Aerobic Metabolism of Lactic Acid Bacteria

Aerobic Metabolism of Lactic Acid Bacteria
Author(s): S. Condon
Source: Irish Journal of Food Science and Technology, Vol. 7, No. 1 (1983), pp. 15-25
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Jr.J. FdSci. Technol 7: 15-25,1983
AEROBIC METABOLISM OF LACTIC ACID BACTERIA
S. Condon
Dairy and Food Microbiology Department, University College, Cork
INTRODUCTION
Discussion in thispaper is confined to bacteria of the generaStreptococcus, Leuconostoc,

Pediococcus and Lactobacillus which have proved interestingto food microbiologists.
The lactic acid fermentation is the accepted means by which these bacteria derive the
energy they need for growth from common carbohydrates. It is commonly believed that
these bacteria have no means other than fermentation of obtaining energy for growth but
this is not true in many cases. Oxygen involvement in the utilisation of several substrates
by many lactic acid bacteria has been demonstrated in our laboratory and elsewhere
(Table 1). In at least some of these instances e.g. the utilisation of glycerol, growthwas
oxygen dependent.
Lactic acid bacteria are variously classified as aerotolerant, micro-aerophilic or facult
atively anaerobic; none of these labels is completely satisfactory.The termaerotolerant

indicates that the bacteria can tolerate the oxygen concentration found in air i.e. 21%;
it usually further implies that the microorganisms do not use the oxygen in energy
deriving growth processes. Microaerophiles are organisms which cannot survive in air
because the oxygen concentration is too high; theygrow best in environmentscontaining
low levels of oxygen. Often inherent in this description is that the organisms utilise
oxygen in respiratorygrowthprocesses, but cannot cope with high concentrations of it.
Facultative anaerobes are microorganisms which grow in the presence or absence of air.
The term isusually applied to thosemicroorganisms capable of switchingfroman aerobic
to an anaerobic energyyieldingprocess provided a suitable substrateis available.
The inadequacy of these terms to decribed the relationships between lactic acid
bacteria and oxygen can be gauged froma studybyWhittenbury(36) inwhich he examined
growth patterns of some lactic acid bacteria in tubes of soft agar (rich)medium. In such
tubes the top fewmm were aerobic; the remainderwas graduallymore anaerobic with
increasing depth.
A strain of Str. faecalis grew uniformly throughout the tube with glucose as the
or possibly
energy substrate. This growth pattern was aerotolerant facultatively anaerobic
but not microaerophilic. Under exactly the same conditions strains of Leuc. mesenteroides
grew rapidly in a thin layerat the top andmore slowly inthe anaerobic part of the tubewith
a clear zone in between. These Leuconostoc bacteria rapidly utilise glucose aerobically
using molecular oxygen as an electron acceptor and anaerobically (more slowly) using a
heterolactic fermentation i.e. typical facultatively anaerobic behaviour. The clear zone
was due to hydrogenperoxide, a by-productof the aerobic utilisation of glucose diffusing
is

16 IR. J. FD. SCI. TECHNOL., VOL. 7, NO. 1
TABLE 1: Involvementof oxygen inmetabolism of variousmetabolites by whole cells

or cell extractsof lactic acid bacteria
Subtrate Bacterial genus Reference
Glu co se Lactobacillus 1-11

Strep tococcus 2,12-20
Leuconostoc 19,20
Fructose Streptococcus 13
Leuconostoc 19,20
Galactose Lactobacillus 21
Streptococcus 22
Lactose Streptococcus 22,23

Gluconate Leuconostoc 19,20
Mannitol Lactobacillus 1,7,10,11
Sorbitol Lactobacillus 1,10
Gly cerol Lactobacillus 1,5,9,24

