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SOAJ Entomological Studies
Volume 1 (2012) 1-32
Review Article

ISSN 2278-5566

DIGESTIVE PHYSIOLOGY OF SYNANTHROPIC
MITES (ACARI: ACARIDIDA)
Tomas Erbana,b and Jan Huberta,b 
a.Medical Center Prague, Prague 4, Czechia
b.Crop Research Institute, Department of Product Stored Pest Control and Food Safety, Prague 6,
Czechia.
(Received 25 November 2011, Accepted 25 December 2011; Academic Editor: Arash Zibaee)
Copyright © 2012 Tomas Erban and Jan Hubert. This is an open access article distributed under the
Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction
in any medium, provided the original work is properly cited.
Abstract
Although nutritional biology and digestive enzymes of the synanthropic acaridid mites have been studied for
many decades, full understanding of these processes remains incomplete. Twenty one species of acaridid mites
by high frequency of occurrence were used in enzymological studies, including species living in house dust or
products stored for human and animal consumption. In mites by allergen importance, the proteases, α-amylases,
chitinases have been identified as allergens and characterized on biochemical level, even if the crystal structure
has been described. However, basic informations about in vivo conditions such as lumen pH offer key
informations to study the activity of mite digestive enzymes including their inhibitors and gut microflora. The
gut contents of acaridid mites were determined to be within a pH range of 4 to 7. Mite habitats provide various
nutrients, mainly structural (keratin, collagen, elastin) and “unstructural” proteins; lipids, structural and storage
carbohydrates, sucrose and nutrients in microorganism. Reviewes on hydrolyzing enzymes indicate that mites are
well equipped to hydrolyze structural and storage carbohydrates in plant cells and microorganisms. The
symbiotic interactions between mites and microorganisms are important to explore nutrient sources and
microphagy, i.e. bacteriophagy and mycophagy, seems to be favorable or, in some environments, even essential
for synanthropic acaridid mites. Previously, the concepts of feeding habits and enzymatic activity were
suggested, however the review of activity relegated that there are no direct correlation among the enzymatic
activity and feeding habits.
Keywords: Digestion, Enzyme, Inhibitor, Allergen, Mite

CONTENTS
1. Introduction
2. Food Resources and Feeding Guilds of Mites in Human Made Habitats



. Corresponding: Tomas Erban ([email protected]), Crop Research Institute, Department of Stored Product
Pest Control and Food Safety, Laboratory of Proteomics. Tel: +420604127807.

Erban and Hubert 1 (2012) 1-32/ DIGESTIVE PHYSIOLOGY OF ACRIDIDAE

3. Gut Morphology of Synanthropic Acaridid Mites
4. Role of pH in Digestion
5. Digestive Enzymes Necessity for Utilization of Food Sources
5.1. Proteolytic Enzymes and Digestion of Proteins
5.2. Digestion of Starch, Maltose and Sucrose (Glycosidases)
5.3. Digestion of Structural Plant Polysaccharides
5.4. Digestion of Lipids
5.5. Digestion of Microorganisms
5.5.1 Bacteriolytic Enzymes
5.5.2. Digestion of Fungal Cells
5.6. Miscellaneous Proteins Participating on Digestion
6. Medical Importance of Digestive Enzymes as Allergens
7. Possible Interaction to Microroganisms for Utilization of Food Sources
8. Conclusion

1. Introduction
Nearly 300 species of mites are associated with human habitats (Montealegre et al., 2002), however
only 21 species of acaridid mites by high frequency and abundance were used in enzymological
studies. The synanthropic mites are usually divided into two artificial groups: (1) HDMs – house dust
mites [Pyroglyphidae: Dermatophagoides farinae (Hughes 1961), D. pteronyssinus (Trouessart 1897),
Euroglyphus maynei (Cooreman 1950); Echimyopodidae: Blomia tropicalis (van Bronswijk, de Cock
and Oshima 1974)] and (2) SPMs – stored product mites [Acaridae: Acarus siro (Linnaeus 1758), A.
farris (Oudemans 1905), Aleuroglyphus ovatus (Troupeau 1879), Tyrophagus putrescentiae (Schrank
1781), T. longior (Gervais 1844), T. similis (Volgin 1949), Tyroborus lini (Oudemans 1924,
Thyreophagus entomophagus (Laboulbène and Robin 1862), Rhizoglyphus robini (Claparède 1868), R.
echinopus (Fumouze and Robin 1968), Sancassania berlesei (syn. Caloglyphus redickorzevi (Michael
1903); Carpoglyphidae: Carpoglyphus lactis (Linnaeus 1758); Glycyphagidae: Lepidoglyphus
destructor (Schrank, 1781), Glycyphagus domesticus (DeGeer 1778); Chortoglyphidae: Chortoglyphus
arcuatus (Troupeau 1879); Aeroglyphidae: Aeroglyphus robustus (Banks, 1906)]. Except synanthropic
(free living) mites a precise study of digestive enzymes was done on scab mite Psoroptes ovis (Hering
1838), a member of family Psoroptidae (Hamilton et al., 2003).
It is believed that acaridid mites are derived from an ancestral fungivorous species that originally
inhabited soil and penetrated into human habitats through the nests of birds and mammals during the
neolithic revolution (OConnor, 1979, OConnor, 1982). The ancestors of acaridid mites are suggested
within the Oribatida of Malaconothroidea (Norton, 1998). Such origin means that their digestive
adaptations are similar to those of oribatid mites and the soil mites in vertebrate nest. OConnor also
concluded that the mites evolved tolerance by feeding under variable environmental conditions. Some
mites reduced independence on hypopus for survival and many species often form deuteronymphs
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(OConnor, 1979, OConnor, 1982). The stored product mites are associated with specific resources and
may be, based on OConnors´ conception regarding natural habitat preferences, grouped into four
categories (OConnor 1979, OConnor, 1982, OConnor, 1984): (i) those are associated with specific
resources, such as fruit or meat, which are not widely distributed in space or time: Carpoglyphus spp.
(Carpoglyphidae) infests rotting fruit in the field and other materials with high sugar content;
Aeroglyphus spp. (Aeroglyphidae) is associated with a variety of specialized habitats, such as bat
roosts, bird nests and nests of social insects; (ii) those are associated widespread field resources:
Tyrophagus spp. (Acaridae) is widely distributed in a variety of natural habitats and is abundant in
grassland soil and litter; Glycyphagusspp.(Glycyphagidae) occupies the widest habitat range; species
reside in grassland, tree foliage, caves, bat roosts, rodent nests, stored products and house dust; (iii)
those associated with the nests of mammals, especially rodents: Acarus and Aleuroglyphus spp.
(Acaridae) are inhabitants of

a wide variety of mammals nests, including the roosts of bats;

