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Fermented foods, feeds and beverages
Biotech Advs vol.l,pp 31-46, 1983 0734-9750/83 $0.00.+.50 Printed in Great Britain. All Rights Reserved. Copyright © Pergamon Press Ltd
FERMENTED FOODS, FEEDS AND BEVERAGES KEITH H. STEINKRAUS Institute of Food Science, Cornell University, Genevo, N e w York 14456, USA
ABSTRACT There has been a proliferation of books and papers dealing with the indigenous fermented foods/beverages of the world.
It is anticipated that
these foods/beverages will play an ever-increasingly important role in feeding both the developing and the developed world as population increases from approximately 4.5 billion to 6 billion by the year 2000 and to 8 to 12 billion people in the 21st century.
The indigenous fermented foods consist
of microbial protein grown on edible substrates.
Microbial or single cell
protein (SCP) per se continues to receive research and development attention.
It is likely to play an important role in feeding animals in
the future when it becomes competitive with soy protein.
It may play a
direct role in feeding humans in the future after its safety for feeding animals has been adequately demonstrated and it has been shown that it can be processed into foods acceptable to humans.
At the present time,
mushrooms, a form of microbial protein highly acceptable to humans, which can be grown readily on ligno-cellulosic and other agricultural and food processing wastes, offer considerable opportunity for expanding man's food supply. KEYWORDS Indigenous fermented foods; microbial protein; single-cell protein (SCP); edible mushrooms; fermented beverages
31
32
K.H. STEINKRAUS INDIGENOUS FERMENTED FOODS/BEVERAGES
Over the last few years,
there has been a proliferation
dealing directly or indirectly with the expanding fermented foods of the world. Fermentations"
their comprehensive
the indigenous
i.e., soybean,
peanut,
Promising Technologies
the supply of nutritious Ramakrishnan the fermented
indigenous
fermented
the Western diet. "Nutritionally
cassava, vegetables
and non-
in their "Microbial
Countries"
Processes:
covered a wide-range
of
that could expand and improve
food fQr the world. (1981) provided
foods of India. Wood
et al
i.e., alcoholic beverages,
food fermentations
(1979) and Batra
Modified Foods".
(1979)
for Developing
indigenous
Appleton
and Man" which
fermented milks etc.
The National Academy of Sciences
under-utilized
of Food
foods on the basis of their substrates,
to their products,
cheeses,
However,
"Microorganisms
rice, other cereals,
seafoods and according alcoholic beverages,
fermented
in the indigenou~
(1979) "Microbiology
remains the classic reference.
(1979) published summarized
Pederson's
of books and papers
interest
(1981)
Wang and Hesseltine discussed
Steinkraus
(1979)
(1979)
information
discussed
soy sauce,
described
on
"Mold-
the rather rapid introduction
foods such as yogurt,
Significant
comprehensive
of
tempe and miso into
and classified
Indigenous Fermented
Foods
Involving an
Alcoholic Fermentation". The fermented for Africa
foods of particular
(Muller,
1981); Mexico
sections of the world have been described
1981); Mainland
(Ulloa-Sosa
China
and Herrera,
been dealt with in greater detail, e.g.,
(Chiao,
1981);
soy sauce/miso
black bean sauce
1981) and sake (Nunokawa,
Steinkraus
(1981, 1983d)
industrialization investigations
occurring
organisms
for the processes, in the substrates.
foods.
necessary
for scale up or
He proposed
involved,
the optimum conditions
process
and
and nutritional changes
(1982) classified
the indigenous
foods into groups based upon those which utilized molds, utilized bacteria,
1981).
common to each fermentation
and biochemica] Ko
(Hua et al, 1981);
the conditions
fermented
into the basic questions
such as the essential parameters
described
of indigenous
have
(Wood, 1982); miso
(Abiose et al, 1982); Taiwanese (Gandjar,
(Ko,
1981). Certain fermentations
soybeans
in Indonesia
Indonesia
fermented
those which
those utilizing molds and yeasts and those using molds
FOODS, FEEDS AND BEVERAGES followed by bacterial and yeast fermentation.
33
Steinkraus (1982a) discussed
the interaction of microorganisms in production of fermented foods and beverages.
Saisithi (1982) emphasized the high acceptability,
ease of preparation,
low cost,
safety, digestibility and therapeutic properties of
traditional fermented foods in feeding and helping to solve problems of malnutrition in the developing countries. Steinkraus (1982b) summarized recent progress in preservation of food through fermentation at the International Conference on Chemistry and World Food Supplies (CHEMRAWN II, 1982).
A workshop sponsored by the Board on
Science and Technology for International Development (BOSTID) of the National Research Council as a follow-up of CHEMRAWN II gave a high priority to the utilization of fermentation for the bio-enrichment and nutritional improvement of food substrates through the application of indigenous food fermentations Steinkraus
(BOSTID, 1983).
(1982d, 1983b, 1983d) described the indigenous fermented foods
in terms of their potential usefulness as industrial resources.
These
included (I) fermentations involving proteolysis of vegetable proteins by microbial enzymes in the presence of salt and/or acid with production of amino acid/peptide mixtures with meat-like flavors (examples: Chinese soy sauce and Japanese miso);
(2) fermentations involving enzymic hydrolysis of
fish/shrimp or other marine animals in the presence of relatively high salt concentrations to produce meat-flavored sauces and pastes (examples: Philippine patis and bagoong);
(3) fermentations producing a meat-like
texture in cereal grain/legume substrates by means of fungal mycelium that knits the particles together (examples:Indonesian tempe and oncom);
(4)
fermentations in which ethanol is a major product (examples: primitive wines and beers);
(5) fermentations in which organic acids are major products
(examples: sauerkraut and pickles); and (6) fermentations involving the Koji principle in which microorganisms with desired enzymes are grown on a cereal grain or legume substrate to produce a crude enzyme concentrate that can be used to hydrolyze particular components in a fermentation. Steinkraus
(1983a) categorized indigenous fermentations into "solid-state
(solid substrate)" -no free moisture; "solid-substrate-submerged";
"semi
solid substrate"; "semi-solid-substrate-submerged";
"pulverized substrate-
submerged" and "submerged (substrate in solution).
Moo-Young et al (1983)
reviewed the principles of solid-substrate fermentation,
Steinkraus
(1983c)
34
K.H. STEINKRAUS
discussed
the important
fermented
foods from vegetables,
authoritative, published
comprehensive
(Steinkraus,
A set of references of fermentations Cooperative
role played by lactobacilli
cereals and legumes.
"Handbook
of Indigenous
In 1983, the Fermented Foods" was
that contains
additional
information
on a wide variety
are the "Annual Reports of the International
Research and Development
(Taguchi,
1978, 1979, 1980, 1981a,
Shurtleff
and Aoyagi
in Microbial
Engineering
Osaka University
Center for (ICME)"
(Japan)
1982b).
(1979) published
a popular book - The Book of Tempeh -
a wealth of detail on tempeh production
including recipes.
In 1980, they published
which deals primarily with establishing
and utilization
a book "Tempeh Production"
a tempeh factory for production
tempeh in the United States and elsewhere That same year they also published
(Shurtleff
and Aoyagi,
"Miso Production",
information
for anyone wishing to produce miso on a larger scale 198Ob).
In 1982, the Nestle Products Technical
Assistance
1989a).
(Shurtleff
Co. Lt., La-Tour de-Peilz,
Switzerland,
the central,
ed a special
basic research division of the Nestle Co, publish-
issue of "Nestle Research News 1980/81" which included an
summary of indigenous
Steinkraus,
and other food fermentations
(Farr,
1982;
1982c).