Strep tococcus 13,24-26
Pediococcus 27
Fructose 1-6 diphosphate Lactobacillus 9
a-glycerophosphate Lactobacillus 5
Streptococcus 28
Dihydroxyacetone Lactobacillus 5,9
Pyruvate Lactobacillus 3,4,9,29
a-ketoglutarate Streptococcus 30
Lactate Lactobacillus 3,5,31
Streptococcus 12,13,32
Ethanol Lactobacillus 5
Streptococcus 33
Succinate Streptococcus 12
Butyrate Streptococcus 34,35
downwards and inhibitingdevelopment of the slower growing bacteria below it.When

cellobiose was the growth substrate a strain of L. plantarum reacted like a strict anaerobe
whereas with glycerol a strainof Str. faecium behaved as a strict aerobe. A strainof
L. cellobiosus grew only anaerobically on glucose; a later sparse growth in the more
aerobic part of the tubewas ascribed to the aerobic utilisation of acids diffusingupwards
from the anaerobic zone. In extreme environmental conditions the normal growth patterns
of some strainswere altered.A strainofPediococcus in the presence of 10% salt and a
strain of L. fructovorans at a temperature close to itsmaximum, grew in central zones in
the tube as might be expected ofmicroaerophiles.
These data indicate that any of the termsoften used to describe the relationshipof
lactic acid bacteriawith oxygen should be used with caution. A specificbacteriummay

CONDON: AEROBIC METABOLISMOF LACTIC ACID BACTERIA 17
behave as a strict anaerobe, a facultative anaerobe, a microaerophile or an aerotolerant
anaerobe depending on the growth substrateand/orother environmentalconditions.

A cytochrome electron transport system is a common feature of organismswhich
dissimilate organic compounds aerobically. A key property of lactic acid bacteria is that
they are incapable of synthesisinghemeporphyrins,essential components of cytochromes.
For this reason they are often classified as being catalase negative and cytochrome
oxidative phosphorylationnegative.
Such a classification should not go unqualified. Not all catalases are heme-proteins.
Non heme catalases, termed pseudocatalases, have been observed in all four genera of
lactic acid bacteria (37?42). In addition a few of these bacteria are evidentlycapable of
formingheme catalases (37,41-45) ifgrown in thepresence of hematin.
To classify lactic acid bacteria as cytochrome-oxidative phosphorylation negative
without qualification may also be erroneous. Cytochromes have been observed in some
strains grown in the presence of hematin (17, 44?47). These and other data have been
interpretedas evidence for oxidative phosphorylation principally in one strainof Str.
faecalis (16, 18, 43?48) but also in strainsof Str. lactis (17, 46) and in one of Leuc.
mesenteroides (17). The positive Str. faecalis data were obtained from cells (or extracts
of cells) grown in the presence (44 47) or absence (16,18,48) of hematin i.e.with and
without cytochromes.
TOXICITYOF AEROBICENVIRONMENTS
FOR LACTIC
ACID BACTERIA
Aerobic metabolism of any microorganisms involvesbiochemical reactionswhich are a

consequence of interactionsof themicroorganismswith oxygen. Oxygen enters through
the cell membrane as dioxygen molecules in aqueous solution.Dioxygen molecules are
not very reactivebut in the reducingatmosphere insidemicrobial cells they can acquire
one or two additional electrons and become much more reactive as superoxide anions
and hydrogen peroxide molecules. These, in furtherreactions,may be converted to the
highly reactivehydroxyl radicals and singletoxygenmolecules. Production and accumul
ation of such compounds may result in a toxic condition formicrobial cells unless they
are equipped with adequate protective systemswhich convert the toxicmetabolites into
harmless compounds.
Of the possible oxygenmetabolites only hydrogen peroxide is known to accumulate
to any significantextent, in cultures of lactic acid bacteria incubated under normal
aerobic conditions. Superoxide anion may be produced in significantquantities in some
cultures under hyperbaric oxygen or in the presence of chemical stimulants such as
plumbagin (1, 2). There are numerous reports of hydrogen peroxide accumulation by
lactic acid bacteria growing aerobically at the expense of various substrates (22, 23, 26,
35, 49-65). A few of these reports (23, 26, 51, 57, 58, 64) have shown that accumul
ation of hydrogen peroxide was autoinhibitory. In a survey of 20 strainsof Group N
streptococci in this laboratory (Fitzgerald, unpublished data) about half were inhibited
by aerobic growth in some circumstances; growth of the other half was unaffected by

aeration irrespective of other environmental conditions. The sensitive cultures all ac