Lepidoglyphus spp. (Glycypgagidae) is commonly encountered in stored products; Chortoglyphus spp.
are mites associated with nests of birds; (iv) mites associated with nests of birds: Dermatophagoides
spp. (Pyroglyphidae) inhabited house dust or stored products and are clearly derived from species
inhabiting the nests of birds.
Although the nutritional biology and digestive enzymes of synanthropic acaridid mites have been
studied for many decades, full understanding of these processes remains incomplete. The proteases, αamylases, chitinases have been identified as allergens and characterized on biochemical and cDNA
level, even if the crystal structure has been described (Tovey et al., 1981, Fernandez-Caldas and Calvo,
2005, Thomas et al., 2010). In particular, nutritional studies of enzymatic activities are still lacking.
The small size of mites complicates the digestive studies and gut dissection is impossible. The pioneer
studies describe chelicerae and feeding apparatus to estimate the feeding of mites (Schuster, 1956,
Akimov, 1985, Kaneko, 1988). Other studies were focused to presence and activity of carbohydrases
hydrolyzing structural and storage saccharides, the presence of the enzyme was suggested as an
important determinant of the feeding ability of mites (Luxton 1972, Akimov and Barabanova, 1976,
Akimov and Barabanova, 1978, Bowman, 1981, Akimov, 1985, Siepel and de Ruiter-Dijkman, 1993).
The adaptations of mites in nutritional biology and digestion were important to enable them the
colonization and surviving in the human environment. The review summarizes recent knowledge
concerning synanthropic mite digestive enzymes and the digestive capability of mite gut in relation to
utilization of nutrient sources in human habitats.
2. Food Resources and Feeding Guilds of Mites in Human Made Habitats
The above mentioned food resources look diversified, however many authors tried to classify the
nutrients and food sources for mites and correlated them to the enzymatic activities. The pioneer
studies were focused on describing some feeding differences in soil oribatid mites and were based on
enzymatic analysis of the whole body homogenates suggesting that the measured enzymes are
probably digestive (Zinkler, 1971, Luxton, 1972, Luxton, 1979). The species of mites were grouped to
the feeding guilds based on presence or absence of digestive enzymes. It was expected that enzymes
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gives the mite possibility to hydrolyze appropriate nutrients. The major and minor feeding habits for
oribatid mites have been defined (Luxton, 1972): Major feeding habits: (1) macrophytophages feeding
strictly on higher plant material including xylophages (feed on woody tissue), phyllophages feeding on
leaf tissue; (2) microphytophages feeding strictly on microflora including mycophages feeding on
fungi and yeasts, bacteriophages feeding on bacteria, phycophages feeding on algae, (3)
panphytophages combining all or some of the sub-headings above and are similar to
macrophytophages and microphytophages. The casual and incidental feeding habits included
zoophages feeding on living animal material, necrophages feeding on carrion and coprophages feeding
on fecal material.
It is thought that the nutritional capability of oribatid mites is relatively extensive. Two decades
after Luxton´s classification later, Siepel and de Ruiter-Dijkman (1993) defined the feeding guilds of
mites based on carbohydrase activity and the dependence on cellulose, chitin and trehalose as food
sources in 49 species of oribatid mites and one member of acaridid mites (Siepel and de RuiterDijkman, 1993). An analogous study was performed by Berg et al. (2002) on 20 Collembola species.
The enzymatic activity was used to define mite species which are able to digest both the cell wall and
cell contents and the species digest only the cell contents (Siepel and de Ruiter-Dijkman, 1993). They
suggested following feeding guilds: Herbivorous grazers are mites having cellulase activity only; feed
on both cell contents and the cell walls of green plants: (i) fungivorous grazers are mites with chitinase
and trehalase activity; feed on fungi and dead mycelium and are able to digest both cell contents and
the cell walls of fungi; (ii) herbo-fungivorous grazers are able to digest all main food components of
both green plants and fungi (chitin, trehalose and cellulose); (iii) fungivorous browsers are mites
digesting only trehalose and utilizing cell contents of fungi; (iv) opportunistic herbo-fungivores are
able to digest cellulose in litter and cell walls of living green plants and trehalose in fungi; (v)
herbivorous browsers are lacking cellulase, chitinase and trehalase activities; these could be predators,
necrophages or bacteriophages. The last one is omnivores as an unexpected guild which is not
distinguished based on carbohydrase activity.
The enzymatic analyses showed that stored product and house dust mites are able to feed on higher
plant material and on microflora (Erban and Hubert 2008, Erban et al., 2009a, Erban et al., 2009b,
Hubert et al., 2011). The mites are panphytophagous species based on Luxton‟s classification
(Luxton, 1972). It includes their adaptation to digest bacteria and fungi. They are able to utilize
bacterial and fungal cell walls as well as bacterial and fungal cell content (Erban and Hubert 2008,
Erban et al,. 2009a, Erban et al., 2009b, Nesvorna et al. 2012).
Siepel and de Ruiter-Dijkman (1993) mentioned that carbohydrase activities, especially those for
the digestion of differentiating plant and fungal componen-ts, appear to provide a solid basis for the
feeding guild definition. It is thought that the quantitative data of enzyme activities is the best
characterization of guilds and estimation of proteolytic activity. Such classification was tested by
Bowman (1981) using activities of 19 hydrolases on ten populations respecting six different acaridid
species. In the study, Bowman identified differences in enzymatic activities among species. It was
firstlydocumented interspecies heterogen- ecity in digestive enzymes based on activity level between
different strains of mites. According to the classification of feeding guild, the suggestion was that R.
callae, R. robini and T. longior are phytophages, with relatively low proteolytic and chitinolytic
activity. L. destructor, G. domesticus and A. siro were classified as fungivores. The differences were in
level of proteolytic activity, which was higher in A. siro than in L. destructor and G. domesticus
(Bowman 1981).Sustr and Stary (1998) claimed that analyses of enzymatic activities in whole body
homogenates were erroneous. These authors mentioned that the activities in the whole body
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homogenates (WME) may be influenced by non-digestive enzymes and/or enzymes of microbial
origin. In addition, the discrepancies may be derived from in vivo versus in vitro enzyme action (Sustr
and Stary, 1998).
A review of the literature in which feeding guilds are proposed based on enzymatic activity
indicates the following limitations of prior research: (i) the authors did not mention that chitinase and
trehalase are used in nature primarily for purposes other than digestion; (ii) all animals having chitin
must be equipped with chitinases, which are used for molting processes (growth); (iii) chitinolytic
activity can be caused by the action of chitinase or other enzymes like lysozyme; (iv) any
invertebrates, especially insects, utilize trehalase to degrade trehalose, which functions as a source of
energy (i.e. flying) or a protectant against the effects of freezing or dehydration; (v) the presence of
trehalase in invertebrates is joined mainly with chitin metabolism and chitin synthesis during molting
processes. The problem is given by small size of mites in the comparison to insects and impossibility
of gut dissection. However the analyzes of feces or feces fractions (SGME) confirms the presence of
enzyme in the gut. The enzyme is produced by mesodeal cells into gut lumen and entrance into the
food boli and is passed via gut and defecated in feces. Many enzymes analyzed from WME and SGME
were considered to be digestive, but this interpretation of an enzyme‟s function is questionable in the
following cases: (i) when the enzymes were not purified from gut or feces and (ii) were not localized
in gut or feces; or (iii) were not analyzed with respect to the physiological pH of gut.
Cellulases are enzymes that are very rare in animals and are present in plants and bacteria. The
evaluation of cellulases as digestive enzymes must be based on localization in the gut or determination
of association with microorganisms rather than measuring cellulolytic activity. Nevertheless, the
presence of cellulases in mite extracts suggests presence of symbiotic bacteria in mites or presence of
digestive cellulases (Bowman and Childs, 1982).
The nature of above-mentioned limitations serves primarily methodological inaccuracies, the low
number of individuals and difficulty with their rearing limited the number of individuals for
experiments and the possibility of enzyme analyzes in the feces. The concept of feeding guilds is
possible to approximate on food sources available for mites. It is believed that house dust mites are
living in the house dust, however sometime are present in stored food (Matsumoto et al., 2001). The
house dust mites are found mostly in house dust where they can feed on the shed skin of humans and
domestic animals. The stored product mites occur in stored commodities including cereals and coral
products, oils seeds, dried fruits, root crops and ornamentals, honey, ham and dried milk and chesses
(Hughes, 1976). Recently, the stored product mite infestation of the animal feed, especially for dogs
has been reported (Brazis et al., 2008). The next habitats are mushrooms in mushrooms production
(Okabe, 1999) or fungal laboratory cultures (Duek et al., 2001).
For the purchase of the review we have simplified the food sources for synanthropic mites according
to previously mentioned concepts of feeding guilds as follows: (i) structural proteins - keratin, collagen,
elastin in dead animal skin, nails and hairs; (ii) “unstructural” proteins in plant product (e.g. lettuce and
rape seeds), chesses, dried milk, pet feed and microorganisms; (iii) lipids are presented in plant cells,
cheeses, dried milk, pet feed, microorganisms, cheese and dried milk products and dried meat; (iv)
structural carbohydrates in plant cell walls in plant debris in stored products (e.g. grain): cellulose,
hemicellulose; (iv) storage carbohydrates in plant cells: starch, glycosides; (v) sucrose in dried fruits and
honey; (vi) fungal hyphae, spores and yeasts are formed from cell walls: chitin and some bacteria has
murein in their cell walls; (vii) fungal and yeast cell contents containing storage compounds like
trahalose, starch and lipids.

