The inoculation of newly formed fungus comb withTermitomyces inMacrotermes colonies (Isoptera, Macrotermitinae)

Leuthold, R. H.; Badertscher, S.; Imboden, Hans

doi:10.1007/bf02224884

Cited by 77 publications

(83 citation statements)

References 12 publications

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“…Indeed, both our NMR and thermochemolysis data compellingly reveal that the rapid first gut passage through young workers considerably depolymerizes and degrades lignin. Far beyond the young termite's traditionally held role to simply mix asexual spores and lignocellulosic substrates (11,28), these observations align with previous studies, providing evidence that lower termites (nonfungus-cultivating species) enable lignin sidechain oxidation (37,44). After the first gut-passage step, the lignin degradation products in the woody residue are continuously cleaved/removed by the fungus-comb microbiome.…”

Section: Confirmation Of Lignin Depolymerization and Degradation By Psupporting

confidence: 84%

Lignocellulose pretreatment in a fungus-cultivating termite

Yelle

et al. 2017

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

114

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: Confirmation Of Lignin Depolymerization and Degradation By Psupporting

confidence: 84%

Lignocellulose pretreatment in a fungus-cultivating termite

Yelle

et al. 2017

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

114

102

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“…In Macrotermes species, the fungus comb is managed in a highly structured way, with older workers collecting crude forage material and bringing it back to the nest, where younger workers ingest it together with asexual Termitomyces spores (conidia) provided by fungal nodules from established "fungus-garden combs" to produce primary feces that is deposited as new layers of comb (17,20) (Fig. 1C).…”

Section: Significancementioning

confidence: 99%

“…1C). This new substrate quickly develops dense hyphal networks and produces the next cohorts of nodules (2,20), whereas older termites ultimately consume the old comb (Fig. 1C).…”

Section: Significancementioning

confidence: 99%

Complementary symbiont contributions to plant decomposition in a fungus-farming termite

Poulsen

et al. 2014

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

247

351

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Termites normally rely on gut symbionts to decompose organic matter but the Macrotermitinae domesticated Termitomyces fungi to produce their own food. This transition was accompanied by a shift in the composition of the gut microbiota, but the complementary roles of these bacteria in the symbiosis have remained enigmatic. We obtained high-quality annotated draft genomes of the termite Macrotermes natalensis, its Termitomyces symbiont, and gut metagenomes from workers, soldiers, and a queen. We show that members from 111 of the 128 known glycoside hydrolase families are represented in the symbiosis, that Termitomyces has the genomic capacity to handle complex carbohydrates, and that worker gut microbes primarily contribute enzymes for final digestion of oligosaccharides. This apparent division of labor is consistent with the Macrotermes gut microbes being most important during the second passage of comb material through the termite gut, after a first gut passage where the crude plant substrate is inoculated with Termitomyces asexual spores so that initial fungal growth and polysaccharide decomposition can proceed with high efficiency. Complex conversion of biomass in termite mounds thus appears to be mainly accomplished by complementary cooperation between a domesticated fungal monoculture and a specialized bacterial community. In sharp contrast, the gut microbiota of the queen had highly reduced plant decomposition potential, suggesting that mature reproductives digest fungal material provided by workers rather than plant substrate.carbohydrate-active enzymes | eusocial | symbioses | cellulose | lignin

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“…New colonies of fungus-growing termites are usually initiated by a pair of alates that become king and queen of the society. Some termite species show a vertical symbiont transmission, meaning that reproductives carry asexual spores of the symbionts from their parental nest with them (Grassé and Noirot, 1958;Johnson et al, 1981;Leuthold et al, 1989). However, in most fungus-growing termite species, new colonies acquire their symbiotic fungal partners via horizontal transmission.…”

Section: Introductionmentioning

confidence: 99%

Environmental and biological determinants of Termitomyces species seasonal fructification in central and southern Côte d’Ivoire

et al. 2011

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The Macrotermitinae subfamily is characterized by its symbiosis with fungi of the genus Termitomyces. The most common and presumably primitive mode of reproduction for these fungi is to produce basidiocarps on the mounds of the host termite colony. The seasonal fructification pattern of the fungi seems to depend on the habitat type and termite ecology. We examined Termitomyces diversity and distribution in two phytogeographic zones in central and southern Côte d'Ivoire. Data were collected in different habitats in exhaustive searches with standardized methods for termites and basidiocarps as well. The respective findings were complemented with behavioral and life cycle data of the associated termite species. Basidiocarps occur speciesspecifically either during the long or the short rainy season in wooded habitats. The diversity and abundance of termites and their associated basidiocarps were significantly correlated only with woody plant species richness. Nuptial flight of termites, comb biomass and Termitomyces fructification periods were correlated. Termitomyces appear to fructify during (1) the period of strong precipitation, (2) in habitats with appropriate microclimatic characteristics.

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The inoculation of newly formed fungus comb withTermitomyces inMacrotermes colonies (Isoptera, Macrotermitinae)

Cited by 77 publications

References 12 publications

Lignocellulose pretreatment in a fungus-cultivating termite

Lignocellulose pretreatment in a fungus-cultivating termite

Complementary symbiont contributions to plant decomposition in a fungus-farming termite

Environmental and biological determinants of Termitomyces species seasonal fructification in central and southern Côte d’Ivoire

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