While it is clear that the indigenous attention
of
a source of practical
and Aoyagi,
excellent
of
1983e).
published by the Faculty of Engineering,
which contains
in the production
as valuable
food resources
there are undoubtedly many fermented by scientists
foods are getting increasing
for humanity,
it should be noted that
foods that have not as yet been noticed
in the Western world and, of those that have been described
date, many have been inadequately microorganisms,
fermented
biochemical
studied regarding
and nutritive
to
their essential
changes that occur in the
substrates. Indian Idli Reddy et al (1981) published food Idli.
an excellent
Several researchers
during the idli fermentation
(18.6% - Rao
(1967); 60.0% - Padhye and Salunkhe Vanaja
(1967), Ramakrishnam
review on the Indian fermented
have reported an increase
(1977)
(1961);
(1978)).
in methionine
10.6% - Steinkraus,
Rao (1961), Rajalakshmi
and Padhye and Salunkhe
(1978)
et al and
FOODS, FEEDS AND BEVERAGES reported an improvement
in nutritional
occur with an improved methionine al
(1967) reported a decrease
protein following
fermentation
value of the protein
content.
in Protein
and Khandawala,
essential
(PER) of the
et al (1962) and van Veen, et
of the idli was the same as that
mixture of ingredients.
that the idli fermentation
that would
On the other hand, van Veen et Efficiency Ratio
al (1967) reported that the digestibility of the unfermented
35
If it can be substantiated
utilizing Leuconostoc mesenteroides
organism can synthesize methionine
this will be of great nutritional
in legume/cereal
significance
are the first limiting amino acids in legumes. which can be easily accomplished
as the mixtures,
since methionine/cystine An idli-type fermentation
even under rather primitive
conditions
would be a low cost method of improving the protein quality. Dawadawa
(Daddawa)
Dawadawa
is an African fermented food that has been known for centuries
Nigeria and plays an important nutritional It is beginning Dawadawa
to get more attention
of the African
in the villages.
from researchers.
is a food produced by a natural,
cotyledons
role especially
uninoculated
fermentation
locust bean (Parkia filicoidea)
The brown-to-black
1980; and Ikenebomeh,
of the
a tree legume
found not only in Africa but in Southeast Asia and tropical (Eka, 1980; Campbell-Platt,
in
South America
1982).
coated seeds are removed from their pods, washed,
soaked
and boiled with added potash for up to 24 hours until swollen and softened. The hulls are then removed by pounding gently or rubbing between and the cotyledons The cotyledons
are then reboiled for about 30 minutes.
are drained and placed in a basket,
a hole in the ground lined with leaves. with leaves or plastic at ambient particularly
(25 to 35°C) temperature. bacilli,
develop
The cotyledons
calabash pot or
are then covered
the fermentation
types of bacteria,
in the fermenting beans producing viscous
resembles Japanese natto.
and auunoniacal.
The initial
In this
The beans change from
sweet beany odor becomes strongly
The bean mass is then exposed to the sun,
partially dries and darkens further. formed into round balls
Different
material which link the beans together,
light to dark brown in color. proteolytic
sacking,
sheeting and allowed to ferment for 48 to 72 hours
strands of mucilaginous respect,
the hands
The partially dried beans may then be
(5 cm in diameter)
or flattened
cakes depending upon
36
K.H. STEINKRAUS
the locality and then are further dried in the sun following which the dawadawa remains stable for at least a year
(Campbell-Platt,
1980).
Dawadawa is used in much the same ways bouillon or Maggi cubes are used in the Western world as a nutritious grains in soups and stews. in Northern Nigeria.
Dawadawa contains about 40% protein and 35% fat
making it a concentrated of protein
flavoring additive along with cereal
Consumption ranges from 1 to 7 grams/day/person
source of nutrients and the second cheapest source
(after groundnut)
in Nigeria.
Eka (1980) reported that thiamine
increased from 0.65 mg/iO0 grams in the unfermented beans to 1.35 mg/IO0 grams and riboflavin increased from 0.45 mg/iOO grams to 1.30 mg/IOO grams in the fermented dawadawa. Platt
(1964) and Leung, Busson and Jardin
increase in riboflavin,
(1968) reported a threefold
a sixfold increase in thiamine and a decrease of a
third in niacin during fermentation. The essential microorganisms
in the dawadawa have not been identified.
There is insufficient knowledge of the biochemical and nutritional changes that occur during the fermentation.
It appears that bacilli play an
important role but there are numerous bacteria present and it would be interesting to know if there is a sequence of microorganisms and why the substrate does not spoil or become toxic rather than yield a highly acceptable fermented food. Soy Sauce Soy sauces continue to be manufactured by small-scale traditional processes as well as by modern large scale factories such as the one built by Kikkoman Co. in Walworth, Wisconsin. Bhumiratana et al (1980)
studied five different
soy sauce strains of
Aspergillus and one of Mucor for proteolytic activity.
A strain of
Aspergillus flavus var. columnaris with superior protease production showed no detectable aflatoxin production on glutinous rice or soybean and yielded a soy sauce of superior quality in a traditional
soy sauce factory.
Impoolsup et al (1981) found that A. flavus var. columnaris produced two major proteases,
an alkaline and a neutral protease, both of which appeared
in the late phase of fungal growth.
These results lead to a recommendation
FOODS, FEEDS AND BEVERAGES
37
that koji, beans covered with mold growth, be transferred in two days rather than the traditional
4 to 7 days.
production
facilities
production
and overall quality of the soy sauce.
another modification
by more than twice thus improving both efficiency
of
This group is also trying
of the process in which the two day-old koji is
incubated at 50 to 55°C for I or 2 hours to maximize submersion
to the salt brine
This expands koji
in the salt brine where the proteolytic
proteolysis
prior to
activity is inhibited
85
to 90%. Flegel et al (1982) emphasized
that soy sauce manufacturers
prefer a "green" koji indicative koji indicative
of Rhizopus,
of As~ergillus
Mucor etc.
in Thailand
oryzae rather than "black"
Green kojis are generally more
common in cool weather and the black kojis occur more frequently weather. sauces.
They referred to white crystalline materials The crystals proved to be pure tyrosine.
in hot
found in some soy
They also referred
to an
improved method of producing dry spore inoculum on rice starch in plastic bags. Indonesian Tape Indonesian Tape, Malaysian Tapai, Thai Kaomag are sweet/sour products highly appreciated reviewed by Steinkraus organisms
present
Predominant
mold-like
were isolated.
Towprayoon
Takada et al (1981)
Torulopsis.
rice
and Kootin
(1982)
studied the
a mold bran inoculum for making Thai kaomag.
yeasts.
yeast-like molds, and
Molds belonging
rouxii, Endomyqopsis
studied the microflora
an inoculum available
Mucor, Rhizopus
alcoholic
Production has been
to Mucor and Rhizo~us
also
Kaomag with superior flavor was produced using a mixed
inoculum of Amylomyces
contained
(1983e).
in loogpang,
in Asia.
organisms found were Amylomyces,
E ndomycopsis,
Loog pang,
as a dessert
and Aspergillus
Lactobacilli
fibuliger and Hansenula
anomala
in various Thai fermented
foods.
on the market,
contained molds of genera
plus yeasts of genera Candida and
were predominant
some Candida and Torulopsis
in koe mug (kaomag) but it also
yeasts.
Pediococci
dominated
the
thua nao fermentations. Fish Sauces Tongthai
and Okada
(1981) divided
tion into three stages:
the nampla
(numpla)
fish sauce fermenta-
early, during which soluble nitrogen
acids increase very rapidly due to exopeptodase
originating
and free amino in the fish
38
K.H. STE INKRAUS
tissue itself;
middle (5th to 20th weeks), when endopeptodases are
predominant; and the late stage (20th to 50th weeks), during which time halophiles become active. Japanese Ko$i Kojis, crude enzyme sources for the production of soy sauce,miso, sake etc. are generally prepared by incubation in open systems where it is possible for contaminating organisms to invade the developing koji.
Takano et al
(1982) studied the use of selected lactobacilli inoculated along with Aspergillus oryzae to inhibit growth of contaminants such as Bacillus subtilis and Micrococcus luteus.
They found that Pediococcus cerevisiae in
populations of 105 to 106 cells/gram dry koji inhibited the growth of 104 cells of Bacillus subtilis inoculated as a contaminant. Nigerian Millet Beer ("Oyokpo") Nkanga and Uraih (1981) improved the quality of native millet beer - Oyokpo by better control of germination (malting)and use of a pure culture of Saccharomyces cerevisiae. Kenyan uji Mbugua (1981) reported that coliforms were active early in the fermentation of the East African acid cereal porridge--Uji.
The major lactic species
isolated from fermenting Uji was Lactobaeillus plantarum.
Inoculation with
Leuconostoc mesenteroides inhibited development of coliforms and resulted in an improved flavor and aroma in the product. MICROBIAL/SINGLE CELL PROTEIN (SCP) In 1980, BioScience, the publication of the American Institute of Biological Sciences devoted a special issue to "Food from Microbes".
The
viewpoint presented was that microbes especially in the form of indigenous fermented foods will likely play an important role in feeding animals and humanity in the future (Steinkraus, 1980).
The consumption of microbes
directly as food by man (except for mushrooms) requires considerably more research, development and study (Waslien and Steinkraus, 1980). Litchfield
(1980) reviewed the status of microbial protein production
including algae, bacteria and fungi.
Algal production is limited by the
amount of available sunlight, the carbon dioxide content of the water,
FOODS, FEEDS AND BEVERAGES suitable pH of the water,
suitable
concentrations
39 of nitrogen,
and minerals.
Ponds must be agitated by mechanical
recirculation.
Yields are relatively
phosphorus
agitation or
low 1 to 2 grams/liter
and harvesting
is difficult. Imperial Chemical the largest methanol.
Industries,
installations
Ltd.