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3. Gut Morphology of Synanthropic Acaridid Mites
A generalized diagram of the mite gut is shown in Figure 1. The following compartments of the gut
of synanthropic acaridid mites have been described: (i) foregut – pharynx and esophagus; (ii) midgut –
ventriculus, paired caeca, colon, intercolon and postcolon; and (iii) hindgut – anal atrium (Sobotnik et
al., 2008a, Wu et al., 2009). The caeca and ventriculus compose a large portion of the gut. Thus, it is
suggested that these organs play a key role in food digestion (Wu et al., 2009). Some species of mites
also have a postcolonic diverticula in their gut (Sobotnik et al., 2008a, Wu et al., 2009), which can host
bacterial symbionts (Sobotnik et al., 2008a, Hubert et al., 2011).
Mites digest food using cheliceres. Food then enters the pharynx and passes through the esophagus
into the ventriculus (Sobotnik et al., 2008a). The ventricular and caecal lumen contains fine particles,
which are probably of mucoid nature, and digestive enzymes. Endogenous enzymes are produced by
secretory cells in the ventriculus and caeca (Hughes 1950, Kuo and Nesbitt, 1970). The ingested food
is concentrated into the middle of the ventriculus and becomes enveloped by a peritrophic membrane
(Wharton and Brody, 1972), which includes chitin (Sobotnik et al., 2008b). The enzymes that are
enclosed by or attached to the peritrophic membrane are concentrated into fecal pellets, resulting in
higher proteolytic activity in the feces than in the whole body (Stewart et al., 1992a, Stewart et al.,
1994b). The food bolus then passes to the colon and intercolon. The next part of the midgut is the
postcolon, a long, wide chamber that is separated from the intercolon by an inconspicuous
constriction. Finally, the food bolus enters the anal atrium and is defecated (Sobotnik et al., 2008a).
For some in vivo studies the intercolon was omitted for description because of its hard distinguishing
from colon (Erban and Hubert, 2011).
4. Role of pH in Digestion
The pH of the gut contents is one of the most important factors that affects digestive processes,
acaricidal function and pathogen infection success. Therefore, study of digestive enzymes must be
performed with respect to the gut physiological pH (Terra and Ferreira, 1994, Regel et al., 1998,
Funke et al., 2008). The pH of the midgut lumen is actively regulated and varies with phylogeny and
feeding ecology (Harrison, 2001). The gut physicochemical properties are optimized with respect to
the food source (Zimmer and Brune, 2005). The pH in the gut is important for the activity of digestive
enzymes.
Studies of digestive enzymes should take into account the physiological gut pH. Previous studies
have determined the acidobasic conditions in the mite gut range from pH 5.4 to 6 in the ventriculus
and caeca, from pH 5.9 to 7.4 in the colon and from pH 6.5 to 8 in the postcolon (Hughes 1950,
Wharton and Brody, 1972, Akimov and Barabanova, 1976a, Akimov and Barabanova, 1978, Akimov,
1985). The mentioned studies used 18 indicators to measure the pH in vivo after indicator ingestion.
Many indicators are toxic, therefore limits the number of available compounds is limited. In the
studies, the pH was determined to an accuracy of 0.1 pH units. This is impossible using acidobasic pH
indicators, because each pH indicator determines the pH at an accuracy of pH ± 1. Erban and Hubert
(2008) determined the gut pH in twelve species of acaridid mites using 18 indicators. The gut contents
of acaridid mites were determined to be within a pH range of 4 to 7 and showed a pH gradient from
the anterior to the posterior mesodeum. The anterior mesodeum (ventriculus and caeca) of most
species has a pH ranging from 4.5 to 5, or slightly more alkaline, whereas the middle mesodeum
(intercolon/colon) has a pH of 5 to 6. The pH of the posterior mesodeum (postcolon) is the most
alkaline part of the gut and the pH ranges between 5.5 and 7. Differences were found only in D.
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farinae and D. pteronyssinus, which had a more acidic anterior gut (pH of 4 to 5) and colon (pH of 5)
with postcolon (pH of below 6) (Erban and Hubert, 2010b). House dust mites were unique due to their
acidobasic conditions in gut. The acidic buffering in gut of Dermatophagoides spp. corresponds to
their preferred food source in comparison to the mites that predominate in stored products (Erban and
Hubert, 2010b). Finally, it is necessary to mention that digestive enzymes should have an optimal pH
in the range of 4 to 7. This is crucial for maintaining the digestive enzymatic activity in the feces,
which are commonly used as the source of digestive enzymes for mites. Otherwise the enzymatic
activity which showed maxima out of observed pH indicating no digestive activity (Erban and
Hubert, 2010b).

Figure 1. Schematic model 3D of Acarus siro gut, A – dorsal view; B – lateral view, C –front view. Legend: 1 –pharynx, 2
esophagus, 3 ventriculus, 4 caecum, 5 colon, 6 intercolon, 7 postcolon, 8 poscolonic diverticula, 9 anal atrium.

