of sourdough technology as it is an additive-free
method. Moreover, anti-ropiness activity of sourdough is
not solely due to the presence of lactic acid (Katina, Sauri,
Alakomi, & Mattila-Sandholm, 2002). Infact, although the
acidity level of sourdough is the main determining factor of
the inhibitory activity of LAB (Oscroft, Banks, & McPhee,
1990; Voysey, 1990), other factors may significantly con-
tribute to such antimicrobial activity, as discussed above.
4. Monitoring of lactobacilli dynamics during sourdough
fermentation
The outstanding importance of molecular analysis is
reflected by their exploitation to monitor (changes in)
 A. Corsetti, L. Settanni / Food Research International 40 (2007) 539–558
microbial populations in various ecosystems, such as com-
plex food matrices, without any prior cultivation. The
methods used at this proposal during food fermentation
have recently been reviewed by Giraffa (2004). Ehrmann
and Vogel (2005) reported on the use of RAPD-PCR not
only as a survey of but also in monitoring the change of
composition of lactobacilli in a type II model fermentation,
demonstrating that the dominance of Lb.amylovorus could
be overcome by Lb. pontis and Lb. frumenti over addition
of an enzyme preparation. Settanni et al. (2005b) used this
technique to follow the fate of starter cultures used to pro-
duce sourdoughs. The presence and identity of inoculated
strains (Lb. sanfranciscensis CB1, Lb. plantarum 20 and
Lc. lactis M30 and Q13) was monitored following isolation
from dough, by microscopic inspection and comparing
their RAPD profiles, generated with two oligonucleotide
primers (P4 and M13), to those obtained from the original
cultures. The same approach was used by Reale et al.
(2004) to confirm the presence of lactobacilli (Lb. planta-
rum, Lb. brevis and Lb. curvatus) inoculated as sourdough
starter cultures at the end of fermentation.
PCR-based methods, that target primarily a given gene
(most commonly a ribosomal gene), are the most widely
applied technologies, although a polyphasic approach, e.g.
an approach, employing both genotypic and phenotypic
information (Rosselló-Mora & Amann, 2001), appears
to be more helpful and realistic to describe microbial
population dynamics (ben Omar & Ampe, 2000). Within
culture-independent methods, developed to circumvent
the limitations of conventional cultivation for analysis of
microbial communities (Vaughan et al., 2002), PCR-dena-
turing gradient gel electrophoresis (PCR-DGGE) analysis
is one of the most suitable and widely applied methods to
study complex bacterial communities originating from var-
ious environments (Muyzer, 1999). PCR-DGGE provides
information about variation of PCR products of the same
length but with different sequences upon differential mobil-
ity in an acrylamide gel matrix of increasing denaturant
concentration; its application to food environments have
been recently reviewed by Temmerman, Huys, and Swings
(2004), Giraffa (2004) and Ercolini (2004). In particular,
the latter author reported that ‘‘PCR-DGGE applied to
template DNA directly extracted from a food matrix gener-
ates a specific profile of that product in that moment, given
the conditions used. The fingerprint gives a picture of the
microbiota of the product and can be taken into account
as a specific trait of that food just like other biochemical,
structural, or sensorial properties’’. With this in mind
PCR-DGGE is exploited to take a photograph of sour-
dough at any moment. PCR-DGGE has been successfully
applied to the study of the LAB composition of fermented
cereal-based products (Ampe, Sirvent, & Zakhia, 2001;
ben Omar & Ampe, 2000; Meroth et al., 2004; Meroth
et al., 2003; Miambi, Guyot, & Ampe, 2002; Randazzo,
Heilig, Restuccia, Giudici, & Caggia, 2005) and to compare
sourdough LAB communities subjected to different fermen-
tation processes (Meroth et al., 2004; Meroth et al., 2003).