(ICI) in England have developed
growing bacteria
Methylophilus
protein and is used in animal feeds. Minnesota,
(Candida utilis) on an ethanol
substrates
cheese-whey,
processing waste,
process
methane,
bagasse,
carob bean extract,
cornstarch
in which Paecilomyces
Crude protein content
associates
(1979) developed
cellulolyticum
SO 2 is stripped
is 0.55 g/gram reducing
Total production
Air
from
sugar.
is 15 to 16.5 tons of Moo-Young
and
a pilot plant process growing Chaeotomium corns over cellulosic
Protein content of the product
(1980) suggested
aerobically
cellulosic waste and
is used for animal feeds.
on solid-substrate
and sawdust.
coffee-
vaiota is grown on spent sulfite liquor.
is 52-57%.
The product
waste,
of
potato
is the Finnish "Pekilo"
sterile to two fermentors.
Yield of microorganism
dry mycelium/day.
production
purified n-alkanes,
corn wet-milling
The largest fungal process at present
the substrate.
Meyer
ethanol,
sulfite waste liquor,
and ammonia are supplied
wastes
70-72%
substrate.
being used in pilot plant and commercial
SCP include methanol,
sawdust.
Pruteen contains
Amoco Foods co., Hutchinson,
a subsidiary of Standard Oil Co. of Indiana is producing human
food grade yeast
waste,
on
The factory can produce 70,000 tons of "Pruteen" per year or
nearly 192 tons per day in a continuous process.
Present
one of
methylotrophus
that "Carboxydobacteria",
and other farm
is about 45%.
bacteria able to grow
on CO as their sole source of carbon and energy be used to
reduce the environmental
levels of carbon monoxide
and also yield microbial
protein for feeding animals and man. Rank, Hovis and MacDougall
developed
edible mold is grown on low-cost combined with meat flavorings for human consumption
(Spicer,
a fermentation
carbohydrates,
process
and fats to produce a quality meat substitute 1971a,
1971b).
Recently the product has
been accepted by the British Food and Drug Administration consumption
in which an
recovered by filtration,
and it can be anticipated
that production
the RHM meat analogues will be expanded
as safe for human
and consumption
in the coming years.
of
40
K.H. STEINKRAUS
Takahashi
(1982)
reviewed the present status of SCP and showed how
efficiency of SCP production using normal alkanes as substrate could be greatly inproved by operating the fermentor under approximately 4 atmospheres pressure. Hesseltine and Wang
(1980) and Steinkraus
(1980) support the idea that
consumption of microbial protein in the form of traditional fermented foods remains one of the best ways of improving the human diet. Mushrooms The most direct and the most acceptable form of microbial protein available today in both the developed and developing world is mushroom which can be cultivated on lignocellulosic
and other agricultural and food wastes.
Mushrooms are being extensively produced and consumed in Asia today and most people in the world rich and poor alike find them a very acceptable food. (1980).
The subject of mushrooms
as human food has been reviewed by Chang
Fresh mushrooms of the Agaricus, Volvariella and Pleurotus types
contain generally more than 3% protein, essential versus 99 for milk, nutritional
amino acid indices of 98
amino acid scores of 89 versus 91 for milk and
indices of 28 versus 25 for milk and 31 for soybeans.
One kilogram of dry composting material will yield as much as 1 kilogram of fresh mushrooms
in 3 or 4 flushes over a period of 30 to 45 days.
yield is 600-750 grams of fresh mushrooms/kg dry compost.
there are an estimated 2325 million tons of straw produced per year 1977) over half of which may be burned, to produce approximately efficiency)
(FAO,
straw could be used as a substrate
1511 million tons of fresh mushrooms
(65%
or 336 kg of fresh mushrooms annually for each of the present
4.5 billion human inhabitants of the earth about 28 g of protein per person/day). lignocellulosic and other wastes
(920 g fresh mushrooms containing
Microbial protein production on
should be exploited to the fullest as an
adjunct to the world's supply of food and protein. mushrooms,
Usual
Considering that
Following growth of the
the spent beds can be used as a protein-enriched
supplement for
cattle and other animals, used as a nitrogen enriched soil conditioner or used as sources of cellulases and lignases for the hydrolysis of other lignocellulosic
substrates for the production of fermentation products.
FOODS, FEEDS AND BEVERAGES
41
REFERENCES i.
S.H. Abiose, M.C. Allan and B.J.B. Wood, Microbiology and biochemistry of miso (soy paste)fermentation,
in Adv. in Applied Micro., 28, 239-
265 (1982). 2.
J.M. Appleton, V.F. McGowan and V.B.D. Skerman, Microorganisms and ~lan, UNESCO/UNEP Publication under Contract No. 258117, World Data Center, Brisbane
3.
(1979).
L.R. Batra, Fermented cereals and grain legumes of India and vicinity, in Advances in Biotechnology, M.Moo-Young et al (Eds.), Pergamon Press, II, 547-553 (1981).
4.
A. Bhumiratana, T.W. Flegel, T. Glinsukon and We Somporan, Isolation and analysis of molds from soy sauce koji in Thailand, Appl~ and Environ. Micro., 39, 430-435 (1980).
5.
Board on Science and Technology for International Development
(BOSTID),
Chemistry and World Food Supplies, Report of a Workshop following CHEMRA~q II, National Academy Press (1983). 6.
G. Campbell-Platt, African locust bean (Parkia species) and its West African fermented food product, dawada, Ecology of Food and Nutrition, ~, 123-132.
7.
S.T. Chang, Mushrooms as human food, BioScience, 30, 399-401 (1980)~
8.
J.S. Chiao, Modernization of traditional Chinese fermented foods and beverages,
in Advances in Biotechnology, M.Moo-Young et al (Eds.),
Pergamon Press, I I, 511-516 (1981). 9.
O.U. Eka, Effect of fermentation on the nutrient status of locust beans. Food Chem., ~, 303-308 (1980).
i0.
D. Farr, Traditional fermented foods: a great potential for the future, Nestle Research News 1980/81, pp. 31-37 (1982).
II.
T.W. Flegel, A. Bhumiratana, A. Impoolsup, N. Takada, Y. Oshima and H. Okada, Studies on Aspergillus flavus vat. columnaris in soy sauce koji, in Microbial Utilization of Renewable Resources, Vol. 2, H. Taguchi
(Ed.), ICME, Faculty of Engineering, Osaka University, Osaka,
Japan, pp. 59-63 (1982). 12.
Food and Agricultural Organization of the United Nations
(FAO), 1977
FAO production yearbook, FAO, Rome, Italy (1978). 13.
I. Gandjar, Soybean fermentation in Indonesia, in Advances in Biotechnology, M.Moo-Young et al (Eds.), Pergamon Press, II, 531-534. (1981).
K.H. STEINKRAUS
42
14.
C.W. Hesseltine and H.L. Wang, The importance of traditional fermented
15.
J. Hua, I.H. Wang, S.K. Chen and W.H. Hsu, Fermented sauce made from
foods, BioScience, 30, 402-404 (1980).
black soybean,
(Inyu), Advances in Biotechnology, M.Moo-Young
Pergamon Press, II, 517-523 16.
(Ed),
(1981).
M.J. Ikenebomeh, The Solid Substrate Fermentation of African Locust Beans (Parkia filicoidea Welw.), P h . D .
Thesis, McGill University
(1982). 17.
A. Impoolsup, A. Bhumiratana and T.W. Flegel, Isolation of alkaline and neutral proteases from Aspergillus flavus var. columnaris, a soy sauce koji mold, Appl. and Environ. Micro., 42, 619-628 (1981).
18.
P.K. Khandwala, S.D. Ambegaokar,
S.M. Patel, M.V. Radhakrishna Rao,
studies in fermented foods, I. Nutritive value of idli, J. Sci. Ind. Res. 19
(india), 21C, 275-278.
S.D. Ko, fermented foods of Indonesia except those based on soybeans, in Advances in Biotechnology, M.Moo-Young et al. (Eds), Pergamon Press, I I, 525-530 (1981).
20.
S.D. Ko, Indigenous fermented foods, in Fermented Foods, Economic Microbiology, Vol. 7, A.H. Rose (Ed.), Academic Press, pp. 15-38 (1982).
21.
W.T.W. Leung, F. Busson and C. Jardin, Food Composition Tables for Use in Africa, U.S. Dept. of Health/Food and Agricultural Organization of United Nations (FAO), Bethesda, Maryland
22.
(1968).
J.H. Litchfield, Microbial protein production, BioScience, 30, 387396 (1980).
23.
S.K. Mbugua, Microbiological and Biochemical Aspects of Uji (an East African Sour Cereal Porridge) Fermentation, and Its Enhancement Through Application of Lactic Acid Bacteria, Ph.D. Thesis, Cornell University
(1981).
24.
O. Meyer, Using carbon monoxide to produce single-cell protein,
25.
M, Moo-Young, A.J. Daugulis, D.S. Chahal and D.G. MacDonald, The
BioScience, 30, 405-407 (1980).