The gut pH also plays an important role in bacterial colonization (Funke et al., 2008). It can also
influence the solubility of food components, the dissociation or coagulation of ingested proteins, and
the presence of gut microflora (Funke et al. 2008). Bacterial colonization is limited to the mite
mesodeum; however the mesodeum conditions are not friendly for symbiotic bacteria due to the
presence of mildly acid pH and many antibacterial proteins and proteases (Erban et al., 2009a). In spite
of that bacteria are highly abundant postcolonic diverticula of A. siro (Sobotnik et al., 2008).
5. Digestive Enzymes Necessity for Utilization of Food Sources
5.1. Proteolytic Enzymes and Digestion of Proteins
Proteases catalyze the hydrolytic cleavage of peptide bonds of proteins and peptides.
Endopeptidases split proteins into smaller peptides by targeting peptide bonds near the center of the
molecule and may cause esterolysis, and they exhibit various degrees of amino acid specificity
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(Berrens, 1968). The exopeptidases, aminopeptidases (EC 3.4.11) and carboxypeptidases (EC 3.4.16 –
3.4.18) act only near the ends of polypeptide chains.
Proteases in domestic mites have been intensively studied since they are compounds of high
allergenic hazard. Even though many studies have been performed, comparative studies are very rare.
The enzymatic activities from the literature had some discrepancies in the evaluation of the data. For
example, Ortego et al. (2000) analyzed the proteolytic activities with a highest activity measured at pH
10 in the feces (Ortego et al., 2000). Monteallegre et al. (2002) reported the activity and the inhibition
of serine proteases in the mite bodies at pH 7.8 and 7.4 (Montealegre et al., 2002). The results of
digestive function were incorrect in accord with the pH in mesodeum of mites (Erban and Hubert,
2010b).
Mite endopeptidases belong to one of the following three groups: (i) serine proteases (EC 3.4.21),
with the presence of a serine residue in the active site involved in catalysis; (ii) cysteine proteases (EC
3.4.22), utilizing a Cys residue for their catalytic activity; and (iii) aspartate proteases (EC 3.4.23),
utilizing Asp residue for catalysis (Beyon and Bond, 2001).
The comparative analysis of proteases in homogenates of seven mite species showed very low
activity towards BApNA (Nα-Benzoyl-D,L-arginine 4-nitroanilide hydrochloride) at pH 5 and 6,
indicating that trypsin-like proteases are likely to be of limited functional importance (Erban and
Hubert, 2010a). In addition, there is a possible effect of cysteine proteases (group one mite allergens)
on BApNA, indicating a lower trypsin activity in the whole body extracts or lower affinity to the
substrate (Erban and Hubert, 2010a).
Trypsin serine proteases (EC 3.4.21.4) preferentially cleave protein chains with Arg and Lys
residues (Weiner et al., 1985). Trypsin-like serine proteases were identified in whole mite extracts and
in feces (SGME), suggesting their digestive potential (Stewart et al., 1992a, Stewart et al., 1992c,
Ando et al., 1993, Stewart et al., 1994a, Stewart et al., 1994b, Ortego et al., 2000, Sanchez-Ramos et
al., 2004). The molecular weight of mite trypsins ranges from 28 kDa to 30 kDa. In addition, Der f3, a
trypsin allergen, was shown to be localized in the postcolon and in fecal pellets using monoclonal
antibody against recombinant Der f3 (Zhan et al., 2010).
Chymotrypsins (EC 3.4.21.1) are serine endopeptidases that preferentially cleave protein chains on
the carboxyl side of aromatic amino acids. The mite chymotrypsins are also considered to be digestive
enzymes, because their activity was identified in mite feces (Stewart et al., 1992a, Ortego et al., 2000,
Sanchez-Ramos et al., 2004). Mite chymotrypsins and trypsins are mite-derived allergens.
Chymotrypsin-like activity exhibited Grp 6 and Grp 9 mite-derived allergens (Table 1). Whereas Grp
6 are typical chymotrypsins, Der p9 is a collagenase, which is enzymatically similar to chymotrypsin
and Cathepsin G (King et al., 1996).
The optimal activity towards AAPpNA (N-Succinyl-L-alanyl-L-alanyl-L-phenyla- alanine 4nitroanilide), a chymotrypsin substrate, with optimum at pH 6 suggests that chymotrypsins play an
important role as digestive enzymes in mites (Erban and Hubert, 2010a). The presence of Der p9
allergens was predicted in the other seven species of synanthropic acaridid mites because high
proteolytic activity was observed towards chromogenic substrate MAAPMpNA (N-MethoxysuccinylL-alanyl-L-alanyl-L-prolyl-L-methionine 4-nitroanilide), which is designed for Cathepsin G. In
addition, this is supported by the fact that the proteolytic activity in seven species of mites was similar
using azocol as a substrate in comparison to MAAPMpNA (Erban and Hubert, 2010a). The high level
of activity of chymotrypsin-like enzymes at a pH corresponding to the mite gut pH led to the
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conclusion that proteases exhibit chymotrypsin-like activity and may be the primary digestive
proteases in mites (Erban and Hubert, 2010a).
The most familiar mite allergens are Grp 1 (Table 1), which are termolabile glycoproteins that are
structurally homologous to Cathepsins B and H, papain and actidine (Khlgatyan and Perova, 1995).
The activity of these 24- to 39-kDa proteins has traditionally been attributed only to cysteine protease
activity. More recently, it was established that Der p1 contains both cysteine and serine components
with a maximal activity at pH 6 and 8 (Brown et al., 2003). These allergens are localized in the
digestive tract and feces of pyroglyphid mites (Tovey et al., 1981, Tovey and Baldo, 1990); the
greatest enzyme concentration is observed in the ventriculus and caeca (Thomas et al., 1991). The
possible digestive function of Grp 1 mite allergens may be related to the replacement of serine
proteases by cysteine proteases. This event was described in insects (Oppert et al., 2005). Ortego et al.
(2000) detected in T. putrescentiae a 3-fold greater Cathepsin B activity in the feces than in mite
bodies. In comparison, the activity of serine proteases was 50-fold higher in the feces (Ortego et al.,
2000). These results show that the digestive function of cysteine proteases may be minor in
comparison to serine proteases.
Low activity towards ZRRpNA (Benzyloxycarbonyl-L-arginine-L-arginyl 4-nitroanilide) at a pH
corresponding to the mite gut pH in the seven species of mites tested suggests a low Cathepsin B
activity. In addition, the effect of TCEP, an activator of cysteine proteases, showed a negative effect
on general protease activity at pH 5 and 6. Decreases in the general protease activity at pH 6 suggest a
higher cysteine protease activity at this pH (Erban and Hubert, 2010a). The low cysteine protease
activity is in agreement with the results obtained by Ortego et al. (2000), whereas serine protease
activity was much higher in the feces than the cysteine protease activity when comparing the WME
and SGME (Ortego et al., 2000). This indicated an unusual cysteine protease activity in mites (Ortego
et al., 2000). Nevertheless, the efficiency of proteolytic degradation in mites is based on the interplay
of serine and cysteine proteases.
In some insects, aspartate proteases are involved in digestion and are related to the replacement of
serine proteases (Terra and Ferreira, 1994). The digestive function of aspartate proteases in mites has
not been confirmed (Ortego et al., 2000, Nisbet and Billingsley 2000, Sanchez-Ramos et al., 2004).
Aspartate protease activity in mites is highest at pH 3 and is probably limited to acid lysozomes (Erban
and Hubert, 2010a).
Aminopeptidases hydrolyze single amino acids from the N-terminus of peptide chains. The activity
of leucine aminopeptidase was observed in the Dermatophagoides species and in Tyrophagus
putrescentiae (Stewart et al., 1992a, Ortego et al., 2000). Leucine and valine aminopeptidases were
detected in the extracts of A. siro and P. ovis (Nisbet and Billingsley, 2000). Insect glycoproteins
located in the midgut membrane are very similar to the enzyme aminopeptidase N (EC 3.4.11.2) and
serve as a receptor for δ-endotoxins of insecticidal Bacillus thuringiensis (Knight et al., 1994, Budatha
et al., 2007). Optimal and high aminopeptidase activity corresponding to the mite gut pH was observed
in seven species of acaridid mites (Erban and Hubert, 2010a). Carboxypeptidases act at the free Cterminus of polypeptides and liberate single amino acid residues. Carboxypeptidases A and B are 50fold more active in feces extracts than in the mite homogenates of T. putrescentiae, indicating a
digestive function (Ortego et al., 2000). In addition, carboxypeptidases A and B have been detected in
D. pteronyssinus and D. farinae (Stewart et al., 1991).
Collagen, keratin and elastin are thought to be an important food source for pyroglyphid mites (van
Bronswijk and Sinha, 1973). In addition, Bowman (1981) suggested that collagenous material could be
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digested by A. siro, L. destructor, G. domesticus, R. callae and R. robini mites (Bowman, 1981b).
However, these substrates are not a suitable source of nutrition for acaridid mites (Bowman, 1981b).
Ortego et al. (2000) did not find elastase activity in T. putrescentiae (Ortego et al., 2000). Proteolytic
activity towards the substrates azocol, keratin azure and SA3pNA (N-Succinyl-L-alanyl-L-alanyl-Lalanine 4-nitroanilide) was confirmed in D. farinae and in six species of stored product mites;
however, the majority of digestion occurred in basic pH. The low activity towards keratin and collagen
suggests that these substrates are not important sources of energy for mites. However, it is
hypothesized that the effective utilization of these substrates is mediated by symbiotic microorganisms
growing on the substrate (Erban and Hubert 2010a). Although Ortego et al. (2000) did not report
activity using SA3pNA, we found hydrolytic activity to the substrate in seven species of acaridid mites.
The fact that activity on SA3pNA was similar to activity on ZRRpNA may indicate an interaction
involving these two (elastase and cathepsin B and/or trpysin) enzyme actions (Erban and Hubert
2010a).

5.2. Digestion of Starch, Maltose and Sucrose (Glycosidases)
Glycosidases are enzymes that catalyze the hydrolysis of a bond joining the sugar of a glycoside to
an alcohol or to another sugar unit. The most abundant class of organic compounds found in stored
plant products are, especially in cereals, carbohydrates (saccharides). Starch and sucrose are the
primary digestible carbohydrates (Nichols et al., 2003). Starch is degraded by the combined action of
α-amylases (EC 3.2.1.1), α-glucosidases (EC 3.2.1.20) and α-dextrinases (EC 3.2.1.10; EC 2.4.1.2).
The products of α-amylase are maltotriose and maltose from amylose. Amylopectin is hydrolyzed to
maltose, glucose and a lesser amount of dextrin. Sucrose is degraded by invertase (betafructofuranosidase) enzymes (EC 3.2.1.26) (Voet and Voet, 2003).
The enzymatic activities of α-amylases and α-D-glucosidases have been measured in many species
of acaridid mites (Matsumoto, 1965, Akimov and Barabanova, 1978, Bowman and Childs, 1982,
Bowman, 1984, Akimov, 1985, Morgan and Arlian, 2006). Additional amylase isoforms have been
observed in the WME and SGME of mites (Stewart et al., 1992a, Stewart et al., 1998). In addition, αamylases are Grp 4 mite allergens and their molecular weight ranges from 56 to 60 kDa (Table 1).
The activities of α-amylases and α-glucosidases differed among compared nine species of
synanthropic mites (Erban et al., 2009b). These differences were suggested as adaptations to starch
digestion. The optimal pH for the digestion of starch, maltose and sucrose in the WME and SGME of
nine species of synanthropic acaridid mites ranged from pH 4 to 6.75, with maximal activity at pH 5
(Erban et al., 2009b). These results are in agreement with previously reported data using mites
(Hughes, 1950, Matsumoto, 1965, Akimov and Barabanova, 1976b, Akimov and Barabanova, 1978,
Akimov, 1985, Lake et al., 1991a, Lake et al., 1991b, Sanchez-Monge et al., 1996). Enzymatic activity
in the anterior mesodeum (Erban and Hubert, 2010b) and the equivalent release of glucose from four
types of starch (i.e. corn, wheat, potato and rice), amylopectin, dextrin, maltose and sucrose by
hydrolysis of WME and SGME indicated that the enzymes digesting these substrates are produced in
the anterior mesodeum, not in the tissues of mites. The species with higher starch hydrolytic activities
in the SGME are more tolerant of acarbose (unspecific α-amylase and α-glucosidase inhibitor), which
inhibits starch digestion. The high specific hydrolytic activities of α-amylase and maltase
demonstrated the importance of their synergetic activity in producing glucose from the starch (Erban et
al., 2009b).

