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Review Article
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Termite Digestomes as a Potential Source of Symbiotic Microbiota for Lignocelluloses Degradation: A Review |
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L.J. Wong,
P.S. H`ng,
S.Y. Wong,
S.H. Lee,
W.C. Lum,
E.W. Chai,
W.Z. Wong
and
K.L. Chin
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ABSTRACT
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Termites thrive in great abundance in terrestrial ecosystems
and the symbiotic gut microbiota play important roles in digestion of lignocelluloses
and nitrogen metabolism. Termites are excellent models of biocatalysts as they
inhabit dense microbes in their guts that produce digestive enzymes to decompose
lignocelluloses and convert it to end products such as sugars, hydrogen, and
acetate. Different of digestive system between lower and higher termites which
lower termites dependent on their dual decomposing system, consisting of termites
own cellulases and guts protists.
Higher termites decompose cellulose using their own enzymes, because of the
absence of symbiotic priotists. Termite gut prokaryotes efficiently support
lignocelluloses degradation. In this review, a brief overview of recent experimental
works, development and commercialization is discussed. Significant progress
has been made to isolate cellulolytic strains from termites and optimise the
digestion efficiency of cellulose. Future perspective should emphasize the isolation
of cellulolytic strains from termites, genetically modifying or immobilization
of the microbes which produce the desired enzyme and thus benefits on the microbiology
and biotechnology.
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Received: July 15, 2013;
Accepted: January 18, 2014;
Published: March 29, 2014
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INTRODUCTION
Termites are one of the most successful wood-degraders on Earth, tunnelling
and chewing on wood for millions of years (Radek, 1999).
These insects made their first imprint as early as the Cretaceous period with
the unearthing of oldest termite fossils of approximately 100 million years
old. Termites are representing one of the social insects. They are grouped in
ancient insect order Isoptera and they are closely related to cockroach and
mantises (Radek, 1999; Kricher,
2011). Throughout the world, termites are traceable along the equators,
in the tropical forests and Mediterranean shrublands, where dense biomass and
the greatest biodiversity take place (Abensperg-Traun and
Milewski, 1995). As mankind are fearful for their structures and crops damaging
capabilities, the nature graciously welcomes these wood-grazers. Termites also
account for severe damage to wood in use. In order to enhance the resistance
ability of wood towards termites invasion, application of termite repellent
and post heat treatment on wood are now widely used (Hng
et al., 2012). Nevertheless, ecologically speaking, termites are
beneficial insects that play an essential role in recycling nutrients, forming
habitats, aerating and improving soils, and as food for countless predators
(Radek, 1999; Kricher, 2011).
Termites survive on any wood and lignocellulose materials (Hng
and Chin, 2008; Lee et al., 2013). They
coverts the cellulose of wood and lignocellulosic materials into carbohydrates
before translated into energy. Cellulose is part of plant structures and the
basic structural components of cell wall. Cellulose is a polysaccharide, a tough
linear chain of glucose joined by β-1,4-glycosidic and hydrogen bonds.
To disintegrate this polysaccharide into simple glucose, termites are loaded
with as much as 250 different species of microorganisms in their relatively
tiny guts (Nadin, 2007). Nonetheless, not all the microorganisms
in the gut of termites function in cellulosic degradation. Each of the microorganisms
is responsible in breaking down specific components of the plant structures
to different end products. The termites provide the needed settlement for the
microbes and feed on wood, while the microbes digest the food for their hosts
in return. Such exchange reflects a mutual symbiotic relationship that benefits
both the host and symbiont.
The microbial organisms inside the termites gut, however, do not develop
by themselves. Before termites could start munching on wood, they need to engage
in trophallaxis (Wilson, 1971; Machida et al., 2001).
In other words, they are exchange food and digestive fluid through mouth-to-mouth
(stomodeal) or feeding on each other's faeces (proctodeal) (Quarcoo,
2009). Such fluid contains the essential nutrients and endosymbionts that
are passed on to the younger instars by the mature termites (James,
2008). Termites are lost most of their symbionts at every molt, and termites
have to feed themselves with the recycled symbionts via proctodeal trophallaxis
(James, 2008). They rely on symbiotic bacteria embedded
on their surfaces to produce some of the digestive enzymes to degrade cellulose
for their termite host (Radek, 1999). The resulting
glucose and acetate are then absorbed by the termites as a primary source of
energy (Radek, 1999; Ohkuma, 2003)
Termites successful survival on cellulose-rich diet suggests that significant
decomposition of wood components is taking place in the gut. Almost 90% of the
cellulose in wood is turned into acetate (Nadin, 2007).