Waterloo process for SCP production from waste biomass, Process Biochem., 14(10), 38-40 (1979). 26.
M. Moo-Young
(General Editor), Advances in Biotechnology, Vol. II,
Fuels, Chemicals, Foods and Waste Treatment, Pergamon Press (1981). 27.
M. Moo-Young, A.R. Moreira and R.P. Te~gerdy, Principles of solidsubstrate Fermentation,
in The Filamentous Fungi, Vol. IV, Fungal
FOODS, FEEDS AND BEVERAGES
43
Technology, J.E. Smith, D.R. Berry and B. Kristiansen (Eds.), Edward Arnold, pp. 117-144 (1983). 28. H.G. Muller, Fermented cereal products of tropical Africa, Advances in Biotechnology, M.Moo-Young et al, Pergamon Press, II, 541-546 (1981). 29. National Academy of Sciences (NAS), Microbial Processes: Promising Technologies for Developing Countries, National Academy of Sciences (1979). 30. Nestle Products Technical Assistance Company Ltd., Nestle Research News 1980/81 (1982). 31. E.I. Nkanga and N. Uraih, Improved brewing of millet beer-(OYOKPO) and production of single cell proteins from the spent grains, Acta Biotechnologica, (DDR), ~, 153-159 (1981). 32. Y. Nunokawa, Enzymes affecting the fermentation of sake moromi-mash, in Advances in Biotechnology, M.Moo-Young et al. (Eds.), Pergamon Press, II, 563-568 (1981). 33. V.W. Padhye and D.K. Salunkhe, Biochemical studies on black gram (Phaseolus mumgo L.), III. Fermentation of black gram and rice blend and its influence on the in vitro digestibility of the proteins, J. Food Biochem., ~, 327-347. 34. C.S. Pederson, Microbiology of Food Fermentations, 2nd Edition, AVI Press (1979). 35. B.S. Platt, Biological ennoblement: improvement of the nutritive value of foods and dietary regimens by biological agencies.
Food Tech., 18,
68-76 (1964). 36. R. Rajalakshmi and K. Vanaja, Chemical and biological evaluation of the effects of fermentation on the nutritive value of foods prepared from rice and grams, Brit. J. Nutr., 21, 467-473. 37. C.V. Ramakrishnan, Study of Indian fermented foods from legumes and production of similar fermented foods from soybeans, Fourth Annual Research Report, pp.l-77, M.S. University of Baroda, Baroda, India (1977) 38. C.V. Ramakrishnan, Studies on Indian fermented foods, Baroda J. Nutrition, 6, 1-54 (1979). 39. N.R. Reddy, S.K. Sathe, M.D. Pierson and D.K. Salunkhe, An Indian fermented food: a review, J. Food Quality, 5, 89-101 (1981). 40. P. Saisithi, Roles of fermented foods in solving nutritional problems, in H. Taguchi (Ed.), Microbial Utilization of Renewable Resources.
44
K.H. STEINKRAUS Vol.2 ICME, University of Osaka, Osaka, Japan, pp. 200-210 (1982).
41. W. Shurtleff and A. Aoyagi, The Book of Tempeh, Harper and Row (1979). 42. W. Shurtleff and A. Aoyagi, Tempeh Production, New-Age Foods Study Center
(1980a).
43. W. Shurtleff and A. Aoyagi, Miso Production, New-Age Foods Study Center
(1980b). 44. A. Spicer, Synthetic proteins for human and animal consumption, Vet. Record, 89, 482-487 (1971a). 45. A. Spieer, Protein production by microfungi, Trop. Sci., XIII, 239-250 (1971b). 46. K.H. Steinkraus, A.G. Van Veen and D.B. Thiebeau, Studies on Idli--An Indian fermented black gram-rice food, Food Technol., 21, 110-113 (1967). 47, K.H. Steinkraus, Nutritionally significant indigenous fermented foods involving an alcoholic fermentation, in Fermented Food Beverages in Nutrition, C.F. Gastineau, W.J. Darby and T.B. Turner (Eds.), Academic Press, pp. 35-59 (1979). 48. K.H. Steinkraus, Introduction: food from microbes, BioScience, 30, 384-386 (1980). 49. K.H. Steinkraus, Industrialization of home and village food fermentations, in Advances in Biotechnology, M.Moo-Young et al. (Eds.), Pergamon Press, II, 473-478 (1981). 50. K,H. Steinkraus, Fermented foods and beverages: the role of mixed cultures, in Microbial Interactions and Communities, Vol. i, A.T. Bull and J.H. Slater (Eds.), Academic Press, pp. 407-442 (1982a). 51. K.H. Steinkraus, Progress in preservation of food through fermentation, Presented at CHEMRAWN II, Manila, Philippines (1982b). 52. K.H. Steinkraus, The indigenous fermented foods, Nestle Research News. 1980/81, pp, 23-28 (1982c). 53. K.H. Steinkraus, Traditional food fermentation as industrial resources, in Traditional Food Fermentation as Industrial Resources, S. Saono, F.G. Winarno and D. Karjadi (Eds.), Indonesian Institute of Sciences (LIPI), Jakarta, Indonesia, pp. 3-16 (1982d). 54. K.H. Steinkraus, Solid-state (solid-substrate) food/beverage fermentation involving fungi, Acta Biotechnologica (DDR), In Press (1983a). 55. K.N. Steinkraus, Traditional food fermentations as industrial resources Acta Biotechnologica (DDR), ~, 1-12 (1983b).
FOODS, FEEDS AND BEVERAGES 56.
45
K.H. Steinkraus, Lactic acid fermentation in the production of foods from vegetables, cereals and legumes, Antonie van Leeuwenhoek, In Press (1983c).
57.
K.H. Steinkraus, Industrial applications of Oriental fungal fermentations, in The Filamentous Fungi, Vol. IV, J.E. Smith, D.R. Berry and B. Kristiansen (Eds.) Edward Arnold, pp. 171-189 (1983d).
58.
K.H. Steinkraus, Handbook of Indigenous Fermented Foods, Marcel Dekker
59.
H. Taguchi, Annual Reports of International Center of Cooperative
Inc. (1983e).
Research and Development in Mirobial Engineering (ICME), Faculty of Engineering, Osaka University, Osaka, Japan (1978), (1979), (1980), (1981), (1982). 60.
N.Takada,T. Iwashiro, J. Yagyu, A. Bhumiratana, T. Flegel and Y. Oshima, Microflora in Various Thai fermented foods, in Microbial Utilization of Renewable Resources, Vol. I, H. Taguchi (Ed.), ICME, Faculty of Engineering, Osaka University, Osaka, Japan, pp. 85-91 (1981).
61.
J. Takahashi, Present status of single cell protein-with some aspects of gaseous alkanes as novel substrates, in Microbial Utilization of Renewable Resources, Vol. 2, H. Taguchi (Ed.) ICME, Faculty of Engineering, Osaka University, Osaka, Japan, pp. 40-46 (1982).
62.
M. Takano, B.K. Datta and I. Shibasaki, Lactic acid bacteria as a safe additive for koji process, in Microbial Utilization of Renewable Resources, Vol. 2, H. Taguchi (Ed.), ICME, Faculty of Engineering, Osaka University, Osaka, Japan, pp. 24-32 (1982).
63
C. Tongthai and H. Okada, Change of nitrogenous compounds during numpla fermentation, in Microbial Utilization of Renewable Resources, Vol. I, H. Taguchi (Ed.), ICME, Faculty of Engineering, Osaka University, Osaka, Japan, pp. 101-107 (1981).
64.
S. Towprayoon and S. Kootin, Fermentation of sweetened rice by pure culture, in Microbial Utilization of Renewable Resources, Vol. 2, H. Taguchi (Ed.), ICME, Faculty of Engineering, Osaka University, Osaka, Japan, pp.20-23 (1982).
65. M. Ulloa-Sopsa and T. Herrer, Fermented corn products of Mexico. Advances in Biotechnology, M.Moo-Young et al.
(Eds.), Pergamon Press,
II, 535-540 (1981). 66. A.G. Van Veen, L.R. Hackler, K.H. Steinkraus and S.K. Mukherjee, Nutritive quality of idli, a fermented food of India, J. Food Sci., 32, 339" 341 (1967).
46
K.H. STEINKRAUS
67. H.L. Wang and C.W. Hesseltine, Mold-modified foods, in Microhial Technology, Vol. II, A.H, Rose (Ed~), Academic Press, pp. 95-129 (1979). 68. C.I. Waslien and K.H~ Steinkraus, The potential of microbial cells as protein for man. BioScience, 30, 397-398. 69. B.J.B. Wood, Introduction of new fermented foods into western culture, in Advances in Biotechnology, M.Moo-Young et al. (Edso), Pergamon Press, II, 467-472
(1981).