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The stored product mites A. siro, A. ovatus, T. lini and L. destructor exhibit elevated starch
digestive activity associating with starch-type substrates. While D. farinae, C. arcuatus and S. berlesei
(syn C. redickorzevi) are associated with sucrose, T. putrescentiae and C. lactis have low or
intermediate enzymatic activity on the starch-type substrates and sucrose (Erban et al., 2009b). Starch
digestion was localized by in vivo observation of starch azure digestion and the primary component of
starch digestion was in the ventriculus and caeca; however, digestion also occurs in the colon and
postcolon. Only D. farinae showed very poor activity towards starch azure as determined by in vivo
observations. This is consistent with the wide pH range for optimal starch and maltase digestion (4 to
6.75) (Erban et al., 2009b). Nevertheless, the addition of sucrose to the diet did not positively
influence mite population growth, and A. siro, A. ovatus, T. lini, L. destructor and T. putrescentiae
showed an accelerated increase in population on a starch-enriched diet (Erban et al., 2009b).

5.3. Digestion of Structural Plant Polysaccharides
Polysaccharide cellulose is widely distributed in few bacteria, protists, fungi, invertebrate animals,
and plants. It is the most abundant compound in plant cell walls, contributing to approximately 20–
40% of its dry weight (Watanabe and Tokuda, 2010). Cellulose is a linear polymer that consists of β1,4-linked D-glucopyranosyl units. Cellulose differs from starch and glycogen and is extremely hard to
digest due to its structure. The enzymes that digest cellulose are cellulytic enzymes, of which three
classes are recognized: endoglucanases (EC 3.2.1.4), exoglucanases (EC 3.2.1.74 and 3.2.1.91), and βglucosidases (EC 3.2.1.21) (Watanabe and Tokuda, 2010).
Cellulolytic activity was detected in several stored product mites (A. ovatus, A. siro, R. echinopus,
T. entomophagus), whereas most of the mites lacked cellulose activity (Bowman and Childs, 1982,
Bowman, 1984). Nevertheless, to date, any mite cellulase has not been isolated or characterized. The
optimal pH for cellulolytic activity in the WME of acaridid mites varies from pH 5 to 8 and showed
more optima in one species (Akimov and Barabanova, 1976a, Akimov, 1985). Bowman and Childs
(1982) suggested that the cellulolytic activity is a result of microorganism exoenzymes in the mite gut
(Bowman and Childs, 1982).

5.4. Digestion of Lipids
Lipids serve as a source of energy for mites and are present in seeds and in the fat of animals and
fungi as well as in cell membranes (Voet and Voet, 2003). Esterases digest lipids (EC 3.1.-.-), and
lipases are a subclass of esterases. Esterases and lipases both hydrolyze ester bonds. Whereas the
lipases display high activity towards the substrate in an aggregated state, the activity of esterases is
typically highest toward the soluble state of the substrate (Fojan et al., 2000).
Alkaline phosphatase (EC 3.1.3.1) and acid phosphatase (EC 3.1.3.2) activity has been detected in
acaridid mites (Bowman, 1984, Stewart et al., 1992a). Lipases were detected in the spent growth
medium extracts (SGME) of house dust mites and are thought to be digestive (Stewart et al., 1991,
Stewart et al., 1992a). A comparative study showed that extracts of A. siro and P. ovis contain acid and
alkaline phosphatase, C4 and C8 esterases and lipase. A. siro has low C14 lipase activity in
comparison to C4 esterase and C8 esterase lipase (Nisbet and Billingsley, 2000).
Enzymes acting at an ester bond are also important in the development of resistance to pyrethroids,
organophosphates and carbamates. An increase in esterase activity in comparison to a control
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condition, is considered to provide metabolic resistance (Li et al., 2007). The organophosphates
resistance was well documented in stored product mites (Szlendak et al., 2000).

5.5. Digestion of Microorganisms
5.5.1 Bacteriolytic Enzymes
To utilize nutrients from bacteria, bacterial cell walls must be digested. Because bacterial cell walls
are small in size (usually 1 to 3 µm in diameter) they are ingested without mechanical damage by
chelicerae, unlike the ingestion of larger fungal mycelium and spores (Schuster, 1956, Kaneko, 1988,
Sobotnik et al., 2008a). Bacteria were not considered to be a mite food source (Luxton, 1972, Sinha
and Harasymek, 1974, Siepel and de Ruiter-Dijkman, 1993). Nevertheless, Sinha and Harasymek
(1974) observed the survival and reproduction of G. domesticus and A. siro using six species of
bacteria as a food source. Mortality was relatively high, but the mites were able to be longer survive on
pure bacteria for more than seven days in comparison with starve mites. Although the mortality on a
diet of pure bacteria was relatively high, mites were able survive for more than 50 days. A difference
in tolerance to various species of bacteria was observed (Sinha and Harasymek, 1974). Symbiotic
mite-bacterial interactions are hypothesized to exist, especially the breakdown of hard digestible
polysaccharides by microflora in the gut, especially chitin (Smrz et al., 1991).
The diverse bacterial community was observed in the parasitic sheep scab mite P. ovis (Acari:
Psoroptidae) suggesting that P. ovis digestive enzymes are supplemented with bacteria as a direct and
indirect source of nutrition (Hogg and Lehane, 1999, Nisbet and Billingsley, 2000, Hamilton et al.,
2003). The bacteria were identified in the whole body homogenates in D. pteronyssinus and D. farinae
(Oh H and T. Y. I. K., 1986, Valerio et al., 2005), A. siro, L. destructor and T. putrescentiae (Hubert et
al., 2011). In the bacterial community, bacteria Bacillus and Staphyloccocus have been identified
based on by culturing and culture-independent approaches and bacteria are suggested as nutrients for
mites (Hubert et al., 2011).
Lysozymes are thought to digest bacterial cell walls. Lysozymes (1,4-β-N-acetylmuramidase; EC
3.2.1.17) are enzymes that break down peptidoglycan (murein), a component of the bacterial cell wall,
by hydrolyzing the β(1 → 4) glycosidic bond from N-acetylmuramic acid (NAM) to Nacetylglucosamine (NAG) (Chipman and Sharon, 1969). Lysozymes are widely distributed and are
present in many animals (Callewaert and Michiels, 2010). The primary function of this enzyme is to
protect against attack by pathogenic bacteria, as a part of the nonspecific immune system (Jolles and
Jolles, 1984). However, in many invertebrates and vertebrates, lysozymes have a digestive function
(Callewaert and Michiels, 2010). These digestive lysozymes are resistant to proteolytic degradation
(Lemos et al., 1993). Furthermore, lysozymes exhibit weak non-specific esterase and proteolytic
activity. These activities are topographically distinct form the lysozyme lytic site (Jolles and Jolles,
1983, Oliver and Stadtman, 1983). The digestive function of lysozymes has been studied in
haematophagous mites, such as the soft tick Ornithodoros moubata (Grunclova et al., 2003). In mites,
lysozyme activities were detected in the WME and SGME in the stored product and house dust mites
(Childs and Bowman, 1981, Stewart et al., 1992b, Stewart et al., 1998). The lysozymes of D. farinae
and D. pteronyssinus have a molecular weight of 10 kDa to 13 kDa and are optimally active in a pH of
6.2 (Stewart et al., 1991, Stewart et al., 1992b). There are many lysozyme isoforms present in L.
destructor (Stewart et al., 1998).