cumulated hydrogen peroxide to levels greater than 0.2 mM and addition of catalase or
other hydrogenperoxide dismutingagents allowed growthat unaerated rates.The cultures
insensitiveto air failed to accumulate hydrogen peroxide, or accumulated levels towhich
theywere insensitive.Accumulation of peroxide to inhibitorylevels by sensitive strains
of lactic streptococci did not occur during all aerobic incubations; accumulation was
dependent on the carbohydratewhich the bacteria were metabolising. In our experience
air sensitive strainswere much less sensitivewhen growingaerobically at the expense of
glucose than at the expense of some other sugars such as lactose or galactose. Cells
growingaerobically on glucose accumulated hydrogen peroxide to about 0.2 mM which

later decreased, whereas galactose grown cells accumulated peroxide to 0.4 mM and
this level remained in the cultureswhich became more and more inhibited.Addition of
catalase allowed normal growthof the sensitivecultures in the galactosemedium (22).
Some strains of L. plantarum examined in this laboratory accumulated con
high
centrations of hydrogen peroxide in aerobic culture under certain conditions.With L.
plantarum P5 the hydrogen peroxide accumulated to 1.0?1.5 mM in aerobic glucose
cultures,when a very large inoculumwas used to seed the culture but this levelwas not
autoinhibitory (4, 60, 61). Resistance to relativelyhigh concentrations of hydrogen
peroxide by some lactobacillihas been previouslynoted (51).
It is our experience, therefore,that only some strainsof Group N streptococci and
L. plantarum can produce hydrogen peroxide in aerated cultures and accumulation to
autoinhibitory levels requires specific cultivation conditions such as growth of some

Group N streptococci in galactose or lactose media.
Production of hydrogen peroxide by a specific strainmay give it an advantage in a
mixed population as there are severalwell documented examples of hydrogen peroxide
produced by one culture and inhibitinganother (52,59,62,66,67).
Evidence of growth inhibition due to superoxide anion production by lactic acid
bacteria exposed to air has been sought in this laboratory.Cultures of Group N strepto
cocci being inhibitedby aerobic growth,were not relievedof the inhibitionby addition
of superoxide dimutase (SOD). Addition of a superoxide generating system (e.g. xan
thine plus xanthine oxidase) did not cause any obvious inhibition to mildely aerated
cultures. An air sensitive culture was shown to have an SOD activity but its concentration
varied little (2?3 fold) between aerated and unaerated cultures and between conditions
causing aeration inhibitionand conditions thatdid not cause problems (22).
There has been considerable debate about the presence of SOD inL. plantarum. In
theiroriginal proposal that anaeroboisis was caused solely by a lack of SOD Fridovich
and his colleagues (68,69) claimed thatL. plantarum did not take up 02 froman aerated
environment and therefore did not require a mechanism to deal with superoxide. How
ever, others have shown that L. plantarum strains do react with oxygen and are capable
of dismuting superoxide anion (3, 6, 70). The discrepancywas cleared up satisfactorily
when Archibald and Fridovich (1, 2) confirmed thatL. plantarum strainsdid reactwith
oxygen and that theywere capable of dismuting superoxide.However, the dismutation
systemwas not enzymatic but involveda veryhigh internalconcentration (20?25 mM)
of Mn+2 ion. In a survey(50) of representativestrainsof lactic acid bacteria they showed

