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, 8 (9), e72770
eCollection

Insectivorous Bats Digest Chitin in the Stomach Using Acidic Mammalian Chitinase

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Insectivorous Bats Digest Chitin in the Stomach Using Acidic Mammalian Chitinase

Sara Strobel et al. PLoS One.

Abstract

The gastrointestinal tract of animals is adapted to their primary source of food to optimize resource use and energy intake. Temperate bat species mainly feed on arthropods. These contain the energy-rich carbohydrate chitin, which is indigestible for the endogenous enzymes of a typical mammalian gastrointestinal tract. However, the gastrointestinal tract of bat species should be adapted to their diet and be able to digest chitin. We hypothesized that (i) European vespertilionid bat species have the digestive enzyme chitinase and that (ii) the chitinolytic activity is located in the intestine, as has been found for North American bat species. The gastrointestinal tracts of seven bat species (Pipistrellus pipistrellus, Plecotus auritus, Myotis bechsteinii, Myotis nattereri, Myotis daubentonii, Myotis myotis, and Nyctalus leisleri) were tested for chitinolytic activity by diffusion assay. Gastrointestinal tracts of P. pipistrellus, P. auritus, M. nattereri, M. myotis, and N. leisleri were examined for acidic mammalian chitinase by western blot analysis. Tissue sections of the gastrointestinal tract of P. pipistrellus were immunohistochemically analyzed to locate the acidic mammalian chitinase. Chitinolytic activity was detected in the stomachs of all bat species. Western blot analysis confirmed the acidic mammalian chitinase in stomach samples. Immunohistochemistry of the P. pipistrellus gastrointestinal tract indicated that acidic mammalian chitinase is located in the stomach chief cells at the base of the gastric glands. In conclusion, European vespertilionid bat species have acidic mammalian chitinase that is produced in the gastric glands of the stomach. Therefore, the gastrointestinal tracts of insectivorous bat species evolved an enzymatic adaptation to their diet.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Exemplary gel plate for the measurement of the chitinolytic activity of the GI tract.
1– reference, 2– stomach, 3– duodenum, 4– jejunum/ileum, 5– ileum/colon samples of Plecotus auritus and 6– negative control.
Figure 2
Figure 2. Mean chitinolytic activity in the stomach samples of Pipistrellus pipistrellus at different pH values.
Curve fitted by distance-weighted least square smoothing procedure.
Figure 3
Figure 3. Exemplary western blot analysis of AMCase in the GI tract of Pipistrellus pipistrellus.
Individual 1: lane 1 =  stomach, lane 2 =  duodenum, lane 3 =  jejunum/ileum, lane 4 =  ileum/colon, lane 5 =  colon/rectum; individual 2: lane 6 =  stomach; lane 7 =  positive control (stomach sample of Mus musculus). The AMCase displayed a sharp band in the lane containing stomach proteins (46 k) except that lane 6 contained two distinct bands under 46 k probably caused by proteolytic digestion. Primary antibody dilution 1:1000.
Figure 4
Figure 4. Western blot analysis of AMCase in the stomachs of three different bat species.
Lane 1 =  Plecotus auritus, lane 2 =  Myotis myotis, lane 3 =  Nyctalus leisleri. Primary antibody dilution 1∶1000.
Figure 5
Figure 5. Immunohistochemical analysis of the stomach of Pipistrellus pipistrellus.
Picture overlay of labeling of the α-AMCase antibody (red); DAPI counterstained (blue) and phase contrast demonstrating positive labeling of the antibody at the bottom of the gastric glands. Bar  = 50 µm. G  =  gastric gland, M  =  mucosa, SubM  =  submucosa.

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Grant support

The authors have no support or funding to report.
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