70. B.J.B. Wood, Soy sauce and miso, in Fermented Foods, Vol. 7, Economic Microbiology, A.H. Rose (Ed,), Academic Press, pp. 39-86 (1982).
FERMENTED FOODS, FEEDS AND BEVERAGES KEITH H. STEINKRAUS Institute of Food Science, Cornell University, Genevo, N e w York 14456, USA
ABSTRACT There has been a proliferation of books and papers dealing with the indigenous fermented foods/beverages of the world.
It is anticipated that
these foods/beverages will play an ever-increasingly important role in feeding both the developing and the developed world as population increases from approximately 4.5 billion to 6 billion by the year 2000 and to 8 to 12 billion people in the 21st century.
The indigenous fermented foods consist
of microbial protein grown on edible substrates.
Microbial or single cell
protein (SCP) per se continues to receive research and development attention.
It is likely to play an important role in feeding animals in
the future when it becomes competitive with soy protein.
It may play a
direct role in feeding humans in the future after its safety for feeding animals has been adequately demonstrated and it has been shown that it can be processed into foods acceptable to humans.
At the present time,
mushrooms, a form of microbial protein highly acceptable to humans, which can be grown readily on ligno-cellulosic and other agricultural and food processing wastes, offer considerable opportunity for expanding man's food supply. KEYWORDS Indigenous fermented foods; microbial protein; single-cell protein (SCP); edible mushrooms; fermented beverages
31
32
K.H. STEINKRAUS INDIGENOUS FERMENTED FOODS/BEVERAGES
Over the last few years,
there has been a proliferation
dealing directly or indirectly with the expanding fermented foods of the world. Fermentations"
their comprehensive
the indigenous
i.e., soybean,
peanut,
Promising Technologies
the supply of nutritious Ramakrishnan the fermented
indigenous
fermented
the Western diet. "Nutritionally
cassava, vegetables
and non-
in their "Microbial
Countries"
Processes:
covered a wide-range
of
that could expand and improve
food fQr the world. (1981) provided
foods of India. Wood
et al
i.e., alcoholic beverages,
food fermentations
(1979) and Batra
Modified Foods".
(1979)
for Developing
indigenous
Appleton
and Man" which
fermented milks etc.
The National Academy of Sciences
under-utilized
of Food
foods on the basis of their substrates,
to their products,
cheeses,
However,
"Microorganisms
rice, other cereals,
seafoods and according alcoholic beverages,
fermented
in the indigenou~
(1979) "Microbiology
remains the classic reference.
(1979) published summarized
Pederson's
of books and papers
interest
(1981)
Wang and Hesseltine discussed
Steinkraus
(1979)
(1979)
information
discussed
soy sauce,
described
on
"Mold-
the rather rapid introduction
foods such as yogurt,
Significant
comprehensive
of
tempe and miso into
and classified
Indigenous Fermented
Foods
Involving an
Alcoholic Fermentation". The fermented for Africa
foods of particular
(Muller,
1981); Mexico
sections of the world have been described
1981); Mainland
(Ulloa-Sosa
China
and Herrera,
been dealt with in greater detail, e.g.,
(Chiao,
1981);
soy sauce/miso
black bean sauce
1981) and sake (Nunokawa,
Steinkraus
(1981, 1983d)
industrialization investigations
occurring
organisms
for the processes, in the substrates.
foods.
necessary
for scale up or
He proposed
involved,
the optimum conditions
process
and
and nutritional changes
(1982) classified
the indigenous
foods into groups based upon those which utilized molds, utilized bacteria,
1981).
common to each fermentation
and biochemica] Ko
(Hua et al, 1981);
the conditions
fermented
into the basic questions
such as the essential parameters
described
of indigenous
have
(Wood, 1982); miso
(Abiose et al, 1982); Taiwanese (Gandjar,
(Ko,
1981). Certain fermentations
soybeans
in Indonesia
Indonesia
fermented
those which
those utilizing molds and yeasts and those using molds
FOODS, FEEDS AND BEVERAGES followed by bacterial and yeast fermentation.
33
Steinkraus (1982a) discussed
the interaction of microorganisms in production of fermented foods and beverages.
Saisithi (1982) emphasized the high acceptability,
ease of preparation,
low cost,
safety, digestibility and therapeutic properties of
traditional fermented foods in feeding and helping to solve problems of malnutrition in the developing countries. Steinkraus (1982b) summarized recent progress in preservation of food through fermentation at the International Conference on Chemistry and World Food Supplies (CHEMRAWN II, 1982).
A workshop sponsored by the Board on
Science and Technology for International Development (BOSTID) of the National Research Council as a follow-up of CHEMRAWN II gave a high priority to the utilization of fermentation for the bio-enrichment and nutritional improvement of food substrates through the application of indigenous food fermentations Steinkraus
(BOSTID, 1983).
(1982d, 1983b, 1983d) described the indigenous fermented foods
in terms of their potential usefulness as industrial resources.
These
included (I) fermentations involving proteolysis of vegetable proteins by microbial enzymes in the presence of salt and/or acid with production of amino acid/peptide mixtures with meat-like flavors (examples: Chinese soy sauce and Japanese miso);
(2) fermentations involving enzymic hydrolysis of
fish/shrimp or other marine animals in the presence of relatively high salt concentrations to produce meat-flavored sauces and pastes (examples: Philippine patis and bagoong);
(3) fermentations producing a meat-like
texture in cereal grain/legume substrates by means of fungal mycelium that knits the particles together (examples:Indonesian tempe and oncom);
(4)
fermentations in which ethanol is a major product (examples: primitive wines and beers);
(5) fermentations in which organic acids are major products
(examples: sauerkraut and pickles); and (6) fermentations involving the Koji principle in which microorganisms with desired enzymes are grown on a cereal grain or legume substrate to produce a crude enzyme concentrate that can be used to hydrolyze particular components in a fermentation. Steinkraus
(1983a) categorized indigenous fermentations into "solid-state
(solid substrate)" -no free moisture; "solid-substrate-submerged";
"semi
solid substrate"; "semi-solid-substrate-submerged";
"pulverized substrate-
submerged" and "submerged (substrate in solution).
Moo-Young et al (1983)
reviewed the principles of solid-substrate fermentation,
Steinkraus
(1983c)
34
K.H. STEINKRAUS
discussed
the important
fermented
foods from vegetables,
authoritative, published
comprehensive
(Steinkraus,
A set of references of fermentations Cooperative
role played by lactobacilli
cereals and legumes.
"Handbook
of Indigenous
In 1983, the Fermented Foods" was
that contains
additional
information
on a wide variety
are the "Annual Reports of the International
Research and Development
(Taguchi,
1978, 1979, 1980, 1981a,
Shurtleff
and Aoyagi
in Microbial
Engineering
Osaka University
Center for (ICME)"
(Japan)
1982b).
(1979) published
a popular book - The Book of Tempeh -
a wealth of detail on tempeh production
including recipes.
In 1980, they published
which deals primarily with establishing
and utilization
a book "Tempeh Production"
a tempeh factory for production
tempeh in the United States and elsewhere That same year they also published
(Shurtleff
and Aoyagi,
"Miso Production",
information
for anyone wishing to produce miso on a larger scale 198Ob).
In 1982, the Nestle Products Technical
Assistance
1989a).
(Shurtleff
Co. Lt., La-Tour de-Peilz,
Switzerland,
the central,
ed a special
basic research division of the Nestle Co, publish-
issue of "Nestle Research News 1980/81" which included an
summary of indigenous
Steinkraus,
and other food fermentations
(Farr,
1982;
1982c).
While it is clear that the indigenous attention
of
a source of practical
and Aoyagi,
excellent
of
1983e).
published by the Faculty of Engineering,
which contains
in the production
as valuable
food resources
there are undoubtedly many fermented by scientists
foods are getting increasing
for humanity,
it should be noted that
foods that have not as yet been noticed
in the Western world and, of those that have been described
date, many have been inadequately microorganisms,
fermented
biochemical
studied regarding
and nutritive
to
their essential
changes that occur in the
substrates. Indian Idli Reddy et al (1981) published food Idli.
an excellent
Several researchers
during the idli fermentation
(18.6% - Rao
(1967); 60.0% - Padhye and Salunkhe Vanaja
(1967), Ramakrishnam
review on the Indian fermented
have reported an increase
(1977)
(1961);
(1978)).
in methionine
10.6% - Steinkraus,
Rao (1961), Rajalakshmi
and Padhye and Salunkhe
(1978)
et al and
FOODS, FEEDS AND BEVERAGES reported an improvement
in nutritional
occur with an improved methionine al
(1967) reported a decrease
protein following
fermentation
value of the protein
content.
in Protein
and Khandawala,
essential
(PER) of the
et al (1962) and van Veen, et
of the idli was the same as that
mixture of ingredients.