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Although the bacterial cell wall is highly resistant to disruption by the proteases (Voet and Voet,
2003), some proteases have evolved the ability to digest these walls. In the larvae of Musca domestica
(Diptera: Cyclorrhapha), the central region of the midgut can digest bacteria. These larvae grow in
decaying organic material and digest material under acidic pH using digestive lysozymes and
cathepsin D-like (aspartate) proteases (Espinoza-Fuentes et al., 1987, Lemos and Terra, 1991a, Lemos
and Terra, 1991b). Similarities were found among cyclorrhaphan larvae, Anastrepha fraterculus
(Lemos and Terra, 1991a), and Drosophila melanogaster (Kylsten et al., 1992, Regel et al., 1998).
Whereas the acid conditions in the ventriculus and caeca are favorable for digesting bacteria, the
digestive function of aspartate proteases in mites has not been confirmed (Ortego et al., 2000, Nisbet
and Billingsley, 2000, Sanchez-Ramos et al., 2004).
Hubert and Erban (2008) confirmed the presence of lysozyme-like activity in the WME and SGME
of 14 species of synanthropic acaridid mites. The optimal pH of lysozymes was 4.5 in SGME for the
majority of the species tested. The commercial anti-lysozyme antibodies to HEWL were applied to
identify lysozyme in the feces of HDMs (D. farinae and D. pteronyssinus (Erban et al., 2012). The
antibodies identified HEWL type of lysozyme in whole body homogenates and feces. In confirmed
digestive activity of lysozyme (Erban et al., 2012). Eight species of astigmatid mites showed a higher
rate of population growth on a Micrococcus lysodeicticus additive diet than on a control diet (Erban
and Hubert, 2008). The lysozyme activity in the SGME of mites positively correlated with the
standardized rate (rs) of population growth, although no correlation was found between r s and
lysozyme activity in the WME. The lysozyme activity in the WME was negatively correlated with that
in the SGME.
The digestion of bacteria was examined using fluorescein-labeled M. lysodeicticus cells. Digestion
of bacteria began in ventriculus and continued during the passage of a food bolus through the gut.
Fluorescein was absorbed by mesodeal cells and penetrated the parenchymal tissues (Erban and
Hubert, 2008).
Because studies have determined that proteolytic enzymes participate in the digestion of bacteria in
insect guts (Espinoza-Fuentes et al., 1987, Lemos and Terra, 1991a, Lemos and Terra, 1991b), it is
possible that this occurs in mites. The cysteine proteases, formerly Grp 1 mite allergens, could be
candidates. It supported observed hydrolytic activity of D. fariane and D. pteronyssinus extracts to
gram negative bacteria Escherichia coli in vitro (Stewart et al., 1991, Mathaba et al., 2002).
Hydrolyzes of green fluorescent protein expressing E. coli in mesodeum mites was confirmed in vivo
in Dermatophagodies farinae and D. pteronyssinus (Erban et al. 2012).
The bacteriolytic activity observed in D. farinae showed that this mite is adapted to digest bacteria.
On other hand, similar species, such as D. pteronyssinus, have a lesser degree of adaptation to feed on
bacteria (Erban and Hubert, 2008). Both Dermatophagoides species are not identical, even though they
live in the same habitat and in mixed populations. Valerio et al. (2005) found that 16S ribosomal DNA
from D. farinae contained a significantly greater number of copies of DNA encoding 16S ribosomal
RNA than did D. pteronyssinus, indicating a greater diversity of bacterial strains in D. farinae (Valerio
et al., 2005). This suggests a higher degree of bacteriophagy in D. farinae than in D. pteronyssinus
(Erban and Hubert, 2008).
It appears that, although D. farinae has low proteolytic activity, it is able to digest bacteria with
higher efficiency. It is probable that house dust mites tend to rely on microphagy more than the other
species. A similar situation is suggested for P. ovis, which is most likely an ancestor of
Dermatophagoides spp. (Hamilton et al., 2003). In addition, it could be stated that D. farinae is the
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most unique mite of the species studied, not only in relation to its acidobasic properties and proteolytic
activity, but also for its high degree of bacteriophagy.
The hypothesis of OConnor (1979) that Dermatophagoides spp. is derived from species inhabiting
the nests of birds is consistent with the fact that these mites inhabit house dust, where keratin and
collagen are widely distributed. We suggest that these mites may have evolved relationships with
keratinolytic bacteria and fungi before synanthropization in the nests of birds. A similar situation is
possible for other species of mites that penetrated human environments through the nests of mammals.
Since the largest group of stored product mites is derived from the nests of mammals, especially
rodents (OConnor, 1979, OConnor, 1982), these mites may have adapted the ability to digest food
stored by the rodents as well as the ability to interact with keratinolytic and collagenolytic
microorganisms growing on hair and skin found in the nest. This hypothesis is supported by the fact
that many stored product species are also found in house dust being considered domestic mites
(Colloff and Spieksma, 1992).
The analysis of digestive enzymes in mites is applicable to their nutritional biology, but there are
the limitations. Although mites are able to digest basic carbohydrates and proteins, in some
environments, they require the help of microbes to survive. The symbiotic interactions between mites
and microorganisms are importance to explore nutrient sources. Feeding on microorganisms
(microphagy) is a favorable digestive strategy for mites living in environments where they feed on the
skin, hair, nails and feathers from humans and animals. Dermatophagoides spp. and L. destructor were
the most unique mites tested. The different enzymatic properties of Dermatophagoides spp. are
probably due to environmental constraints. L. destructor has a uniquely high activity of digestive
enzymes, which was several-fold higher than in the other species tested.

5.5.2. Digestion Fungal Cells
It is well known that acaridid mites are associated with fungi which can serve as food source and or
produce some necessary nutrients for mites. Some micromycetes represent a food source for mites,
while others are low suitable for their development (Griffiths et al. 1959, Solomon 1964, Rodriguez et
al. 1984, Pankiewicz-Nowicka et al. 1986, Smrz and Catska 1987). For example D. pteronyssinus
population growth showed antagonistic effect to Aspergillus penicillioides (de Saint Georges-Gridelet
1987) however the mites were not able to survive in fungal free diets (Hay et al. 1993). Nine species of
fungi were isolated from D. pteronyssinus in house dust (Hay et al. 1992). The fungi are suggested to
provide the sterols and vitamins (van Asselt, 1998). Based on cultivation experiments and population
growth of Dermatophagoides spp., Petrova-Nijitina et al. (2011) suggested that A. penicilloides can
affect the ability of Dermatophagoides spp to explore the trophic substrates.
The stored product mites have fungal vectors and can undergo selective transfer (Sinha 1979,
Armitage and George 1986, Hubert et al., 2003). The primary mite-digested substances in fungi are
trehalose, chitin, glycogen, lipids, proteins and sugar alcohols. Fungi can perform extracellular
digestion by secreting enzymes into the environment and absorbing the nutrients thus produced. Fungi
store excess energy as glycogen, which has an analogous structure to plant starch. Glycogen is a starch
polymer of glucose. Whereas glycogen is composed of a branched chain of glucose units, starch is a
long, straight chain of glucose units (Voet and Voet, 2003). The combined action of amylases and αglucosidases digests glycogen and starch in mites (see section 2.3.3.2). The amylase-mediated
digestion of glycogen from spores and mycelia from fungi has been reported in mites Bowman and
Childs (1982).
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The major constituents of the fungal cell wall are glucan, chitin, and protein (Lee et al., 2010).
Chitin is a tough and rigid glucosamine homopolymer that functions as a protective structure in the
exoskeleton of fungi and arthropods. Chitinases are enzymes that hydrolyze the β(1,4)- N-acetyl-Dglucosamine bonds within chitin, an essential fungal cell wall component. Chitinases are enzymes
required for the growth and morphogenesis of fungi and arthropods, including mites (Alberti and
Coons, 1999, Adams 2004, Rao et al., 2005, Hurtado-Guerrero and van Aalten, 2007). Chitinolytic
enzymes include chitinase (EC 3.2.1.14), which catalyze the hydrolysis of internal bonds in chitin and
β-acetyl-D-glucosaminidase (chitobiase, EC 3.2.1.52), thus liberating N-acetylglucosamine from the
non-reduced end of oligosaccharides (Terra and Ferreira, 1994). Another chitinolytic enzyme is
lysozyme (see section 2.3.3.3.) (Skujins et al., 1973). In addition, some chitinases act similarly to
lysozyme and in some cases they can be utilized for defense against pathogens as well as lysozymes
(Minic et al,. 1998).
In general, chitinase functions in the molting process. Nevertheless, this enzyme is localized to the
midgut in some insect species (Terra et al., 1996). The utilization of chitin from fungal cell walls has
been studied (e.g. (Smrz and Catska, 1989, Siepel and de Ruiter-Dijkman, 1993). Chitinolytic activity
was detected in the WME of acaridid mites (Bowman and Childs, 1982) with an optimal pH of 5 to 7.5
(Akimov and Barabanova, 1976a, Akimov and Barabanova, 1976b, Akimov and Barabanova, 1978,
Akimov, 1985). More recently, the chitinase isoforms Der f15 and Der f18 (Table 1) have been
purified from D. farinae. Both chitinases are allergenic (McCall et al., 2001, Weber et al.,, 2003).
Localization of Der f15 using a monoclonal antibody showed intracellular distribution in the
proventriculus and intestine, suggesting a digestive rather than a molting-related function (McCall et
al., 2001). Der f18 is similar to Der f15, which is localized in the digestive system of D. farinae but
not to the feces (Weber et al., 2003).The chitinolytic activity observed in mesodeum and feces of D.
farinae and D. pteronyssinus in vivo using chitin azure (Erban et al. 2012). The still open question
remains is if the activity is caused by chitinases or lysozyme action.
Trehalose (α,α-trehalose) is a non-reducing and widely distributed disaccharide. This protein has
been isolated from several species of bacteria, fungi, invertebrates and plants. Trehalose functions as a
source of energy and protects against the effects of freezing or dehydration. (Richards et al., 2002,
Iturriaga et al., 2009). Trehalose is very stable (in comparison to sucrose and maltose) (Richards et al.,
2002) and the enzyme that splits trehalose into two glucose units is trehalase (EC 3.2.1.28) (Dahlqvist,
1962). Trehalase is one of the most widespread carbohydrases in insects (Terra and Ferreira, 1994)
The function of trehalose and trehalase have been studied extensively and appear to be speciesdependent (Richards et al., 2002).
Trehalose provides an energy source for flight in a variety of insects, and hydrolysis of trehalose is
likely to be a specific adaptation to flight (Clegg and Evans, 1961, Richards et al., 2002). The role of
trehalase in chitin synthesis during molting has also been reported (Tatun et al., 2008). In past decades,
the digestive function of trehalase has been described. Apical and basal trehalases have been found in
the insect midgut. The apical midgut trehalase is a true digestive enzyme, whereas the basal trehalase
probably plays a role in the midgut utilization of haemolymph trehalose (Terra and Ferreira, 1994). In
recent years, trehalases have been purified from several insect species and are divided into soluble
(Tre-1) and membrane-bound (Tre-2) proteins. The function of Tre-1 and Tre-2 has been investigated
in Spodoptera exigua. Tre-1 plays a major role in expression of the chitin synthesis gene A and chitin
synthesis in the cuticle. Tre-2 has an important role in the expression of chitin synthesis gene B and
chitin synthesis in the midgut (Chen et al., 2010).