Many scientists are now convinced that termites gut resembles an efficient
living bioreactor. Different species of the microbes in termite gut have different
needs and release different end-products but they share a common goal-to degrade
lignocelluloses into different applicable products. By turning the energy-rich
cellulose into acetate and glucose, the symbiotic microbial community in termites
gut could be the key to generate customised enzymatic-cocktails to apply in
the biomass processing industry. Termites are therefore a potentially powerful
catalyst for feasible bioethanol production.
DISTRIBUTION OF TERMITES
According to the theoretical and empirical data from Models of Population Dynamics
and Models of Population Oscillations, the maximum of termite population would
be gotten during 2020s years and world population may be until 107-108
billion (Sapunov, 2008). In the high population of termites, there are 2,650
species of termites, and the majority of them occur only within tropical and
sub-tropical latitudes (Kricher, 2011). Termites are
playing significant roles in food webs and influence the provision of ecosystem
such as decomposition. They occur in vast numbers in tropical regions, which
exceed 100 g m-2 and 10,000 individuals m-2 in the tropical
forests (Eggleton et al., 1996). But their area
prolongs to increase included Italy, New Zealand, and Australia.
In addition, the distribution of Drywood termites, Subterranean termites, Formosan
termites, and Dampwood termites is varying by region. Drywood termites are live
in the countries that do not reach freezing temperatures during winter and they
are found along East Coast from the Mid-Atlantic States to South Florida, along
the Gulf Coast, through the Southwest into California, and in Hawaii. The Subterranean
termites which live in the soil underground; are able to survive in wide range
of temperatures. In US, the subterranean termites are found in every state,
except Alaska. As a pest of forest tree, Dampwood termites are rarely damage
wood in buildings. They do not nest in the soil but mainly nest in decaying
stumps, logs and eucalypt trees.
In Malaysia alone, it is estimated there could be 180 species of termites representing
48 genera that live in different habitats in the country (Tho, 1992). A termite
can correspond to up biomass of invertebrates in decomposing trunks (Bandeira
and Torres, 1985). At least ten identified species are known to invade wooden
structures, paper products, cotton clothings or ornamental trees. Coptotermes
gestroi (Asian subterranean termite) is the most common and aggressive wood-feeding
termite species found in Malaysia and was reported to cause major damages (60-70%)
specifically to interior wooden structures, followed by C. curvignathus
contributing to about 20% of the total structural damage and attacking living
trees as well as rubber, oil palm and coconut plantations (Yeoh and Lee, 2007).
Other essentially threatening species in Malaysia include Odontotermes
sp., Schedorhinotermes sp., Macrotermes gilvus, Nasutitermes
sp., Microcerotermes crassus, Globitermes sulphurous, Macrotermes
carbonarius and Microtermes spp.
LOWER AND HIGHER TERMITES
The order Isoptera of termites is phylogenetically classified into seven families
and fifteen subfamilies (Lee and Wood, 1971). The families
are: (1) Mastotermitidae, (2) Kalotermitidae, (3) Termopsidae, (4) Hodotermitidae,
(5) Rhinotermitidae, (6) Serritermitidae, and (7) Termitidae. The Mastotermitidae,
Kalotermitidae, Termopsidae, Hodotermitidae and Rhinotermitidae families are
identified as the lower termites, whilst the Serritermitidae, and Termitidae
families are acknowledged as the higher termites.
The taxonomy of lower and higher termites is based on the termites stage
of evolution, in terms of their behaviour and anatomically. The main difference
between higher and lower termites is the gut of lower termites comprises with
protozoa, while the gut of higher termites is lack of protozoa (Varma et
al., 1994). In the digestive tracts of lower termites, degrading of cellulose
is depend on flagellates, yeasts and bacteria (Breznak and
Brune, 1994; Varma et al., 1994; Konig et
al., 2002) including by the termite's own cellulases (Tokuda et al.,
1999; Watanabe et al., 1998; Tokuda et al., 2002). The higher
termites are able to decompose cellulose by using their own enzymes (Ohkuma,
2003) through the gut passage.
