The Distribution and Diversity of Euryarchaeota in Termite Guts

https://doi.org/10.1016/S0065-2164(07)62003-6Get rights and content

Publisher Summary

The Euryarchaeota are a critical component of all termite guts, acting as hydrogen sinks in both lower and higher termites. In lower termites and in the wood- and fungus-feeding higher termites, the role of the methanogens appears to be to mop up trace hydrogen. In the soil-feeding higher termites, methanogenesis lies at the heart of termite nutrition and represents an essential gut process. New analyses of termite evolution suggest that the evolution of the higher termites probably occurred via an externalization of the gut in the fungus-feeding Macrotermitinae followed by the evolution of soil-feeding. It is plausible that a first step in this process would have been the acquisition of a Methanomicrobiales strain that had the potential to reduce hydrogen partial pressures to levels that allowed the effective exploitation of soil organic matter.

Introduction

Termites are the dominant invertebrates in tropical ecosystems (Collins 1983, Eggleton 1996, Wood 1978, Wood 1982). Through their consumption and digestion of plant‐derived material, they have a major influence on soil structure, plant decomposition, carbon mineralization, and nutrient availability (Bignell 2000, Lavelle 1997, Lee 1971, Lobry de Bruyn 1990, Wood 1986). Studying their ecology and physiology, including the role of symbiotic microbes, is a vital to understanding their role in the global ecosystem.

Termites are divided into two major groupings: the lower and higher termites (Abe 2000, Inward 2007). The lower termites, which presently consist of six families that all feed on wood or grass, are characterized by relatively simple gut structures and the presence of flagellated protists in their guts. In contrast, the higher termites consist of a single family, the Termitidae, which includes ∼70% of all known termite species and are far more abundant than lower termites. Higher termites feed on a wide range of plant material at different stages of decomposition from sound wood to soil (Donovan 2001, Eggleton 2001). The majority of higher termite species feed on highly humified plant material in soil and are especially diverse and abundant in tropical forest soils (Davies et al., 2003).

Digestion in termites is closely related to gut structure, the physicochemical conditions in different gut regions, and symbiotic microbiota found in their guts (Brauman 2000, Breznak 2000, Kane 2002). In particular, methanogenic archaea (methanogens) have been detected in all termite guts that have been studied. The degree to which gut prokaryotes vary between termites is far from clear, but differences in host diet have been correlated with differences in how the microbial community processes hydrogen produced during the fermentation of organic matter. In anaerobic gut regions of both lower and higher termites that feed on wood, bacterial acetogenesis outcompetes methanogenesis for hydrogen, whereas the reverse is true in the guts of soil‐feeders (Bignell 1997, Brauman 1992, Tholen 1999). In fact the archaeal community in termite guts plays a part not just in termite metabolism but also may have had a role in the evolution and diversification of termites and their ecological success in tropical ecosystems.

Section snippets

Euryarchaeota in Termite Guts

The presence of Euryarchaeota, and specifically methanogens, in termites from all seven families and all feeding guilds is intriguing. This is especially true as some wood‐feeding termites emit little or no methane (Brauman et al., 1992) while in soil‐feeding termites methanogenesis can represent as much as 10% of the termite's respiratory effort (Tholen and Brune, 1999). This difference between feeding guilds has led to an effort to understand the community structure and role of methanogens in

Detection of Euryarchaeota in Termite Guts

A number of studies have investigated Euryarchaeota in termite guts, although, to date, there has been no systematic sampling across the termite phylogenetic tree. These studies have identified a range of different methanogens and these are presented in a schematic tree in Fig. 3.3. All of the published data is presented in Table 3.1 and is organized with reference to phylogenetically supported clades shown in Fig. 3.3.

What is clear from this data is that a considerable diversity of

Why Are There Different Euryarchaeota in Different Termites?

The data that presently exists on the distribution and diversity of Euryarchaeota in termite guts is striking, especially as the greatest difference appears to be between wood‐ and soil‐feeding termites. The limited studies that have been performed on wood‐feeding termites indicate a euryarchaeal community dominated by Methanobrevibacter, while a much more diverse euryarchaeal community is present in soil‐feeding termites. If we assume this difference is real rather than a product of poor taxon

Conclusion

The Euryarchaeota are a critical component of all termite guts, acting as hydrogen sinks in both lower and higher termites. In lower termites and in the wood‐ and fungus‐feeding higher termites, the role of the methanogens appears to be to mop up trace hydrogen. In the soil‐feeding higher termites, methanogenesis lies at the heart of termite nutrition and represents an essential gut process. New analyses of termite evolution suggest that the evolution of the higher termites probably occurred

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