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Trehalase has been detected in the WME of Tyrophagus similis and some oribatid mites (Siepel and
de Ruiter-Dijkman, 1993). However, mite trehalases have not been biochemically characterized,
although the presence of trehalase was suggested as an adaptation to the digestion of fungi in oribatid
mites (Siepel and de Ruiter-Dijkman, 1993). The still open question is the digestive function in
acaridid mites.

5.6. Miscellaneous Proteins Participating on Digestion
The antibacterial proteins are suggested the group 2 of allergens (Der p2 and Der f 2). Due to the
similar molecular size to lysozyme about 14 kDa, group 2 were suggested as lysozyme (Stewart et al.,
1992b). These proteins are produced by mesodeal cells and entrance to the food boli and after
defecation are presented in the feces (Park et al., 2000, Jeong et al., 2002, Park et al., 2002). However
the purified natural and recombinant allergens were lacking the lysozyme type of activity (Hakkaart et
al., 1997). The structure analyses reveal that the proteins show structural homology with MD-2, which
binds the liposaccharide (Ichikawa et al., 2009). If there is any bacteriolytic function of the group 2
mite allergens, it remains still open.
Mathaba et al. (2002) purified from the SGME of D. pteronyssinus a 14.5-kDa (size in BLAST)
protein with antibacterial activity and suggested prokaryotic origin of the protein. Based on PCR
analyses, the bacteriolytic protein was confirmed in D. farinae (Erban et al. 2012). The fact that PCR
products of the expected size (~243 bp) were obtained in both cases suggests that this bacteriolytic
protein is mite-derived (Erban et al. 2012).
6. Medical Importance of Digestive Enzymes as Allergens
Among allergens of house dust-mites, digestive enzymes cover about 44% of these compounds.
The proteases exhibited functionality as allergens, given by their proteolytical activities. Cysteine (Der
p1, Blo t1, Der f1) and serine (Blo t3, Der p3, Der f3, Eur m3, Blot 6, Der p6 and Der p9) proteases
provoke allergic reaction due to the allergenic epitopes and enzymatic activity. Proteolytic enzymes
appear to be particularly potent allergens in susceptible individuals, and are often recognized by more
than 90% of individuals allergic to their source (Stewart and Robinson, 2003)
A typical allergenic protease is the cysteine protease Der p1 in the house-dust mite D.
pteronyssinus. Similar proteases were shown to be produced by other members of the clinically
significant Pyroglyphidae family, D. farinae (Der f1) and E. maynei (Chua et al., 1988, Smith et al.,
1999). Additionally, a cysteine protease is the allergen of the non-pyroglyphid mite B. tropicalis (Blo
t1) (Mora et al., 2003). Blo t1 shared 35% identity with proteases of pyroglyphid mites, the allergen
share unique IgE-binding epitopes (Colloff, 2009). The existence of such epitopes increases the
relevance of the characterization of stored-product mites associated cysteine proteases (Erban and
Hubert, 2010a).
The recent progress on the immunology of mite allergens has clearly demonstrated the importance
of their enzymatic activity in the sensitization process. The best understood example is the cysteine
protease Der p1 from faecal pellets of the house-dust mite D. pteronyssinus (Tovey et al., 1981).
Proteolytically active Der p1 has been reported to cleave both CD23 (Hewitt et al., 1995) and CD25
(Schulz et al., 1998) from the surface of immune cells. Through cleavage of the membrane-associated
CD23, the low affinity receptor for IgE, it is postulated that IgE production may become deregulated,
owing to the lack of feedback inhibition by IgE-CD23 engagement on B cells (Hewitt et al., 1995,
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Schulz et al., 1995). Der p1-mediated cleavage of CD25, the binding component of the high affinity
IL-2 receptor, may bias the T-cell immune response towards an allergic Th2 type (Schulz et al., 1995).
Proteolytically active Der p1 is also able to polarize the immune response to a second antigen by
reducing the Th1 protective response (Comoy et al., 1998). Der p1 critically contributes to the tissue
pathology observed in asthmatic airways as it can increase the passage of proteins across epithelial
monolayer (Herbert et al., 1995). This increased epithelial permeability is likely to occur due to
cleavage of tight junction proteins (Robinson et al., 1997). In addition, Der p1 catalytically inactivates
a naturally occurring serine protease inhibitor, namely 1-antitrypsin (Kalsheker et al., 1996), which
protects lung epithelial cells from damage mediated by endogenous or exogenous serine proteases. Der
p1 is a potent inducer of proinflammatory cytokines from the respiratory epithelium, and its action is
mediated by the protease-activated receptor PAR-1 (Asokananthan et al., 2002).
Except proteases, IgE epitopes for α-amylase (Blo t4 and Der p4) (Mills et al., 1999, Cheong et al.,
2009), and chitinases (Der p15, Der f15, Der p18 and Der f 8) (McCall et al., 2001, Weber et al., 2003,
O'Neil et al., 2006) were described. The cloned Blo t4 had a molecular weight of 56 kDa and shared
68% amino acid homology with group 4 allergens of D. pteronyssinus and 65% with those of E.
maynei (Cheong et al., 2009). The effect of enzymatic activity of α-amylases to the human immune
system has not been studied yet. The cloned Der p15, showed two variants of 58.8 and 61.4 kDa,
respectively. The amino acid sequences had 90% identity to Der f15. The cDNA for Der p 18 encoded
a mature protein of 49.2 kDa with 88% sequence identity to Der f 18. Der p15-specific IgE was
detected in 70% and Der p18-specific IgE in 63% of a panel of 27 human allergic sera (O'Neil et al.,
2006).