that these bacteria usually have either an SOD enzyme or a highMn+2 intracellularpool
system to eliminate superoxide. The lactobacilli with two exceptions (which had neither
system and were very oxygen sensitive) leuconostocs and the pediococci had theMn+2
systemwhile the streptococci had a true SOD. In 1971 McCord et al (69) proposed
that superoxide anion had an essential role in oxygen toxicity.Undoubtedly, the anion
is an importantfactor but it is now apparent thatno single factor is sufficientto explain
why oxygen is toxic for some organismsand not forothers (71).
MECHANISM AND
OF HYDROGENPEROXIDEFORMATION
BREAKDOWN
The enzymes responsible for hydrogen peroxide synthesis in lactic acid bacteria are
flavoproteinoxidases (9, 31, 54, 55, 72). In air sensitiveGroup N streptococci growing
aerobically at the expense of hexoses, an NADH oxidase isprobably themain (if not the
sole) enzyme responsible forhydrogen peroxide synthesis(22,51). This enzyme catalyses
the removalof oxygen from solution on addition of NADH according to the equation:
NADH + 02 + H+-> NAD+ + H202
NADH oxidase was inducible by growthunder aerobic conditions and subject to some
formof catabolite repressionby glucose. Unaerated cultureshad low levelsof the enzyme
irrespectiveof the growth sugar.Aerobic galactose grown cells had much more of the
enzyme than aerobic glucose grown cells and accumulated much greater concentrations
of hydrogen peroxide (22).
The enzyme responsible for hydrogen peroxide accumulation when L. plantarum P5
cells are growingat the expense of glucose isnot an NADH oxidase. L. plantarum P5 had
an NADH oxidase activitywhich was inducibleby oxygen and itsactivitycorrelatedwell
with hydrogen peroxide accumulation (4). However, the enzyme activitydid not produce
hydrogen peroxide; instead it catalysed a 4 e~ reductionofNADH towater without the
release of peroxide as an intermediate.SimilarNADH oxidases have been noted inother
lactic acid bacteria (72, 73). The enzyme responsible for hydrogenperoxide synthesisin
aerobic glucose grownL. plantarum P5 cultureswas pyruvateoxidase (65, 74), previously
observed in other lactobacilli (3, 9, 31). It is a flavoproteinwhich catalyses the following
reaction:
pyruvate+ 02 + phosphate-> acetylphosphate + H202 + C02
At high pyruvate concentrations the hydrogen peroxide and pyruvatemolecules react

non-enzymatically to form acetate. Pyruvate oxidase was inducible by oxygen and its
concentration was always high in L. plantarum P5 cells which accumulated hydrogen
peroxide in glucosemedia (74).
Hydrogen peroxide synthesis by lactic acid bacteria utilising substratesother than
sugars has also been noted. Oxygen dependent utilisation of glycerolwith hydrogen
peroxide synthesishas been shown in several strainsof Lactobacillus C5.9). Pediococcus

pentosaceus (27) and Str. faecalis (26,28,75). The hydrogenperoxide synthesiswas due
to an a-glycerophosphate oxidase which catalysed the production of triose phosphate
in the process (9,26,27). A lactateoxidase systemwhich catalyses synthesisof hydrogen
peroxide has been observed in extracts of a strainof Str. cremoris in this laboratory.
Pyruvate did not serveas a substratewhichmakes itunlikely that the systemconsists of a
lactic dehydrogenase coupled to a NADH or pyruvate oxidase. A lactate oxidation
system inStr. faecium was also described by London (13) but hydrogenperoxide was not
detected as a product.
Since hydrogen peroxide is a toxic oxygen metabolite if allowed to accumulate to
high concentrations it is reasonable to expect that lactic acid bacteria that synthesise
hydrogen peroxide are also equipped to get ridof it.As mentioned earlier some lactic
bacteria have non-heme catalases (38?42) and somemay have heme catalases ifgrown
in the presence of hematin (37, 41?43). Probably the most widespread method of
dealing with peroxide in lacticacid bacteria isvia flavoproteinperoxidases (3,51, 55,75,
76) which utiliseNADH as reducingpower as follows:
NADH + H202 + H+-> NAD+ + 2H20
Unlike catalase NADH peroxidases require continuous metabolism to produce the