that the idli fermentation
that would
On the other hand, van Veen et Efficiency Ratio
al (1967) reported that the digestibility of the unfermented
35
If it can be substantiated
utilizing Leuconostoc mesenteroides
organism can synthesize methionine
this will be of great nutritional
in legume/cereal
significance
are the first limiting amino acids in legumes. which can be easily accomplished
as the mixtures,
since methionine/cystine An idli-type fermentation
even under rather primitive
conditions
would be a low cost method of improving the protein quality. Dawadawa
(Daddawa)
Dawadawa
is an African fermented food that has been known for centuries
Nigeria and plays an important nutritional It is beginning Dawadawa
to get more attention
of the African
in the villages.
from researchers.
is a food produced by a natural,
cotyledons
role especially
uninoculated
fermentation
locust bean (Parkia filicoidea)
The brown-to-black
1980; and Ikenebomeh,
of the
a tree legume
found not only in Africa but in Southeast Asia and tropical (Eka, 1980; Campbell-Platt,
in
South America
1982).
coated seeds are removed from their pods, washed,
soaked
and boiled with added potash for up to 24 hours until swollen and softened. The hulls are then removed by pounding gently or rubbing between and the cotyledons The cotyledons
are then reboiled for about 30 minutes.
are drained and placed in a basket,
a hole in the ground lined with leaves. with leaves or plastic at ambient particularly
(25 to 35°C) temperature. bacilli,
develop
The cotyledons
calabash pot or
are then covered
the fermentation
types of bacteria,
in the fermenting beans producing viscous
resembles Japanese natto.
and auunoniacal.
The initial
In this
The beans change from
sweet beany odor becomes strongly
The bean mass is then exposed to the sun,
partially dries and darkens further. formed into round balls
Different
material which link the beans together,
light to dark brown in color. proteolytic
sacking,
sheeting and allowed to ferment for 48 to 72 hours
strands of mucilaginous respect,
the hands
The partially dried beans may then be
(5 cm in diameter)
or flattened
cakes depending upon
36
K.H. STEINKRAUS
the locality and then are further dried in the sun following which the dawadawa remains stable for at least a year
(Campbell-Platt,
1980).
Dawadawa is used in much the same ways bouillon or Maggi cubes are used in the Western world as a nutritious grains in soups and stews. in Northern Nigeria.
Dawadawa contains about 40% protein and 35% fat
making it a concentrated of protein
flavoring additive along with cereal
Consumption ranges from 1 to 7 grams/day/person
source of nutrients and the second cheapest source
(after groundnut)
in Nigeria.
Eka (1980) reported that thiamine
increased from 0.65 mg/iO0 grams in the unfermented beans to 1.35 mg/IO0 grams and riboflavin increased from 0.45 mg/iOO grams to 1.30 mg/IOO grams in the fermented dawadawa. Platt
(1964) and Leung, Busson and Jardin
increase in riboflavin,
(1968) reported a threefold
a sixfold increase in thiamine and a decrease of a
third in niacin during fermentation. The essential microorganisms
in the dawadawa have not been identified.
There is insufficient knowledge of the biochemical and nutritional changes that occur during the fermentation.
It appears that bacilli play an
important role but there are numerous bacteria present and it would be interesting to know if there is a sequence of microorganisms and why the substrate does not spoil or become toxic rather than yield a highly acceptable fermented food. Soy Sauce Soy sauces continue to be manufactured by small-scale traditional processes as well as by modern large scale factories such as the one built by Kikkoman Co. in Walworth, Wisconsin. Bhumiratana et al (1980)
studied five different
soy sauce strains of
Aspergillus and one of Mucor for proteolytic activity.
A strain of
Aspergillus flavus var. columnaris with superior protease production showed no detectable aflatoxin production on glutinous rice or soybean and yielded a soy sauce of superior quality in a traditional
soy sauce factory.
Impoolsup et al (1981) found that A. flavus var. columnaris produced two major proteases,
an alkaline and a neutral protease, both of which appeared
in the late phase of fungal growth.
These results lead to a recommendation
FOODS, FEEDS AND BEVERAGES
37
that koji, beans covered with mold growth, be transferred in two days rather than the traditional
4 to 7 days.
production
facilities
production
and overall quality of the soy sauce.
another modification
by more than twice thus improving both efficiency
of
This group is also trying
of the process in which the two day-old koji is
incubated at 50 to 55°C for I or 2 hours to maximize submersion
to the salt brine
This expands koji
in the salt brine where the proteolytic
proteolysis
prior to
activity is inhibited
85
to 90%. Flegel et al (1982) emphasized
that soy sauce manufacturers
prefer a "green" koji indicative koji indicative
of Rhizopus,
of As~ergillus
Mucor etc.
in Thailand
oryzae rather than "black"
Green kojis are generally more
common in cool weather and the black kojis occur more frequently weather. sauces.
They referred to white crystalline materials The crystals proved to be pure tyrosine.
in hot
found in some soy
They also referred
to an
improved method of producing dry spore inoculum on rice starch in plastic bags. Indonesian Tape Indonesian Tape, Malaysian Tapai, Thai Kaomag are sweet/sour products highly appreciated reviewed by Steinkraus organisms
present
Predominant
mold-like
were isolated.
Towprayoon
Takada et al (1981)
Torulopsis.
rice
and Kootin
(1982)
studied the
a mold bran inoculum for making Thai kaomag.
yeasts.
yeast-like molds, and
Molds belonging
rouxii, Endomyqopsis
studied the microflora
an inoculum available
Mucor, Rhizopus
alcoholic
Production has been
to Mucor and Rhizo~us
also
Kaomag with superior flavor was produced using a mixed
inoculum of Amylomyces
contained
(1983e).
in loogpang,
in Asia.
organisms found were Amylomyces,
E ndomycopsis,
Loog pang,
as a dessert
and Aspergillus
Lactobacilli
fibuliger and Hansenula
anomala
in various Thai fermented
foods.
on the market,
contained molds of genera
plus yeasts of genera Candida and
were predominant
some Candida and Torulopsis
in koe mug (kaomag) but it also
yeasts.
Pediococci
dominated
the
thua nao fermentations. Fish Sauces Tongthai
and Okada
(1981) divided
tion into three stages:
the nampla
(numpla)
fish sauce fermenta-
early, during which soluble nitrogen
acids increase very rapidly due to exopeptodase
originating
and free amino in the fish
38
K.H. STE INKRAUS
tissue itself;
middle (5th to 20th weeks), when endopeptodases are
predominant; and the late stage (20th to 50th weeks), during which time halophiles become active. Japanese Ko$i Kojis, crude enzyme sources for the production of soy sauce,miso, sake etc. are generally prepared by incubation in open systems where it is possible for contaminating organisms to invade the developing koji.
Takano et al
(1982) studied the use of selected lactobacilli inoculated along with Aspergillus oryzae to inhibit growth of contaminants such as Bacillus subtilis and Micrococcus luteus.
They found that Pediococcus cerevisiae in
populations of 105 to 106 cells/gram dry koji inhibited the growth of 104 cells of Bacillus subtilis inoculated as a contaminant. Nigerian Millet Beer ("Oyokpo") Nkanga and Uraih (1981) improved the quality of native millet beer - Oyokpo by better control of germination (malting)and use of a pure culture of Saccharomyces cerevisiae. Kenyan uji Mbugua (1981) reported that coliforms were active early in the fermentation of the East African acid cereal porridge--Uji.
The major lactic species
isolated from fermenting Uji was Lactobaeillus plantarum.
Inoculation with
Leuconostoc mesenteroides inhibited development of coliforms and resulted in an improved flavor and aroma in the product. MICROBIAL/SINGLE CELL PROTEIN (SCP) In 1980, BioScience, the publication of the American Institute of Biological Sciences devoted a special issue to "Food from Microbes".
The
viewpoint presented was that microbes especially in the form of indigenous fermented foods will likely play an important role in feeding animals and humanity in the future (Steinkraus, 1980).
The consumption of microbes
directly as food by man (except for mushrooms) requires considerably more research, development and study (Waslien and Steinkraus, 1980). Litchfield
(1980) reviewed the status of microbial protein production
including algae, bacteria and fungi.
Algal production is limited by the
amount of available sunlight, the carbon dioxide content of the water,
FOODS, FEEDS AND BEVERAGES suitable pH of the water,
suitable
concentrations
39 of nitrogen,
and minerals.
Ponds must be agitated by mechanical
recirculation.
Yields are relatively
phosphorus
agitation or
low 1 to 2 grams/liter
and harvesting
is difficult. Imperial Chemical the largest methanol.
Industries,
installations
Ltd.
