Termite Gut Spirochetes
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CHAPTER 4.5 e t imreT
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Termite Gut Spirochetes JOHN A. BREZNAK AND JARED R. LEADBETTER
Introduction There are few habitats on earth in which spirochetes are such prominent members of the microbial community as in the hindgut of termites. This was first documented over a century ago by Joseph Leidy (Leidy, 1874–1881; Leidy, 1877), who was struck by their abundance in hindgut contents of the eastern subterranean termite, Termes (now Reticulitermes) flavipes. In some termites, spirochetes account for up to 50% of all prokaryotes in the hindgut (Paster et al., 1996), and even casual phase contrast microscopic observation of hindgut contents usually reveals about a dozen different morphological types, distinguishable on the bases of cell size, wavelength and amplitude, or pitch (Fig. 1). Their size range is striking: from cells measuring only 0.1 mm in diameter ¥ 2.5 mm in length (i.e., at or near the limit of resolution of light microscopy) to many as large as 1.5 mm ¥ 100 mm (Hollande and Gharagozlou, 1967; Bermudes et al., 1988; Paster et al., 1996). Thus, it is not surprising that termites were long ago recommended as an excellent source of spirochetes (and other diverse pro- and eukaryotic microbes) for classroom demonstrations (Beckwith and Light, 1927). Electron microscopy has revealed additional intriguing morphological features of some of the spirochetes, including the presence of crenulations (folds) and a sillon (deep groove) in the outer membrane, bundles of periplasmic flagella, cytoplasmic tubules, and tube-like polar appendages (Bermudes et al., 1988; Radek et al., 1992). Spirochetes are also fairly abundant in hindguts of Cryptocercus punctulatus (Grimstone, 1963; Wier et al., 2000), a wood-eating cockroach that, by most analyses, is closely related to termites phylogenetically (Nalepa and Bandi, 2000). However, not much work has been done on spirochetes of C. punctulatus, perhaps owing to the somewhat limited distribution of this insect (Cleveland et al., 1934). In hindgut contents, spirochetes occur as individual, free-swimming cells within the gut fluid.
In so-called “lower termites” (families Kalotermitidae, Mastotermitidae, Rhinotermitidae, Serritermitidae and Termopsidae), they also occur as epibionts attached end-on to the plasma membrane of flagellate protozoa, which are also abundant in such termites. Depending on the particular protozoan, the attached spirochetes may be uniformly distributed over the surface or localized in specific regions (Kirby, 1941; Ball, 1969; Radek et al., 1992; Radek et al., 1996; Rö sel et al., 1996). Attachment appears to be facilitated by a structural modification of the protozoan plasma membrane and/or the end of the spirochetal cell (Cleveland and Grimstone, 1964; Bloodgood et al., 1974; Smith and Arnott, 1974; Smith et al., 1975a; Smith et al., 1975b; Bloodgood and Fitzharris, 1976; Radek et al., 1992; Radek et al., 1996). A spectacular consequence of such attachment is seen for Mixotricha paradoxa, a protozoan whose locomotion is conferred by a ves
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