The Role of Symbionts in the Evolution of Termites and Their Rise to Ecological Dominance in the Tropics

Bignell, David E.

doi:10.1007/978-3-319-28068-4_6

Cited by 24 publications

(36 citation statements)

References 155 publications

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“…from several Macrotermitinae termite hosts apparently lack typical ligninolytic agents, such as lignin peroxidase (LiP), manganese peroxidase (MnP), and versatile peroxidase (VP), that are found in, for example, white-rot fungi (8,15,16). Research on these enzymes shows that lignin depolymerization may occur via many mechanisms: (i) LiPs and VPs are known to efficiently oxidize nonphenolic β-ether units in lignin within the wood cell wall-beyond where enzymes are permitted to travel-via single electron transfer, creating aryl cation radical intermediates and cleaving the β-ether unit between its Cα and Cβ carbons (17,18); (ii) MnPs preferentially oxidize Mn 2+ to the reactive Mn 3+ which, in its chelated form, can act as a diffusible redox mediator and attack phenolic structures in lignin (19); (iii) unsaturated fatty acids undergo peroxidation by MnP to form organoperoxyl radicals that have also been shown to be potential ligninolytic agents if able to diffuse into the wood cell wall (20).…”

Section: Significancementioning

confidence: 99%

“…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). The way Macrotermitinae termites and symbiotic microbiota circumvent the lignin barrier and cleave the polysaccharide into easily digestible simple sugars has therefore remained a mystery (8,27).…”

Section: Significancementioning

confidence: 99%

“…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).…”

mentioning

confidence: 99%

“…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 symbionts, not only with the lignocellulose-digesting basidiomycete fungi Termitomyces spp., but also with gut microbiota and the bacterial community associated with their fungus comb (8,9).…”

mentioning

confidence: 99%

“…1 A and B) (8). Throughout their evolutionary history, fungus-cultivating termites have evolved in mutualistic association with multiple microbial symbionts, not only with the lignocellulose-digesting basidiomycete fungi Termitomyces spp., but also with gut microbiota and the bacterial community associated with their fungus comb (8,9). The Macrotermitinae termite-fungus-bacterial symbiosis is a system that enables the extensive conversion of plant materials (9,10).…”

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confidence: 99%

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Lignocellulose pretreatment in a fungus-cultivating termite

Yelle

et al. 2017

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

110

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%

Section: Significancementioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Lignocellulose pretreatment in a fungus-cultivating termite

Yelle

et al. 2017

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

110

102

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Colony‐age‐dependent variation in cuticular hydrocarbon profiles in subterranean termite colonies

Gordon

Šobotník²,

Chouvenc

2020

Ecology and Evolution

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Cuticular hydrocarbons (CHCs) have, in insects, important physiological and ecological functions, such as protection against desiccation and as semiochemicals in social taxa, including termites. CHCs are, in termites, known to vary qualitatively and/or quantitatively among species, populations, castes, or seasons. Changes to hydrocarbon profile composition have been linked to varying degrees of aggression between termite colonies, although the variability of results among studies suggests that additional factors might have been involved. One source of such variability may be colony age, as termite colony demographics significantly change over time, with different caste and instar compositions throughout the life of the colony. We here hypothesize that the intracolonial chemical profile heterogeneity would be high in incipient termite colonies but would homogenize over time as a colony ages and accumulates older workers in improved homeostatic conditions. We studied caste‐specific patterns of CHC profiles in Coptotermes gestroi colonies of four different age classes (6, 18, 30, and 42 months). The CHC profiles were variable among castes in the youngest colonies, but progressively converged toward a colony‐wide homogenized chemical profile. Young colonies had a less‐defined CHC identity, which implies a potentially high acceptance threshold for non‐nestmates conspecifics in young colonies. Our results also suggest that there was no selective pressure for an early‐defined colony CHC profile to evolve in termites, potentially allowing an incipient colony to merge nonagonistically with another conspecific incipient colony, with both colonies indirectly and passively avoiding mutual destruction as a result.

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Wood-Feeding Termites

Bignell

2018

Saproxylic Insects

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The Role of Symbionts in the Evolution of Termites and Their Rise to Ecological Dominance in the Tropics

Cited by 24 publications

References 155 publications

Lignocellulose pretreatment in a fungus-cultivating termite

Lignocellulose pretreatment in a fungus-cultivating termite

Colony‐age‐dependent variation in cuticular hydrocarbon profiles in subterranean termite colonies

Wood-Feeding Termites

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