(ICI) in England have developed
growing bacteria
Methylophilus
protein and is used in animal feeds. Minnesota,
(Candida utilis) on an ethanol
substrates
cheese-whey,
processing waste,
process
methane,
bagasse,
carob bean extract,
cornstarch
in which Paecilomyces
Crude protein content
associates
(1979) developed
cellulolyticum
SO 2 is stripped
is 0.55 g/gram reducing
Total production
Air
from
sugar.
is 15 to 16.5 tons of Moo-Young
and
a pilot plant process growing Chaeotomium corns over cellulosic
Protein content of the product
(1980) suggested
aerobically
cellulosic waste and
is used for animal feeds.
on solid-substrate
and sawdust.
coffee-
vaiota is grown on spent sulfite liquor.
is 52-57%.
The product
waste,
of
potato
is the Finnish "Pekilo"
sterile to two fermentors.
Yield of microorganism
dry mycelium/day.
production
purified n-alkanes,
corn wet-milling
The largest fungal process at present
the substrate.
Meyer
ethanol,
sulfite waste liquor,
and ammonia are supplied
wastes
70-72%
substrate.
being used in pilot plant and commercial
SCP include methanol,
sawdust.
Pruteen contains
Amoco Foods co., Hutchinson,
a subsidiary of Standard Oil Co. of Indiana is producing human
food grade yeast
waste,
on
The factory can produce 70,000 tons of "Pruteen" per year or
nearly 192 tons per day in a continuous process.
Present
one of
methylotrophus
that "Carboxydobacteria",
and other farm
is about 45%.
bacteria able to grow
on CO as their sole source of carbon and energy be used to
reduce the environmental
levels of carbon monoxide
and also yield microbial
protein for feeding animals and man. Rank, Hovis and MacDougall
developed
edible mold is grown on low-cost combined with meat flavorings for human consumption
(Spicer,
a fermentation
carbohydrates,
process
and fats to produce a quality meat substitute 1971a,
1971b).
Recently the product has
been accepted by the British Food and Drug Administration consumption
in which an
recovered by filtration,
and it can be anticipated
that production
the RHM meat analogues will be expanded
as safe for human
and consumption
in the coming years.
of
40
K.H. STEINKRAUS
Takahashi
(1982)
reviewed the present status of SCP and showed how
efficiency of SCP production using normal alkanes as substrate could be greatly inproved by operating the fermentor under approximately 4 atmospheres pressure. Hesseltine and Wang
(1980) and Steinkraus
(1980) support the idea that
consumption of microbial protein in the form of traditional fermented foods remains one of the best ways of improving the human diet. Mushrooms The most direct and the most acceptable form of microbial protein available today in both the developed and developing world is mushroom which can be cultivated on lignocellulosic
and other agricultural and food wastes.
Mushrooms are being extensively produced and consumed in Asia today and most people in the world rich and poor alike find them a very acceptable food. (1980).
The subject of mushrooms
as human food has been reviewed by Chang
Fresh mushrooms of the Agaricus, Volvariella and Pleurotus types
contain generally more than 3% protein, essential versus 99 for milk, nutritional
amino acid indices of 98
amino acid scores of 89 versus 91 for milk and
indices of 28 versus 25 for milk and 31 for soybeans.
One kilogram of dry composting material will yield as much as 1 kilogram of fresh mushrooms
in 3 or 4 flushes over a period of 30 to 45 days.
yield is 600-750 grams of fresh mushrooms/kg dry compost.
there are an estimated 2325 million tons of straw produced per year 1977) over half of which may be burned, to produce approximately efficiency)
(FAO,
straw could be used as a substrate
1511 million tons of fresh mushrooms
(65%
or 336 kg of fresh mushrooms annually for each of the present
4.5 billion human inhabitants of the earth about 28 g of protein per person/day). lignocellulosic and other wastes
(920 g fresh mushrooms containing
Microbial protein production on
should be exploited to the fullest as an
adjunct to the world's supply of food and protein. mushrooms,
Usual
Considering that
Following growth of the
the spent beds can be used as a protein-enriched
supplement for
cattle and other animals, used as a nitrogen enriched soil conditioner or used as sources of cellulases and lignases for the hydrolysis of other lignocellulosic
substrates for the production of fermentation products.
FOODS, FEEDS AND BEVERAGES
41
REFERENCES i.
S.H. Abiose, M.C. Allan and B.J.B. Wood, Microbiology and biochemistry of miso (soy paste)fermentation,
in Adv. in Applied Micro., 28, 239-
265 (1982). 2.
J.M. Appleton, V.F. McGowan and V.B.D. Skerman, Microorganisms and ~lan, UNESCO/UNEP Publication under Contract No. 258117, World Data Center, Brisbane
3.
(1979).
L.R. Batra, Fermented cereals and grain legumes of India and vicinity, in Advances in Biotechnology, M.Moo-Young et al (Eds.), Pergamon Press, II, 547-553 (1981).
4.
A. Bhumiratana, T.W. Flegel, T. Glinsukon and We Somporan, Isolation and analysis of molds from soy sauce koji in Thailand, Appl~ and Environ. Micro., 39, 430-435 (1980).
5.
Board on Science and Technology for International Development
(BOSTID),
Chemistry and World Food Supplies, Report of a Workshop following CHEMRA~q II, National Academy Press (1983). 6.
G. Campbell-Platt, African locust bean (Parkia species) and its West African fermented food product, dawada, Ecology of Food and Nutrition, ~, 123-132.
7.
S.T. Chang, Mushrooms as human food, BioScience, 30, 399-401 (1980)~
8.
J.S. Chiao, Modernization of traditional Chinese fermented foods and beverages,
in Advances in Biotechnology, M.Moo-Young et al (Eds.),
Pergamon Press, I I, 511-516 (1981). 9.
O.U. Eka, Effect of fermentation on the nutrient status of locust beans. Food Chem., ~, 303-308 (1980).
i0.
D. Farr, Traditional fermented foods: a great potential for the future, Nestle Research News 1980/81, pp. 31-37 (1982).
II.
T.W. Flegel, A. Bhumiratana, A. Impoolsup, N. Takada, Y. Oshima and H. Okada, Studies on Aspergillus flavus vat. columnaris in soy sauce koji, in Microbial Utilization of Renewable Resources, Vol. 2, H. Taguchi
(Ed.), ICME, Faculty of Engineering, Osaka University, Osaka,
Japan, pp. 59-63 (1982). 12.
Food and Agricultural Organization of the United Nations
(FAO), 1977
FAO production yearbook, FAO, Rome, Italy (1978). 13.
I. Gandjar, Soybean fermentation in Indonesia, in Advances in Biotechnology, M.Moo-Young et al (Eds.), Pergamon Press, II, 531-534. (1981).
K.H. STEINKRAUS
42
14.
C.W. Hesseltine and H.L. Wang, The importance of traditional fermented
15.
J. Hua, I.H. Wang, S.K. Chen and W.H. Hsu, Fermented sauce made from
foods, BioScience, 30, 402-404 (1980).
black soybean,
(Inyu), Advances in Biotechnology, M.Moo-Young
Pergamon Press, II, 517-523 16.
(Ed),
(1981).
M.J. Ikenebomeh, The Solid Substrate Fermentation of African Locust Beans (Parkia filicoidea Welw.), P h . D .
Thesis, McGill University
(1982). 17.
A. Impoolsup, A. Bhumiratana and T.W. Flegel, Isolation of alkaline and neutral proteases from Aspergillus flavus var. columnaris, a soy sauce koji mold, Appl. and Environ. Micro., 42, 619-628 (1981).
18.
P.K. Khandwala, S.D. Ambegaokar,
S.M. Patel, M.V. Radhakrishna Rao,
studies in fermented foods, I. Nutritive value of idli, J. Sci. Ind. Res. 19
(india), 21C, 275-278.
S.D. Ko, fermented foods of Indonesia except those based on soybeans, in Advances in Biotechnology, M.Moo-Young et al. (Eds), Pergamon Press, I I, 525-530 (1981).
20.
S.D. Ko, Indigenous fermented foods, in Fermented Foods, Economic Microbiology, Vol. 7, A.H. Rose (Ed.), Academic Press, pp. 15-38 (1982).
21.
W.T.W. Leung, F. Busson and C. Jardin, Food Composition Tables for Use in Africa, U.S. Dept. of Health/Food and Agricultural Organization of United Nations (FAO), Bethesda, Maryland
22.
(1968).
J.H. Litchfield, Microbial protein production, BioScience, 30, 387396 (1980).
23.
S.K. Mbugua, Microbiological and Biochemical Aspects of Uji (an East African Sour Cereal Porridge) Fermentation, and Its Enhancement Through Application of Lactic Acid Bacteria, Ph.D. Thesis, Cornell University
(1981).
24.
O. Meyer, Using carbon monoxide to produce single-cell protein,
25.
M, Moo-Young, A.J. Daugulis, D.S. Chahal and D.G. MacDonald, The
BioScience, 30, 405-407 (1980).
Waterloo process for SCP production from waste biomass, Process Biochem., 14(10), 38-40 (1979). 26.