7. Possible Interaction to Microorganisms in Utilization of Food Sources
The gut and fat contain associated microflora that produce exogenous enzymes (Smrz, 2003).
Members of the intestinal microbial community of soil oribatid mites and T. putrescentiae have the
ability to decompose cellulose, chitin and lignin (Stefaniak and Seniczak, 1976, Smrz, 2003). Bowman
and Childs (1982) suggested that cellulolytic activity seems to be a result of microorganisms and their
exoenzymes in the mite gut. Chitinase and trehalase activity in mites assist in the mite digestive
process, as do bacterial exoenzymes and the symbiotic relationship between bacteria and mites (Smrz
et al., 1991, Smrz, 1998, Smrz and Trelova, 1995). In A. siro, the transmission microscopy (TEM)
observation of the gut showed that the postcolonic diverticula, sometimes called „„Malphigian tubules
(Hughes, 1950), harbored symbiotic bacteria (Sobotnik et al., 2008a). In addition, TEM observations
of the gut in this species revealed that bacteria in the gut are active and produce exoenzymes
(“hydrolyzed halos” around bacteria) (Hubert et al., 2004). Hubert et al. (2012) found among cloned
sequence of 16S RNA gene from mites the sequences of Sphingobacteriales. In D. farinae the clones
clustered to the sequences of “Ca. Cardinium hertigii”. In A. siro, the cloned sequences of
Sphingobacteriales formed a separate cluster distinct from "Ca. Cardinium hertigii".
The type of species and pattern of feeding and digestion is important for the relationship between
the mites and internal/extraintestinal bacteria. The amount of bacteria in mesenchymal tissue of T.
putrescentiae was correlated with chitinase activity in mite homogenate. Serratia marcescens exhibit
strong chitinolytic and trehalolytic activity in T. putrescentiae (Smrz, 2003).
Our knowledge about microbial symbionts in mites has strong impact in understanding their
feeding ability because the mites: (i) are able to digest bacteria and them as food source (Erban and
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Hubert, 2008); (ii) bacterial community that is associated with the host tells much about the host its
defense/bacterial pathogenic importance and the symbiotic effect is possible also; (iii) the microbes
associated with the mites are possible sources of allergens or endotoxins and may be unacceptable in
therapeutics against mite allergy.
8. Conclusions
A wide range of the enzymatic activities were characterized for a spectrum of synanthropic acaridid
mite species. These in vitro enzymatic results are supported by biotests and by the in vivo observation
of enzymatic activity in the mite gut. The gut contents of acaridid mites were determined to be within
a pH range of 4 to 7. Enzymatic activity outside of this pH range is not considered to be related to
digestion.
The mites are equipped by digestive enzymes for utilizations of the food sources in their habitats. The
review indicates that the mites are well equipped for digestion of proteins in stored plant product,
chesses, dried milk, pet feed and in microorganisms. The lipases and esterases help with utilization of
lipids contained in plant cells, cheeses, dried milk, pet feed, microorganisms, cheese and dried milk
products and dried meat. The carbohydrases participate on utilization of storage carbohydrates in plant
cells and sucrose. All reviewed species are well adapted to digestion of fungal hyphae, spores and
yeasts are formed from cell walls: chitin and some bacteria have murein in their cell walls and fungal
and yeast cell contents. However we did not find relevant activity of enzymes hydrolyzing structural
proteins (keratin, collagen, elastin in dead animal skin, nails and hair) and structural carbohydrates in
plant cell walls (cellulose, hemicellulose). The low level of collagen and keratin digestion of substrates
at the mite midgut pH suggests that keratin and collagen are not important direct sources of nutrients.
Thus, we hypothesize that the effective utilization of nutrients from skin, hair, nails and feathers by
mites is possible through the symbiotic interactions of mites with keratinolytic and collagenolytic
bacteria and fungi.
Why do different species of mites have different enzymatic activity? This may be due to differences in
nutritional needs among different species. For example, very low protease activity to hydrolyze starch
in D. farinae may correspond to a lesser nutritional need; this may also be true for C. lactis, which has
low saccharase activity. Therefore, the level of enzymatic activity may or may not correlate with the
preferred food source but, rather, may be due to nutritional needs. This factor also corresponds with
mite population growth. The stored product mites often found in stored grain containing high
concentration of storage polysaccharides, such as A. siro, A. ovatus, L. destructor and T. lini, are
enzymatically best adapted for the digestion of starch (Erban et al., 2009b). In contrast, other mites,
such as D. farinae, C. arcuatus and S. berlesei (syn C. redickorzevi), are associated with sucrose
digestion (Erban et al., 2009b). T. putrescentiae and C. lactis exhibited low or intermediate activity on
starch and saccharose. C. lactis is a species that infests materials with high sugar content, especially
dried fruit (Hughes, 1976, OConnor, 1979, Halliday, 2003). But C. lactis exhibited only intermediate
activity on sucrose (Erban et al., 2009b). The biotest results using a starch dietary additive suggest that
starch enrichment increases the population growth of the mites. Examination of starch and sucrose
digestion in the nutritive biology of synanthropic acaridid mites showed that the mite gut is equipped
with enzymes that digest these saccharides.
Mites are able to feed on many types of food stored for human consumption as a direct food source
and also through symbiotic interactions. Mite populations increased rapidly with the addition of
bacteria to the diet. Thus, bacteria offer an even higher nutrient benefit than does complex food, which
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is used in laboratory cultures (Erban and Hubert, 2008), or food enriched in starch, sucrose (Erban et
al., 2009b) or protein (Erban and Hubert, 2010a).
Any new knowledge about mite physiology enriches our knowledge about allergens that they produce
to human environment. Study of mite physiology is inherent part of study of allergenicity and vice
versa. Although importance of house dust as a cause of allergic disease has been obvious for many
years, attempts to purify allergens from house dust were initially unsuccessful. The purification
methods of allergens/antigens are pivotal for diagnosis and development of therapeutics and inn
addition for the study of mite physiology. Nowadays are available recombinant and native proteins.
Due to unpredictable posttranslational modifications are antigens more useful than the recombinants
which still require purification steps (Erban and Hubert 2011).
Acknowledgement
The study was supported by the projects COST action CM0804, Grant No. OC10019; COST action
FA0703, Grant No. OC09034 and Kontakt, Grant No. ME09013. The authors also thank Veronika
Stixova for valuable help.

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31

Table 1. Classes of mite allergens (www.allergen.org – update list: November 2011).
Species

Molecular
weight
(kDa)

Description

1

25

cysteine
protease

2

14-18

NPC2 family

3

30

trypsin

4

60

amylase

5

14

unknown

6

25

chymotrypsin

7

22-28

unknown

8

26

9

24

10

36

tropomyosin

11

98

paramyosin

12

14

unknown

13

15

fatty acidbinding protein

14

80-100

apolipophorin

15

98

chitinase

16

53

gelsolin/villin

17

53

calcium
binding protein

18

60

chitinase

19

7

20

unknown

21

unknown

unknown

22

unknown

unknown

23

14

unknown

24

18

Troponin C

Gr.

Total

Aca
sir

Blo
tro
Blo
t1
Blo
t2
Blo
t3
Blo
t4
Blo
t5
Blo
t6

far
Der
f1
Der
f2
Der
f3

Der
mic
Der
m1

Der
f6
Der
f7

glutathion-Stransferase
collagenolytic serine
protease

Aca
s 13

antimicrobial peptide
homologue
arginine
kinase

Blo
t 10
Blo
t 11
Blo
t 12
Blo
t 13

Der
f 10
Der
f 11

Der
f 13
Der
f 14
Der
f 15
Der
f 16
Der
f 17
Der
f 18

pte
Der
p1
Der
p2
Der
p3
Der
p4
Der
p5
Der
p6
Der
p7
Der
p8
Der
p9
Der
p 10
Der
p 11

Der
p 14

Eur
may
Eur
m1
Eur
m2
Eur
m3
Eur
m4

Gly
dom

Lep
Des

Tyr
put

Gly
d2

Lep
d2

Tyr
p2

Lep
d5

Lep
d7

Lep
d 10

Tyr
p10

Lep
d 13

Tyr
p 13

5

Tyr
p24
4

Eur
m 14

Blo
t 19
Der
p 20
Der
p 21

Blo
t 21
Der
f 22

Der
p 23

1

12

14

1

15

5

1

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