Hindgut Microbes

The guts of all cockroach species examined house a diverse anaerobic microbiota, with ciliates, amoebae, flagellates, and a heterogeneous prokaryotic assemblage, including spirochetes (Kidder, 1937; Steinhaus, 1946; Guthrie and Tindall, 1968; Bracke et al., 1979; Bignell, 1981; Cruden and Markovetz, 1984; Sanchez et al., 1994; Zurek and Keddie, 1996; Lilburn et al., 2001). Methano-genic bacteria, a good indicator of microbial fermentative activity (Cazemier et al., 1997b), are found both free in the gut lumen and in symbiotic association with ciliates and mastigotes in most cockroach species tested (Bracke et al., 1979; Gijzen and Barugahare, 1992; Hackstein and Strumm, 1994). Nyctotherus (Fig. 5.1) can host more than 4000 methanogens per cell (Hackstein and Strumm, 1994), and hundreds to thousands of the ciliate can be found in full-grown cockroaches (van Hoek et al., 1998). Microbes are densely packed within the gut, but in a predictable spatial arrangement; food is processed sequentially by specific microbial groups as it makes its way through the digestive system. Volatile fatty acids (VFAs) are present in the hindgut, further suggesting the degradation of cellulose and other plant polysaccharides (Bracke and Markovetz, 1980). The hindgut wall of cockroaches is permeable to organic acids (Bignell, 1980; Bracke and Markovetz, 1980; Maddrell and Gardiner, 1980), indicating that the host may directly benefit from the products of microbial fermentation. Long cuticular spines and extensive infolding of the hindgut wall increase surface area and provide points of attachment for the microbes (Bignell, 1980; Cruden and Markovetz, 1987; Cazemier et al., 1997a). Finally, redox potentials indicate conditions are more reducing than in other insect species, with the exception of termites (Bignell, 1984). These features of cockroach digestive physiology support the notion that plant structural polymers play a significant role in the nutritional ecology of Blattaria; however, we currently lack enough information to appreciate fully the subtleties of the interactions in the hindgut. It is known to be a fairly open system, with a core group of mutualists,together with a "floating"pool of microbes recruited from those entering with food material (Bignell, 1977b, pers. comm. to CAN). Populations of the microbial community shift dynamically in relation to the food choices of the host. Whatever rotting substrate is ingested, a suite of microbes responds and proliferates (Gijzen et al., 1991,1994; Kane and Breznak, 1991; Zurek and Keddie, 1998; Feinberg et al., 1999).

Cellulases are distributed throughout the cockroach

Fig 5.1 Scanning electron micrograph of the ciliate Nycto-therus ovalis from the hindgut of Periplaneta americana. Scale bar = 20 ^m. From van Hoek et al. (1998); photo courtesy of J. Hackstein, with permission of the journal Molecular Biology and Evolution.

digestive system, and these enzymes are both endogenous and microbial in origin (Wharton and Wharton, 1965; Wharton et al., 1965; Bignell, 1977a; Cruden and Mar-kovetz, 1979; Gijzen et al., 1994; Scrivener and Slaytor, 1994b). The nature of the contribution of cellulose to cockroach nutritional ecology, however, has been difficult to determine; in most cases no obvious nutritional benefit can be detected (Bignell, 1976, 1978), even in some wood-feeding cockroaches. Zhang et al. (1993), for example, found that Geoscapheus dilatatus, which feeds on dead, dry leaves, was able to utilize cellulose and hemicel-lulose more efficiently than the wood-feeding species Panesthia cribrata. The latter was surprisingly inefficient in extracting both cellulose (15%) and hemicellulose (3%) from its diet. In omnivorous domestic species, cellulose digestion may be a backup strategy, to be used when other available foods are inadequate ( Jones and Raubenheimer, 2001). This is supported by evidence that solids are retained longer in the gut of starving Periplaneta americana (Bignell, 1981), allowing more time for processing the less digestible components. Retention time in animals with hindgut fermentation is directly related to digestive assimilation and efficiency (Dow, 1986; van Soest, 1994). The fact that so many cockroaches feed on cellulose-based substrates in the field but there is so little evidence for it playing a significant metabolic role suggests another possible function: the breakdown of cellulose may primarily provide energy for bacterial metabolism (Slaytor, 1992,2000). Fibrous materials, then, may be ingested because they serve as fuel for microbial growth on the ingested substrate, on feces, and in the gut, and it is the microbes and their products that are of primary nutritive importance to the cockroach (Nalepa et al., 2001a).

Ontogeny of Microbial Dependence

Although it is often tacitly assumed that hosts derive net advantage from their mutualists throughout their life-cycle, in a number of associations it is only at key stages in the host lifecycle that exploitation of symbionts is important (Smith, 1992; Bronstein, 1994). Regardless of the exact nature of the benefits, young cockroaches depend more than older stages on gut microbiota. If the hind-gut anaerobic community is eliminated, adequately fed adults are not affected. The overall growth of juvenile hosts, however, is impeded, and results in extended developmental periods. The weight of antibiotic-treated P. americana differed by 33% from controls at 60 days of age. Defaunation also lowered methane production and VFA concentrations within the hindgut, and the gut itself became atrophied (Bracke et al., 1978; Cruden and Markovetz, 1987; Gijzen and Barugahare, 1992; Zurek and Keddie, 1996).

The nutritional requisites of young cockroaches also differ from those of adults (P. americana), and are reflected in the activities of hindgut anaerobic bacteria, including methanogens (Kane and Breznak, 1991; Gijzen and Barugahare, 1992; Zurek and Keddie, 1996). Juvenile P. americana produce significantly more methane than adults, particularly when on high-fiber diets (Kane and Breznak, 1991), and demonstrable differences occur in the proportions of VFAs in the guts of adults versus juvenile stages (Blaberus discoidalis) fed on the same dog food diet (McFarlane and Alli, 1985).

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