M. Moo-Young
(General Editor), Advances in Biotechnology, Vol. II,
Fuels, Chemicals, Foods and Waste Treatment, Pergamon Press (1981). 27.
M. Moo-Young, A.R. Moreira and R.P. Te~gerdy, Principles of solidsubstrate Fermentation,
in The Filamentous Fungi, Vol. IV, Fungal
FOODS, FEEDS AND BEVERAGES
43
Technology, J.E. Smith, D.R. Berry and B. Kristiansen (Eds.), Edward Arnold, pp. 117-144 (1983). 28. H.G. Muller, Fermented cereal products of tropical Africa, Advances in Biotechnology, M.Moo-Young et al, Pergamon Press, II, 541-546 (1981). 29. National Academy of Sciences (NAS), Microbial Processes: Promising Technologies for Developing Countries, National Academy of Sciences (1979). 30. Nestle Products Technical Assistance Company Ltd., Nestle Research News 1980/81 (1982). 31. E.I. Nkanga and N. Uraih, Improved brewing of millet beer-(OYOKPO) and production of single cell proteins from the spent grains, Acta Biotechnologica, (DDR), ~, 153-159 (1981). 32. Y. Nunokawa, Enzymes affecting the fermentation of sake moromi-mash, in Advances in Biotechnology, M.Moo-Young et al. (Eds.), Pergamon Press, II, 563-568 (1981). 33. V.W. Padhye and D.K. Salunkhe, Biochemical studies on black gram (Phaseolus mumgo L.), III. Fermentation of black gram and rice blend and its influence on the in vitro digestibility of the proteins, J. Food Biochem., ~, 327-347. 34. C.S. Pederson, Microbiology of Food Fermentations, 2nd Edition, AVI Press (1979). 35. B.S. Platt, Biological ennoblement: improvement of the nutritive value of foods and dietary regimens by biological agencies.
Food Tech., 18,
68-76 (1964). 36. R. Rajalakshmi and K. Vanaja, Chemical and biological evaluation of the effects of fermentation on the nutritive value of foods prepared from rice and grams, Brit. J. Nutr., 21, 467-473. 37. C.V. Ramakrishnan, Study of Indian fermented foods from legumes and production of similar fermented foods from soybeans, Fourth Annual Research Report, pp.l-77, M.S. University of Baroda, Baroda, India (1977) 38. C.V. Ramakrishnan, Studies on Indian fermented foods, Baroda J. Nutrition, 6, 1-54 (1979). 39. N.R. Reddy, S.K. Sathe, M.D. Pierson and D.K. Salunkhe, An Indian fermented food: a review, J. Food Quality, 5, 89-101 (1981). 40. P. Saisithi, Roles of fermented foods in solving nutritional problems, in H. Taguchi (Ed.), Microbial Utilization of Renewable Resources.
44
K.H. STEINKRAUS Vol.2 ICME, University of Osaka, Osaka, Japan, pp. 200-210 (1982).
41. W. Shurtleff and A. Aoyagi, The Book of Tempeh, Harper and Row (1979). 42. W. Shurtleff and A. Aoyagi, Tempeh Production, New-Age Foods Study Center
(1980a).
43. W. Shurtleff and A. Aoyagi, Miso Production, New-Age Foods Study Center
(1980b). 44. A. Spicer, Synthetic proteins for human and animal consumption, Vet. Record, 89, 482-487 (1971a). 45. A. Spieer, Protein production by microfungi, Trop. Sci., XIII, 239-250 (1971b). 46. K.H. Steinkraus, A.G. Van Veen and D.B. Thiebeau, Studies on Idli--An Indian fermented black gram-rice food, Food Technol., 21, 110-113 (1967). 47, K.H. Steinkraus, Nutritionally significant indigenous fermented foods involving an alcoholic fermentation, in Fermented Food Beverages in Nutrition, C.F. Gastineau, W.J. Darby and T.B. Turner (Eds.), Academic Press, pp. 35-59 (1979). 48. K.H. Steinkraus, Introduction: food from microbes, BioScience, 30, 384-386 (1980). 49. K.H. Steinkraus, Industrialization of home and village food fermentations, in Advances in Biotechnology, M.Moo-Young et al. (Eds.), Pergamon Press, II, 473-478 (1981). 50. K,H. Steinkraus, Fermented foods and beverages: the role of mixed cultures, in Microbial Interactions and Communities, Vol. i, A.T. Bull and J.H. Slater (Eds.), Academic Press, pp. 407-442 (1982a). 51. K.H. Steinkraus, Progress in preservation of food through fermentation, Presented at CHEMRAWN II, Manila, Philippines (1982b). 52. K.H. Steinkraus, The indigenous fermented foods, Nestle Research News. 1980/81, pp, 23-28 (1982c). 53. K.H. Steinkraus, Traditional food fermentation as industrial resources, in Traditional Food Fermentation as Industrial Resources, S. Saono, F.G. Winarno and D. Karjadi (Eds.), Indonesian Institute of Sciences (LIPI), Jakarta, Indonesia, pp. 3-16 (1982d). 54. K.H. Steinkraus, Solid-state (solid-substrate) food/beverage fermentation involving fungi, Acta Biotechnologica (DDR), In Press (1983a). 55. K.N. Steinkraus, Traditional food fermentations as industrial resources Acta Biotechnologica (DDR), ~, 1-12 (1983b).
FOODS, FEEDS AND BEVERAGES 56.
45
K.H. Steinkraus, Lactic acid fermentation in the production of foods from vegetables, cereals and legumes, Antonie van Leeuwenhoek, In Press (1983c).
57.
K.H. Steinkraus, Industrial applications of Oriental fungal fermentations, in The Filamentous Fungi, Vol. IV, J.E. Smith, D.R. Berry and B. Kristiansen (Eds.) Edward Arnold, pp. 171-189 (1983d).
58.
K.H. Steinkraus, Handbook of Indigenous Fermented Foods, Marcel Dekker
59.
H. Taguchi, Annual Reports of International Center of Cooperative
Inc. (1983e).
Research and Development in Mirobial Engineering (ICME), Faculty of Engineering, Osaka University, Osaka, Japan (1978), (1979), (1980), (1981), (1982). 60.
N.Takada,T. Iwashiro, J. Yagyu, A. Bhumiratana, T. Flegel and Y. Oshima, Microflora in Various Thai fermented foods, in Microbial Utilization of Renewable Resources, Vol. I, H. Taguchi (Ed.), ICME, Faculty of Engineering, Osaka University, Osaka, Japan, pp. 85-91 (1981).
61.
J. Takahashi, Present status of single cell protein-with some aspects of gaseous alkanes as novel substrates, in Microbial Utilization of Renewable Resources, Vol. 2, H. Taguchi (Ed.) ICME, Faculty of Engineering, Osaka University, Osaka, Japan, pp. 40-46 (1982).
62.
M. Takano, B.K. Datta and I. Shibasaki, Lactic acid bacteria as a safe additive for koji process, in Microbial Utilization of Renewable Resources, Vol. 2, H. Taguchi (Ed.), ICME, Faculty of Engineering, Osaka University, Osaka, Japan, pp. 24-32 (1982).
63
C. Tongthai and H. Okada, Change of nitrogenous compounds during numpla fermentation, in Microbial Utilization of Renewable Resources, Vol. I, H. Taguchi (Ed.), ICME, Faculty of Engineering, Osaka University, Osaka, Japan, pp. 101-107 (1981).
64.
S. Towprayoon and S. Kootin, Fermentation of sweetened rice by pure culture, in Microbial Utilization of Renewable Resources, Vol. 2, H. Taguchi (Ed.), ICME, Faculty of Engineering, Osaka University, Osaka, Japan, pp.20-23 (1982).
65. M. Ulloa-Sopsa and T. Herrer, Fermented corn products of Mexico. Advances in Biotechnology, M.Moo-Young et al.
(Eds.), Pergamon Press,
II, 535-540 (1981). 66. A.G. Van Veen, L.R. Hackler, K.H. Steinkraus and S.K. Mukherjee, Nutritive quality of idli, a fermented food of India, J. Food Sci., 32, 339" 341 (1967).
46
K.H. STEINKRAUS
67. H.L. Wang and C.W. Hesseltine, Mold-modified foods, in Microhial Technology, Vol. II, A.H, Rose (Ed~), Academic Press, pp. 95-129 (1979). 68. C.I. Waslien and K.H~ Steinkraus, The potential of microbial cells as protein for man. BioScience, 30, 397-398. 69. B.J.B. Wood, Introduction of new fermented foods into western culture, in Advances in Biotechnology, M.Moo-Young et al. (Edso), Pergamon Press, II, 467-472
(1981).
70. B.J.B. Wood, Soy sauce and miso, in Fermented Foods, Vol. 7, Economic Microbiology, A.H. Rose (Ed,), Academic Press, pp. 39-86 (1982).