Symbiotic Associations Between Termites and Prokaryotes
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Symbiotic Associations Between Termites and Prokaryotes ANDREAS BRUNE
Introduction
Symbiotic Digestion
The symbiotic associations of termites with microorganisms comprise different levels of interaction, ranging from the extracorporal cultivation of fungus gardens to the most intimate associations, where bacteria reside intracellularly in dedicated bacteriocytes. However, the majority of prokaryotic symbionts of termites are located in the intestinal tract, where they are free-swimming, attached to the gut epithelium, or associated with the intestinal protozoa (Fig. 1). Although it is suggestive that the gut microbiota of termites is directly or indirectly involved in the digestion of lignocellulose or has other nutritional implications, the exact nature of the associations and possible benefits for the partners of each particular symbiosis are often far from clear. Therefore, this chapter will use the term “symbiosis” in its broader sense, as originally defined by Anton de Bary (de Bary, 1878). A definitive classification of the associations into the different categories of symbiosis, such as mutualism, parasitism, or commensalism, would require a level of understanding that is yet to be reached. In view of the enormous body of literature on the intestinal microbiota of termites and its role in lignocellulose digestion, the subject cannot be covered exhaustively. This chapter will attempt to summarize the current state of knowledge on the prokaryotic communities within the intestinal tracts of termites, the major populations and their metabolic activities, and their interactions. In addition, it will focus on the gut as a microbial habitat. The chapter will touch only briefly on the intestinal flagellates, which are most important in the phylogenetically lower termites, the exosymbiotic fungi in fungus-cultivating Macrotermitinae, and the intracellular bacteria in termite tissues. For details on these subjects and for many other aspects of the termite gut symbiosis, the reader will be referred to the pertinent review articles.
Termites, like other insects thriving on a lignocellulosic diet, possess a pronounced gut microbiota housed in specially adapted regions of the alimentary tract (Fig. 2). The symbionts convert a substantial portion of the dietary components to microbial fermentation products, which are then eventually resorbed by the intestinal epithelia. It is generally assumed that the intestinal symbioses provide metabolic capacities that are otherwise not available to the host. For reviews, see Breznak and Brune (1994b), Kane (1997), Brune (1998), Brune (2003), Bignell (2000), Breznak (2000), Brune and Friedrich (2000a), and Ohkuma (2003). The symbiotic digestion of lignocellulose by termites is a complex series of events involving both the host and its gut microbiota (Fig. 3). While the events in the foregut and midgut seem to be mainly due to host activities, the digestive processes in the hindgut are largely controlled by the
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