Scientists discovered that diets and digestion of cellulose seems to differ
between higher and lower termites. In addition, most of the species of lower
termites are wood-feeding termite. The digestion resistance of woods causes
the termites to favour wood that has been attacked by fungi. With the presence
of fungi mycelia, the woods are richer in protein content and easier to be utilised
by termites. Lower termites, such as Coptotermes lacteus and Reticulitermes
speratus, are long known to utilise gut protozoa for cellulose digestion
in addition to synthesising its own cellulases (OBrien
et al., 1979; Kudo et al., 1998).
By digestion of lignocelluloses and extract their dietary requirements from
food resources, it create the symbiotic relationship of termites with the intestinal
flagellates and bacteria contained in a large dilatation of their hindgut, which
is the paunch.
By contrast, higher termites do not harbour flagellates and typically lack
protists hence show different feeding habits. Higher termites decompose cellulose
efficiently in the absence of hindgut flagellate protozoa (Li
et al., 2006) which are recognized sources of cellulase and hemicellulases
in lower termites (Warnecke et al., 2007). The Termitidae ingest a wide
range of materials include leaves, roots, grass, dung, and soil (humus) (Wood
and Johnson, 1986). In addition, there are two groups in Termitidae, fungus-cultivating
species and non-fungus-cultivating species. The fungus-cultivating species of
termites are able to build a large fungal garden in their nests. The garden
is constructed by assembly partially digested plant materials and further digested
by fungal mycelium (Wood and Thomas, 1989). Hence, the termite workers eat the
fungus comb which contained nutrition. In addition to the direct nutritional
value, the ingested fungi may deliver missing enzyme essential for
the completion of cellulose digestion (Martin, 1987,
1991, 1992).
TERMITE AND ITS DEGRADATION ON LIGNOCELLULOSIC MATERIAL
Lignocellulose can serve as a biomass material for a number of industrial biorefinery
process, namely pyrolysis, hydrolysis, gasification to value-added products
such as glucose, xylose, starch, ethanol (Kim and Dale,
2004; Scharf and Tartar, 2008; Chin et al., 2010,
2011; Hng et al.,
2011; Tay et al., 2013; Chin and Hng, 2013).
The main challenge facing lignocellulosic materials utilization is the energy,
costs input involved in treatment and production processes. Therefore, researches
have expanded on the potential of the termite-based biological pretreatment
strategy for use in lignocelluloses degradation.
Termites efficiently digest lignocellulose using their endogenous and digestive
enzymes in the termite gut (Breznak and Brune, 1994;
Watanabe et al., 1998; Ohkuma 2003; Scharf and
Tartar, 2008; Tartar et al., 2009). The symbiotic digestion of polysaccharides
by termites is involving a complex of host and its gut microbiota, which comprises
bacteria, fungi, protozoa to degrade cellulose and hemicelluloses (Radek, 1999;
Brune, 2009). The microbial community in the gut of termites
has been attracting many scientists due to their symbiotic digestion mechanisms
in the hindgut are largely controlled by the symbionts (Brune,
2009). According to previous reports suggested that termites could efficiently
decompose lignocelluloses within a day by degrading 74-99% of the cellulose,
65-87% of the hemicellulose as well as 5-83% of the lignin which are able to
removes most neutral polysaccharides and more than half of the acidic sugars
(Breznak and Brune, 1994; Konig et
al., 2006; Sun, 2008). Nevertheless, cows decompose only 30-40% of polysaccharides
in their forage (Brune and Ohkuma, 2011).
Sound wood is most difficult to digest because the polysaccharides of the secondary
plant cell wall are embedded in an amorphous resin of phenolic polymers which
causing the barrier to enzymatic attack of the polysaccharides (Brune,
2009). Therefore, an efficient of symbiont-derived digestive enzyme in cellulolytic
system is required to the polysaccharides degradation (Scharf and Boucias, 2010).
Therefore, the incredible metabolic capability of the termite gut is potential
biocatalyst in aerobic fermentative degradation of carbohydrates, and in metabolism
of lignin-derived aromatic compounds (Brune, 1998).
ROLE OF TERMITE GUT MICROBIOATA
Let us take a look at how is the role of termite gut microbiota in lignocelluloses
digestion and may bring potentially beneficial in industrials application. For
instance, the lignocelluloses digestion is highly achieved in the termite gut
as the termites digestome is apparent as a pool of host and symbiont genes
(Scharf and Tartar, 2008; Tartar et al., 2009).
