The Intestinal Microbiota of Mastotermes darwiniensis

The lower wood-feeding termite Mastotermes darwiniensis Froggatt (Fig. 5.1.) is the only living member of the family Mastotermitidae. Today, this species is restricted to Northern Australia, but mastotermitid fossil specimen from the Eocene and Miocene have been found in Central America, the Caribic region, Europe, and Australia (Thorne et al. 2000). Termites are assigned to 13 families and 282 genera (Table 5.1; Myles 1999). Mastotermes darwiniensis is believed to be the most primitive existing termite species (Gay and Calaby 1970). Mastotermes darwiniensis developed a complex symbiotic hindgut flora, which consists of protozoa (formerly named Archaezoa; Cleveland and Grimstone 1964; Brugerolle et al. 1994; Berchtold and König 1995; Fröhlich and König 1999a,b), Bacteria (Berchtold and König 1996; Berchtold et al. 1999), Archaea (Fröhlich and König 1999a,b) and yeast (Prillinger et al. 1996; Schäfer et al. 1996). De-faunation experiments showed that the protozoa appeared to be essential for the termites survival (Veivers et al. 1983). In amber containing the Miocene termite Mastotermes electrodominicus, a 20-million-year-old fossil microbial community consisting of protists, spirochetes, and other bacteria has been observed (Wier et al. 2002).

Despite their small volumes of about 0.5-10 ^l, the hindguts of termites are morphologically complex systems. The digestive system of termites consists of the foregut with the crop and the gizzard, the midgut and the hindgut (Noi-rot and Noirot-Timothee 1969; Noirot 1995). The hindgut consists of five segments (P1-P5): the proctodeal segment, the enteric valve, the paunch, the colon and the rectum. The paunch is the microbial fermentation chamber, but the colon also contains microorganisms. Some higher termites possess a

Fig. 5.1. Colony of Mastotermes darwiniensis. Soldiers and workers are present

Table 5.1. Proposed taxonomy of the order Isoptera. (Myles 1999; number of genera and species in parenthesis)

LOWER TERMITES

Family: Termopsidae (rottenwood termites; 5, 20)

Family: Hodotermitidae (harvester termites; 3, 19)

Family Mastotermitidae (primitive termites; 1, 1)

Familiy: Kalotermitidae (dampwood and drywood termites; 22, 419)

Family: Rhinotermitidae (subterranean termites; 14, 343)

Family: Serritermitidae (1, 1)

HIGHER TERMITES Termitidae

Macrotermitinae (14, 349) Apicotermitinae (43, 202) Amitermitinae (17, 295) Nasutitermitinae (91, 663) Cubitermitinae (28, 161) Termitinae (43, 288)

prolonged mesenteron resulting in a transitional mixed segment between the midgut and hindgut. In the lower, phylogenetically most primitive termite, Mastotermes darwiniensis, P1 and P2 are very small. P3, the paunch, is subdivided into a dilated, thin-walled region (P3a) and a thick-walled, more tubular region (P3b), which is followed by a thick-walled, tubular colon (P4) and the rectum (P5) (Fig. 5.2).

P3a

P3b

MT

P1

P5

F

H

Fig. 5.2. Micrograph of the gut of Mastotermes darwiniensis. F foregut with salivary glands Mmidgut, H hindgut. MT malpighian tubules, P1 proctodeal segment, followed by the enteric valve (P1, not marked), P3a thin-walled part of the paunch, P3b thick-walled part of the paunch, P4 colon, P5 rectum. Graduation: mm

Fig. 5.2. Micrograph of the gut of Mastotermes darwiniensis. F foregut with salivary glands Mmidgut, H hindgut. MT malpighian tubules, P1 proctodeal segment, followed by the enteric valve (P1, not marked), P3a thin-walled part of the paunch, P3b thick-walled part of the paunch, P4 colon, P5 rectum. Graduation: mm

In the case of Mastotermes darwiniensis, oxygen diffusion gradients could be detected up to 100 ^m below the epithelium (Berchtold et al. 1999).

Combining the rRNA approach with confocal laser scanning microscopy and oxygen microelectrode measurements, the gut microbial community within the hindgut Mastotermes darwiniensis was examined (Berchtold et al. 1999; cf. König et al. 2002). The anterior part of the paunch (P3a region) of Mastotermes darwiniensis is tightly packed with large flagellates (1285 ± 244 cells of Deltotrichonympha operculata, Deltotrichonympha nana, Koruga bonita, and Mixotricha paradoxa per termite; Table 5.2) (Berchtold et al. 1999). From the combined volume of the larger flagellates it can be estimated that 95% of the anterior part of the paunch (P3a region) is occupied by flagellate protozoa. In Mastotermes darwiniensis, approximately 90% of the DAPI-stained cells were associated with the protozoa in the P3a region, only 2% were attached to the gut wall, and the rest were found in the residual liquid volume of the lumen fraction. In contrast, the flagellate population in the P3b/P4 region was much smaller. The flagellate cells represented only 10% of the total volume. The potentially colonizable surface area provided by the flagellates in the P3a region exceeds that of the wall by a factor of 18. In contrast to the P3a region, about 85% of the prokaryotes of the P3b region are attached to the wall. The prokaryotic cell density on the P3b/P4 epithelium (2*106 per mm2) is considerably higher than that on the P3a surface (3*104 per mm2). The concentration of non-attached cells in the residual volume is higher in the P3a region (7*109 cells per ml) than in the P3b/P4 region (1x109 cells per ml). The flagellates preferentially colonize the paunch, while low numbers are found in the colon (P4 region) (Berchtold et al. 1999).

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