551
In particular, Meroth et al. (2003) used the comparison of
PCR-DGGE bands generated from unknown lactobacilli,
present in sourdough, with an identification ladder con-
structed with 13 sourdough associated Lactobacillus spe-
cies. In this case a second PCR-DGGE assay, using a
different primer pair, was necessary in order to differentiate
Lactobacillus crispatus from Lb. acidophilus and Lb. san-
franciscensis from Lb. pontis, as their migration distances
were identical. Randazzo et al. (2005) used this technique
to study the microbial communities of traditional Sicilian
sourdoughs. PCR-DGGE was useful to reveal the domi-
nance of Lb. sanfranciscensis and Lb. fermentum, but did
not discriminate between the closely related species Lacto-
bacillus kimchii and Lb. alimentarius.
Another culture-independent, nucleic acid-based strat-
egy, representing a rapid and useful tool for monitoring bac-
teria during food fermentation is multiplex PCR, a
methodology that permits, in the same reaction, simulta-
neous amplification of more than one locus (Chamberlain,
Gibbs, Ranier, Nguyen, & Caskey, 1988). Multiplex PCR
assays targeting different genes have been successfully
applied to identify lactobacilli from various environments
(Lucchini et al., 1998; Müller, Ehrmann, & Vogel, 2000b;
sourdough
total DNA extraction
mixed DNA
Grouping-multiplex PCR
agarose gel
differentiation of the 4
Lactobacillus groups
cut of bands
re-amplification of bands with
GC-clamp-incorporating primers
polyacrylamide gel
Lactobacillus species
identification of
denaturant
Fig. 6. Schematic view of multiplex PCR in combination with PCR-
DGGE for monitoring 16 sourdough Lactobacillus species.
552 A. Corsetti, L. Settanni / Food Research International 40 (2007) 539–558
Settanni et al., 2005a; Song et al., 2000; Torriani et al., 2001;
Yost & Nattress, 2000). With particular relevance to the
sourdough ecosystem, Müller et al. (2000b) employed a
multiplex PCR for simultaneously monitoring three Lacto-
bacillus species, withouth prior cultivation, during a labora-
tory-scale sourdough fermentation. In our laboratory, we
have developed a multiplex PCR assay utilizing primers that
were based on sequences derived from the 16S rRNA-
encoding DNA, the 16S–23S rRNA intergenic spacer region
and its flanking 23S rRNA gene (Settanni et al., 2005a)
allowing the in situ detection of a group of 16 sourdough-
associated lactobacilli at group level. The same multiplex
PCR has also been combined with a specific PCR-DGGE
system (Fig. 6) allowing the detection of the above 16 sour-
dough Lactobacillus species up to species level (Settanni
et al., 2006). The systems were then used to identify com-
monly Lactobacillus species isolated from sourdough (Val-
morri et al., 2006), to detect and isolate Lb. rossiae strains
(data not published) and to monitor changes in lactobacilli
population composition (work in preparation).
5. Concluding remarks
Studies of sourdough microbiology revealed a large bio-
diversity of microflora. Recently, molecular approaches
showed a high number of new species, mainly belonging
to Lactobacillus genus, isolated from sourdough made with
different types of flour, both at artisanal and industrial
level. However, at present very little is known about
the interactions among sourdough microorganisms and
between microorganisms and environmental factors, hence,
further investigations of microbial dynamics, with particu-
lar regards to lactobacilli and their interactions with subdo-
minant LAB species and other microorganism groups, are
needed in order to describe the real flora of sourdough eco-
systems. The actual trend of using defined starter cultures
to initiate sourdough fermentation has lead to an intense
study of sourdough microorganism properties, with
emphasis to the production of flavour compounds, their
capability to improve nutritional quality of final products
as well as the production of antimicrobial compounds
ensuring the stability of the typical flora over several
refreshments. The raising tendency is forwarded to better-
controlled processes which need a deep knowledge of such
properties in order to standardize the production of sour-
dough bread and to extend the use of sourdough to prod-
ucts other than bread such as healty snacks, biscuits and
several types of convenience foods. Culture-independent
methods are potent tools to follow strains showing positive
characteristics and, due to their rapidity and ability of anal-
ysing more sourdoughs a time, are gaining more and more
importance.
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