Ancestral predisposition toward a domesticated lifestyle in the termite-cultivated fungus Termitomyces

Peppel, Lennart J.J. van de; Nieuwenhuis, Mathijs; Auxier, Ben; Grum-Grzhimaylo, Alexey A.; Cárdenas, Martha; Beer, Z. Wilhelm de; Lodge, D. Jean; Smith, Matthew E.; Kuyper, Thom W.; Franco-Molano, Ana E.; Baroni, Timothy J.; Aanen, Duur K.

doi:10.1016/j.cub.2021.07.070

Cited by 15 publications

(15 citation statements)

References 76 publications

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“…Compared to the gut bacteriome, the delayed acquisition of the fungal symbiont during the colony foundation seems to support the hypothesis of postdated emergence of the ancestor Macrotermitinae relative to the loss of protozoa. As suggested by Bucek et al (2019), fungus-growing termites may have emerged from a soil-feeding ancestor by reversion toward a wood feeding diet, fostered by the domestication of a saprobic fungus predisposed to trive in insect fecal substrate (van de Peppel et al, 2021).…”

Section: Frontiers In Ecology 12mentioning

confidence: 99%

Succession of the microbiota in the gut of reproductives of Macrotermes subhyalinus (Termitidae) at colony foundation gives insights into symbionts transmission

Diouf

Hervé²,

Fréchault³

et al. 2023

Front. Ecol. Evol.

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Termites have co-evolved with a complex gut microbiota consisting mostly of exclusive resident taxa, but key forces sustaining this exclusive partnership are still poorly understood. The potential for primary reproductives to vertically transmit their gut microbiota (mycobiome and bacteriome) to offspring was investigated using colony foundations from field-derived swarming alates of Macrotermes subhyalinus. Metabarcoding based on the fungal internal transcribed spacer (ITS) region and the bacterial 16S rRNA gene was used to characterize the reproductives mycobiome and bacteriome over the colony foundation time. The mycobiome of swarming alates differed from that of workers of Macrotermitinae and changed randomly within and between sampling time points, highlighting no close link with the gut habitat. The fungal ectosymbiont Termitomyces was lost early from the gut of reproductives, confirming the absence of vertical transmission to offspring. Unlike fungi, the bacteriome of alates mirrored that of workers of Macroterminae. Key genera and core OTUs inherited from the mother colony mostly persisted in the gut of reproductive until the emergence of workers, enabling their vertical transmission and explaining why they were found in offspring workers. These findings demonstrate that the parental transmission may greatly contribute to the maintenance of the bacteriome and its co-evolution with termite hosts at short time scales.

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Section: Frontiers In Ecology 12mentioning

confidence: 99%

Succession of the microbiota in the gut of reproductives of Macrotermes subhyalinus (Termitidae) at colony foundation gives insights into symbionts transmission

Diouf

Hervé²,

Fréchault³

et al. 2023

Front. Ecol. Evol.

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“…Macrotermitinae species termites cultivate basidiomycete fungi in the genus Termitomyces ( Agaricales : Lyophyllaceae ) in a cork-like structure known as fungus comb. As termitomycetoid fungal taxa present a reduced oligosaccharide-degrading enzymatic profile, the fungal metabolism is complimented with gut passages ( Rouland-Lefèvre, 2000 ; Poulsen et al, 2014 ; Li H. et al, 2017 ; van de Peppel et al, 2021 ). Such reduction in plant-degrading enzymes seems to precede domestication by termites and could have even facilitated this process.…”

Section: Plant-degrading Microbial Communities From Insect Fungiculturementioning

confidence: 99%

“…Such reduction in plant-degrading enzymes seems to precede domestication by termites and could have even facilitated this process. By targeting lignin and cellulose while stepping oligosaccharides aside, the Termitomyces ancestor could supposedly enrich the comb nutritional value, thus favoring the termites ( van de Peppel et al, 2021 ). Therefore, the nutritional role of the fungal crop could be considered as both indirect (by degrading lignin and providing easier access to cellulose and other plant components) and direct (by serving as a food source; Hyodo et al, 2003 ; Vesala et al, 2019 ).…”

Section: Plant-degrading Microbial Communities From Insect Fungiculturementioning

confidence: 99%

Lessons From Insect Fungiculture: From Microbial Ecology to Plastics Degradation

Barcoto

Rodrigues

2022

Front. Microbiol.

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Anthropogenic activities have extensively transformed the biosphere by extracting and disposing of resources, crossing boundaries of planetary threat while causing a global crisis of waste overload. Despite fundamental differences regarding structure and recalcitrance, lignocellulose and plastic polymers share physical-chemical properties to some extent, that include carbon skeletons with similar chemical bonds, hydrophobic properties, amorphous and crystalline regions. Microbial strategies for metabolizing recalcitrant polymers have been selected and optimized through evolution, thus understanding natural processes for lignocellulose modification could aid the challenge of dealing with the recalcitrant human-made polymers spread worldwide. We propose to look for inspiration in the charismatic fungal-growing insects to understand multipartite degradation of plant polymers. Independently evolved in diverse insect lineages, fungiculture embraces passive or active fungal cultivation for food, protection, and structural purposes. We consider there is much to learn from these symbioses, in special from the community-level degradation of recalcitrant biomass and defensive metabolites. Microbial plant-degrading systems at the core of insect fungicultures could be promising candidates for degrading synthetic plastics. Here, we first compare the degradation of lignocellulose and plastic polymers, with emphasis in the overlapping microbial players and enzymatic activities between these processes. Second, we review the literature on diverse insect fungiculture systems, focusing on features that, while supporting insects’ ecology and evolution, could also be applied in biotechnological processes. Third, taking lessons from these microbial communities, we suggest multidisciplinary strategies to identify microbial degraders, degrading enzymes and pathways, as well as microbial interactions and interdependencies. Spanning from multiomics to spectroscopy, microscopy, stable isotopes probing, enrichment microcosmos, and synthetic communities, these strategies would allow for a systemic understanding of the fungiculture ecology, driving to application possibilities. Detailing how the metabolic landscape is entangled to achieve ecological success could inspire sustainable efforts for mitigating the current environmental crisis.

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“…Fungus-farming termites (Macrotermitinae, Termitidae: Blattodea) engage in a symbiosis with a fungal cultivar (genus Termitomyces ; Agaricales: Lyophyllaceae) that they have co-evolved with since the origin of fungiculture 30 mya. 9–12 In addition, termite guts and fungus combs harbour diverse and co-adapted microbiomes that play roles in plant biomass decomposition and potentially prophylaxis. 13–16 Symbiont complementarity ensures near-complete plant biomass decomposition with contribution from the termite-nurtured fungal garden and gut microbiomes.…”

Section: Introductionmentioning

confidence: 99%

The chemical ecology of the fungus-farming termite symbiosis

et al. 2022

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Ancestral predisposition toward a domesticated lifestyle in the termite-cultivated fungus Termitomyces

Cited by 15 publications

References 76 publications

Succession of the microbiota in the gut of reproductives of Macrotermes subhyalinus (Termitidae) at colony foundation gives insights into symbionts transmission

Succession of the microbiota in the gut of reproductives of Macrotermes subhyalinus (Termitidae) at colony foundation gives insights into symbionts transmission

Lessons From Insect Fungiculture: From Microbial Ecology to Plastics Degradation

The chemical ecology of the fungus-farming termite symbiosis

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