Role of the mutualistic fungus in lignin degradation in the fungus-growing termite Macrotermes gilvus (Isoptera; Macrotermitinae)

Hyodo, Fujio; Inoue, Tsuneo; Azuma, Junpei; Tayasu, Ichiro; Abe, Takuya

doi:10.1016/s0038-0717(99)00192-3

Cited by 82 publications

(51 citation statements)

References 18 publications

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“…(15,16,21), but its functional role in ligninolysis remains unclear and controversial (22). In addition to genetic and biochemical research approaches, several solid-state NMR studies have shown different peak intensities assigned to lignin structures between spectra of the fresh comb and mature comb (23,24). Although these findings suggest that lignin degradation occurs within the fungus comb, these earlier experiments characterized comb samples from field colonies, with a potentially wide variety of plant debris collected by the termites, making it difficult to match the chemical compositional and structural changes occurring along with the plant substrate processing within these systems (25,26).…”

Section: Significancementioning

confidence: 99%

Lignocellulose pretreatment in a fungus-cultivating termite

Yelle

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

106

102

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Depolymerizing lignin, the complex phenolic polymer fortifying plant cell walls, is an essential but challenging starting point for the lignocellulosics industries. The variety of ether-and carbon-carbon interunit linkages produced via radical coupling during lignification limit chemical and biological depolymerization efficiency. In an ancient fungus-cultivating termite system, we reveal unprecedentedly rapid lignin depolymerization and degradation by combining laboratory feeding experiments, lignocellulosic compositional measurements, electron microscopy, 2D-NMR, and thermochemolysis. In a gut transit time of under 3.5 h, in young worker termites, poplar lignin sidechains are extensively cleaved and the polymer is significantly depleted, leaving a residue almost completely devoid of various condensed units that are traditionally recognized to be the most recalcitrant. Subsequently, the fungus-comb microbiome preferentially uses xylose and cleaves polysaccharides, thus facilitating final utilization of easily digestible oligosaccharides by old worker termites. This complementary symbiotic pretreatment process in the fungus-growing termite symbiosis reveals a previously unappreciated natural system for efficient lignocellulose degradation.ignin is a heterogeneous plant cell wall polymer derived primarily from hydroxycinnamyl alcohols via combinatorial radical coupling reactions (1). Its depolymerization is challenging, making lignin a major barrier to gaining access to stored energy within lignocellulosic materials (2). Woody biomass, such as that contained in pine and poplar trees, represents the most abundant renewable energy resource in our terrestrial ecosystems. Because of a high content of lignin, a complex polymer that contains ether-and carbon-carbon linkages between monomerderived units (1, 3), biotechnological efforts to use this material for bioenergy require expensive chemical, physical, or biological pretreatment processes to partially delignify lignocellulose to allow access to plant polysaccharides (2).Termites are remarkably efficient at degrading woody biomass (4). Within hours, they digest 74-99% of cellulose and 65-87% of hemicellulose, leaving the lignin-rich residues as feces; that is, they process far more efficiently than other herbivores that can digest the less-lignified forages, such as grasses, leaves, and forest litter (5). Among termites, the subfamily Macrotermitinae form a monophyletic group of diverse species that originated in Africa and have cultivated specialized fungi (Termitomyces spp.) in their nests using woody or litter-based biomass for about 31 million years, and are able to almost completely decompose lignocellulose (6, 7). These termites enable the consumption of more than 90% of dead plant tissues in some arid tropical areas (7,8), and thus play central ecological roles in Old World (sub)tropical carbon cycling ( Fig. 1 A and B) (8). Throughout their evolutionary history, fungus-cultivating termites have evolved in mutualistic association with multiple microbial symbi...

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Section: Significancementioning

confidence: 99%

Lignocellulose pretreatment in a fungus-cultivating termite

Yelle

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

106

102

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“…These insects transfer and inoculate fungi on plant substrates, and feed on fungi or their decomposition products (Batra and Batra 1979; Haack and Slansky 1987;Paine et al 1997). Most of these insects, i.e., termites, bark/ ambrosia beetles, and wood wasps, feed on dead plant tissue and are considered dependent on symbiotic fungi for the decomposition of lignin and cellulose (Morgan 1968; Barras and Hodges 1969;Martin and Martin 1978;Bridges 1983;Kukor and Martin 1983;Madden 1988;Watanabe et al 1998;Hyodo et al 2000), which are the main components of plants, but are indigestible by most insect herbivores (Talmadge et al 1973;Abe and Higashi 1991;Martin 1991;Hochuli 1996;Schoonhoven et al 1997). Therefore, insects feeding on nutrient-poor plant tissue gain more nutrients by feeding on fungi inoculated on the tissue or their decomposition products than by feeding on the plant tissue directly.…”

Section: Introductionmentioning

confidence: 99%

Contribution of symbiotic mycangial fungi to larval nutrition of a leaf-rolling weevil

et al. 2007

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Some phytophagous insects have been known to inoculate certain fungi on plant substrates. In many cases of such insect-fungi relationships it has been considered that fungi contribute to insects by decomposing lignin or polysaccharides, and that the insects feed on the decomposition products or fungi themselves. Females of the leaf-rolling weevil in the genus Euops (Attelabidae) store spores of symbiotic fungi in the mycangia and inoculate them on leaf rolls. To determine the effect of mycangial fungi on larval nutrition in E. lespedezae, the nutritional value was compared between leaves with and without mycangial fungi. Two Penicillium species were isolated from the mycangia. These mycangial fungi showed little effect on the decomposition of lignin and polysaccharides, and showed little effect on enhancement of soluble sugars within leaves. Thus, the mutualism between Euops and its mycangial fungi contrasts with the mainly nutritional mutualisms between wood-infesting insects (termites, bark/ambrosia beetles, and wood wasps) and lignin/polysaccharide-decomposing fungi.

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“…The full significance of the fungus in termite nutrition is still debated (Bignell 2000), but it may have some benefits: the fungal symbiont degrades complex substances (such as lignin or cellulose) into substances that can be used by termites (Wood and Thomas 1989;Hyodo et al 2000).…”

Section: Introductionmentioning

confidence: 99%

The first fossil fungus gardens of Isoptera: oldest evidence of symbiotic termite fungiculture (Miocene, Chad basin)

Duringer

Schuster

Genise

et al. 2006

Naturwissenschaften

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Higher termites of the subfamily Macrotermitinae (fungus-growing termites) are known to build fungus gardens where a symbiotic fungus (Termitomyces sp.) is cultivated. The fungus grows on a substrate called fungus comb, a structure built with the termites' own faeces. Here we present the first fossil fungus combs ever found in the world. They were extracted from 7-million-year-old continental sandstone (Chad basin). Fossilized fungus combs have an ovoid morphology with a more or less flattened concave base and a characteristic general alveolar aspect. Under lens, they display a typical millimetre-scale pelletal structure. The latter, as well as the general shape and alveolar aspect, are similar to the morphology of fungus combs from extant fungus-growing termites.

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Role of the mutualistic fungus in lignin degradation in the fungus-growing termite Macrotermes gilvus (Isoptera; Macrotermitinae)

Cited by 82 publications

References 18 publications

Lignocellulose pretreatment in a fungus-cultivating termite

Lignocellulose pretreatment in a fungus-cultivating termite

Contribution of symbiotic mycangial fungi to larval nutrition of a leaf-rolling weevil

The first fossil fungus gardens of Isoptera: oldest evidence of symbiotic termite fungiculture (Miocene, Chad basin)

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