Lignin degradation in wood-feeding insects

Abstract

The aromatic polymer lignin protects plants from most forms of microbial attack. Despite the fact that a significant fraction of all lignocellulose degraded passes through arthropod guts, the fate of lignin in these systems is not known. Using tetramethylammonium hydroxide thermochemolysis, we show lignin degradation by two insect species, the Asian longhorned beetle (Anoplophora glabripennis) and the Pacific dampwood termite (Zootermopsis angusticollis). In both the beetle and termite, significant levels of propyl side-chain oxidation (depolymerization) and demethylation of ring methoxyl groups is detected; for the termite, ring hydroxylation is also observed. In addition, culture-independent fungal gut community analysis of A. glabripennis identified a single species of fungus in the Fusarium solani/Nectria haematococca species complex. This is a soft-rot fungus that may be contributing to wood degradation. These results transform our understanding of lignin degradation by wood-feeding insects.Asian longhorned beetle ͉ Pacific dampwood termite ͉ TMAH thermochemolysis ͉ Anoplophora glabripennis ͉ Zootermopsis angusticollis L ignin plays a central role in carbon cycling on Earth. Its heterogeneous structure imparts plants with structural rigidity and also serves to protect cellulose and hemicellulose from degradation (1). Most of what is known about lignin biodegradation is from pure culture studies with filamentous basidiomycete fungi, known as white-rot and brown-rot decay. Although both white-rot and brown-rot fungal degradation have been characterized, much more is known about the white-rot system (2, 3). White-rot fungi simultaneously degrade the three major components of the plant cell wall: lignin, cellulose, and hemicellulose. Analysis of white-rot-degraded wood shows that the reactions in lignin: (i) are oxidative, (ii) involve demethylation (or demethoxylation), (iii) include side-chain oxidation at C ␣ , and (iv) involve propyl side-chain cleavage between C ␣ and C ␤ (Fig. 1) (4). In contrast to white-rot fungi, brown-rot fungi are able to circumvent the lignin barrier, removing the hemicellulose and cellulose with only minor modification to the lignin. Consequently, lignin remains a major component of the degraded plant cell wall (5). The remaining lignin is demethylated on aryl methoxy groups and contains a greater number of ring hydroxyl groups (6).Little is known about lignin degradation in complex ecosystems, such as insect guts, where a consortium of microbes may be involved in degradation rather than just a single species. Although cellulose degradation in insect guts is well documented (7,8), the fate of lignin has not clearly been demonstrated (9, 10), and it is widely accepted that insect gut systems do not have the capacity to degrade lignin (10). Although the majority of previous reports suggest that many wood-feeding insects overcome the lignin barrier by feeding on predegraded wood (11) or through exosymbiotic relationships with wood-degrading fungi (12, 13), there are species of insects...

Molecular insight into lignocellulose digestion by a marine isopod in the absence of gut microbes

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Symbiosis as a General Principle in Eukaryotic Evolution

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Temperate forest termites: ecology, biogeography, and ecosystem impacts

“…In contrast, efforts to quantify the abundances, regional distributions, and ecosystem effects of temperate forest termites are confounded by their largely subterranean nature and cryptic behavioural traits (Nutting & Jones, 1990;DeHeer & Vargo, 2004). As with tropical and savanna termites, temperate termites emit methane, fix nitrogen, modify soil properties, and alter forest structure and corresponding animal habitat availability by reducing the amount of standing and lying dead wood (Breznak et al, 1973;Holt & Lepage, 2000;Geib et al, 2008;Brune, 2010;Peterson, 2010;Evans, 2011;Jouquet et al, 2011). The few existing estimates of the ecosystem impacts of temperate forest termites are based almost solely on extrapolations from studies in tropical, subtropical, and savanna ecosystems (e.g., Brian, 1978;Abe et al, 2000), or through scaling up the effects of a few temperate termite species at local spatial scales (e.g.…”