The cellulose activity in the hindgut of termites is attributed to cellulose-degradation
bacteria. (Schwarz, 2001). Termite gut contains a lot of microbes which can
digest cellulose such as the Gram-positive bacteria:
Bacillus, Paenibaccillus, Streptomyces, Actinobacteria group and Gram-negative bacteria: Pseudomonas, Acinetobacter; Facultative microbe: Serratia marcescens, Enterobacter aerogens, citrobacter farmer. Gram-positive strains
related to Cellulomonas, Bacillus and Paenibacillus showed
highest CMC-degrading potential. Wenzel et al. (2002) argued that the
cellulolytic bacteria are taking over the role of flagellates in higher termites.
Most of the gut bacteria are necessary for the survival of their hosts even
though they are indirectly involved in cellulose degradation in termites gut
(Slaytor, 1992; Radek, 1999). In a termites gut,
cellulose is broken down into simple sugar by certain cellulolytic species,
subsequently metabolised to form pyruvate. Other microbial species collaborate
in turn to transform the pyruvate to different end-products, such as CO2,
acetate, methane or ethanol, depending on availability of oxygen supply (Nadin,
2007). While concentrations in the midgut are aerobic, oxygen concentrations
are low in the hindgut (Radek, 1999). Eventually the transformation cycle repeats
again on another type of substrates. As much as 250 microbial species are adapted
to live in a termites gut together, but each is individually involved
in different transformation of varying substrates.
Termites are mostly feed on the dead grass, wood, and other plant material
to obtain essential energy from the digestion of cellulose (Andersen
and Jacklyn, 1993; Pearce, 1997). Therefore, it is
an opportunity of termite biomass used as food sources for the aquaculture,
pig, and poultry industries. At present, termite microbes have been proven useful
in poultry feed additive. Purwadaria et al. (2003)
detected cellulolytic activities in the fresh extract of termites (Glyptotermes
montanus) that increases the digestion of poultry feedstuffs containing
high lignocelluloses such as rice bran, wheat pollard, Palm Oil Mill Effluent
(POME), Palm Kernel Cake (PKC), corn and soybean meals. Rich of protein in termite
gut replace 50% fishmeal in formulations and it is a useful supplement for family
poultry. Nutrients left behind in termite wastes may also be useful for horticultural
purposes, particularly compost which potential be a novel resource for organic
biofertilizers (Chai et al., 2013; Peng
et al., 2013).
Current studies showed that termite symbionts have involved as cellulolytic
or lignin-derived component and degradation of aromatic hydrocarbons compounds.
Hence, that would be useful for industrial application such as biomass consumption,
environmental remediation and fine-chemicals production. Advances in the conversion
technology will add value to existing biochemicals production and boost exciting
economic opportunities of bio-based applications as well as fuels, chemicals
and pharmaceuticals. Despite slower reaction time and careful control of microbial
growth conditions, biological system involving termite symbionts appears to
be more appealing (Sun and Cheng, 2002; Zheng et al., 2009) for lignocelluloses
degradation.
CURRENT RESEARCH AND FUTURE PERSPECTIVE ON TERMITES GUT MICROBIOATA
As discussed, termite lignocellulose digestion has been considered as a gut-symbiont-mediated
process. The termite gut is explored as a source of novel microorganisms and
may bring many benefits to large scale industrial applications (Tokuda et
al., 2004). In fact, the symbiotic association of termites with their diversity
intestinal macrobiotic is receiving interests from various aspects such as microbiology,
biochemistry, protozoology, insect physiology and ecology, socio-biology, evolutionary
biology, and even in atmospheric chemistry (Sanderson, 1996; Higashi
and Abe, 1997; Sugimoto et al., 2000). Hence, researches have been
further expanded on the anaerobic food web and nitrogen metabolism in the termite
gut.
In addition, in microbial gut of termite, also include nitrogen fixing bacteria
(Benemann, 1973; Breznak et
al., 1973; French et al., 1976; Potrikus
and Breznak, 1977; Prestwich and Bentley, 1981).
Nitrogen fixation by termite gut microbes has been known for years ago (Breznak,
2000) and nitrogen fixation contributes as much as 60% of N in some termite
colonies (Tayasu et al., 1994). Since the nitrogen compound are insufficient
in wood and soil, the nitrogen fixing bacteria (e.g., Enterobactor, Rhizobium,
Desulfovibrio) is play a vital role in symbiotic community (Lovelock
et al., 1985; Radek, 1999). However, the
wood-feeding termites are strongly nitrogen limited (Brune
and Ohkuma, 2011). Researchers showed that the hindgut microbiota of termites
includes a morphologically diverse population of N-fixing Spirochetes bacteria
which have reached 50% of all prokaryotes (Paster et
al.,1996; Breznak, 2002). The spirochetes are
involved in acetogenesis and N2 fixation process to provide the carbon,
nitrogen and energy needs of their termite host. The N-fixing bacteria produce
amino acids that are partly liberated and may be used by termites and flagellates.