NADH needed to reduce hydrogen peroxide. However, peroxidases are generallymore
efficientat reductionof low concentrationsof hydrogen peroxide than catalases.
BENEFITSOF AEROBICMETABOLISM
PHYSIOLOGICAL
The production of hydrogen peroxide and possibly other toxic metabolites of oxygen
such as superoxide anion by oxidase enzymes of lactic acid bacteria must be hazardous
considering the reactive nature of these compounds. It is reasonable to assume that
oxidase systemswhich produce such toxic compounds would not have evolved unless
therewas some benefit for the cellswhich synthesisethese enzymes.One obvious benefit
is that the range of substrates that can be utilised under aerobic conditions iswider than
that utilised under anaerobic conditions (Table 1). For example, glycerol cannot be used
as a fermentation substrate on its own under anaerobic conditions because in its con
version to pyruvate two equivalents of pyridinenucleotide are reduced and only one is
reoxidised by lactic dehydrogenase.Some strainsmay utilise glycerol anaerobically in the
presence of an external electron acceptor such as fumarate (28, 77). Under aerobic con
ditions on the other hand regenerationof theoxidised formof pyridine nucleotide can
be accomplished with NADH oxidase and consequently glycerol can be utilised as sole
energysubstrateunder aerobic conditions by some lactic acid bacteria (Table 2).
Pyruvate oxidase can be obviously beneficial since it catalyses production of acetyl
phosphate which can be used for the synthesisof extra ATP by means of an acetate
kinase. Lactic acid bacteria which have these two enzymes can derive4 mol ATP permol
hexose metabolised under aerobic conditions, twice that which can be produced by
glycolysis under anaerobic conditions. Furthermore, since some lactic acid bacteria can

TABLE 2: Probable pathways of anaerobic and aerobic glycerolmetabolism in lactic

acid bacteria
Anaerobic Aerobic
Glycerol Glycerol
r Succinate ATP
^NAD^
Fumarate ADP ^
^NAD2^
Dihydroxyacetone L-a-glycerophosphate
ATP
^-02
ADPV'
^H202
Triosephosphatc Triosephosphate
2ATP ~v ~ NAD 2ADP NAD ,*>H2?H2?2

^
2ATP
^ %*
2ADP ^NADH2 V^NADH2*'?2
Pyruvate
1
Pyruvate
/
[^NADH^^
^
CNADH2 / NAD VNAD
J
Acetoin
Lactate Lactate
A*ute
The dotted lines indicate pathways which have not been established; lactate, acetate,
acetoin, C02 and H202 have been observed in aerobic glycerol cultures of different
lactic acid bacteria (26,27).
convert lactate to pyruvate, usually by means of an NAD independent lactic

dehydro
genase (78), they presumably can derive ATP throughaerobicmetabolism of lactate if
they have pyruvate oxidase and acetate kinase. All three enzymes have been demon
strated inL. plantarum strainP5 (Table 3). The end-productof such a sequence is acetate
which has been detected as a major end-product of aerobic metabolims of lactic acid
bacteria (6, 62, 65). In a detailed examination of the end-productsof glucose utilisation
by L. plantarum P5 in this laboratory lactatewas themajor end-productinboth aerobic
and anaerobic cultures as as the glucose concentration remained most
long high. When
of the glucose was utilised the aerobic culture decreased its rateof production of lactate
and began to accumulate acetate whereas the anaerobic culture continued to accumulate
lactate. When all the glucose was utilised the aerobic culturekept on producing acetate

TABLE 3: Probable pathway of oxygen dependent lactate utilisation in Lactobacillus

plantarum
Lactate
lacticdehydrogenase
|
Pyruvate
?2 "N
) pyruvate oxidase
H2?2 1
acetylphosphate
ADP
acetate kinase
J
ATP ?S
acetate
from lactate accumulated during glucose metabohsm until the acetate eventually ac
counted for 60?70% of the glucosemetabolism. In the anaerobic culture60?70% of the
glucose utilised was accounted for as lactate.
Another benefit of aerobic metabolism to lactic acid bacteria is the possibility of
greaterbiomass yields at the expense of specificamounts of a carbohydrateenergysource.
Such effects have been observed with several lactic acid bacteria here and elsewhere
(6, 18, 21). The greater yields are particularly noticeable at low sugar concentrations.
Yousten et al (6) observed a 25?30% increase inyield of aerobically grownL. plantarum
cultureswith glucose compared to anaerobic cultures.A 33% increase inaerobic compared
to anaerobic yield was also observed with an L. plantarum culture grown at the expense
of galactose (21). The yield coefficientforglucose was 58.2 (g dryweight/mol) in aerobic
cultures of an Str faecalis strain compared to 12.5 in anaerobic cultures. The latter
observation is quoted as evidence of non-hememediated oxidative phosphorylation in
Str. faecalis (18), as the magnitude of the difference between aerobic and anaerobic
yields could not be accounted forby substrate levelphosphorylation.
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Aerobic Metabolism of Lactic Acid Bacteria

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