Nonetheless, the metabolic role of Spirochetes is entirely unknown (Radek, 1999).
Hence, more researches are needed to study the metabolic properties of Spirochetes
especially the spirochetes contribution to H2/CO2-acetogenesis
and N2 fixation. Next, the study on the properties of spirochetes
(or of the termite gut itself) enables them to become such a prominent component
of the microbiota is needed in the field of researches also.
In addition, there are fermenting bacteria also found in the termite gut from
the anaerobic food web. The low concentrations of soluble sugars and the accumulation
of their metabolites in the hindgut fluid of termites indicate that polysaccharides
depolymerization is coupled to the fermentative degradation of its hydrolysis
products (Brune and Ohkuma, 2011). The fermenting bacteria
(e.g., of the genera Streptococcus, Bacteroides, Fusobacterium, and Lactobacillus),
profit by the low amount of mono-, di-, and oligosaccharides, liberated by the
flagellates (Breznak, 1984; Radek,
1999). The fermentation of cellulose is following the equation as shown
as below (Odelson and Breznak, 1985; Brune
and Ohkuma, 2011):
[C6H12O6] + 2H2O
→ 2CH3COO¯ + 2H+ + 2CO2 + 4H2
The metabolic end product of the anaerobic fermentation food web is acetate
(termites fuel), and other organic acid, which can be transported across
the gut wall for reabsorbed by the host and form the basis for its energy metabolism
(Radek, 1999; Brune and Ohkuma,
2011). According to the few researches, two species of fermenting bacteria
were identified which include Acetonema longum by Kane
and Breznak (1991) and Enterococcus sp. by Tholen et al. (1997).
In the new study, researchers have suggested the termites enzyme could
be boon to cellulosic ethanol by fermentation process. Researcher claim that
a type of bacteria that helps termite digests wood could be a key to making
ethanol economically from non-food crops such as wood and grass (REF). Meanwhile,
wood decay in the guts of termites generates hydrogen gas from lignin as a key
intermediate product. This explosive, energy-rich hydrogen gas can be combined
with ethyl acetate to make ethanol or provide energy for gasification. As a
result, research is currently applied to understanding the interactions of lignocelluloses
degradation and symbiotic microbes in termites gut to provide innovations in
technology to address this challenge for producing ethanol (Nadin,
2007; Brune, 1998; Scharf and Boucias, 2010; Li
et al., 2012). Bioethanol production with emphasis on cellulosic
ethanol brings a scientific challenge of achieving cost effective degradation
of complex cellulosic biomass (pre-treatment and hydrolysis stages) (McMillan,
1994). Thus, the microbes living in termites gut provide a fast and efficient
hydrolysis of biomass if harnessed and applied appropriately to produce cellulosic
ethanol at an industrial scale.
For increased efficiency and reduced production costs, future findings should
highlight the isolation of cellulolytic strains or microbial species from termites,
genetically modifiying or immobilization of microbes which produce the desired
enzymes. As such, termite gut digestomics is a relatively new area of research.
In the future, termite guts can potentially advance the bioconversion of lignocellulosic
materials to valuable product such as fuel as it is an effective, economic,
and sustainable ways.
CONCLUSION
Termites are regarded as harmful insects because of their ability in destroying
various materials including lignocellulosis biomass. The termites digestion
process on the cellulose is fast and efficient which typically achieving 95%
conversion in 24 h or less. However, the microbiology mechanism is different
between the two classes of termites which are lower termites and
higher termites. In which, the differences of microbiology of lower
termites and higher termites may also differ in their role in degrading cellulose.
In recent years, termites have captured the interests of researchers from various
disciplines to investigate their gut microbial symbionts and their incredible
ecological importance to the global carbon cycle. The ability of termites to
hydrolyse a broad assortment of chemical bonds and break down the lignocelluloses
into monomer sugars quickly has astonished researchers. Apparently, the development
of low-cost enzymatic approach with termites is promising and ecological to
accomplish the bioconversion of lignocelluloses into useful products such as
glucose and ethanol.
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