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

The ancestor of termites relied on gut symbionts for degradation of plant material, an association that persists in all termite families. However, the single-lineage Macrotermitinae has additionally acquired a fungal symbiont that complements digestion of food outside the termite gut. Phylogenetic analysis has shown that fungi grown by these termites forma clade—the genus Termitomyces—but the events leading toward domestication remain unclear. To address this, we reconstructed the lifestyle of the common ancestor of Termitomyces using a combination of ecological data with a phylogenomic analysis of 21 related non-domesticated species and 25 species of Termitomyces. We show that the closely related genera Blastosporella and Arthromyces also contain insect-associated species. Furthermore, the genus Arthromyces produces asexual spores on the mycelium, which may facilitate insect dispersal when growing on aggregated subterranean fecal pellets of a plant-feeding insect. The sister-group relationship between Arthromyces and Termitomyces implies that insect association and asexual sporulation, present in both genera, preceded the domestication of Termitomyces and did not follow domestication as has been proposed previously. Specialization of the common ancestor of these two genera on an insect-fecal substrate is further supported by similar carbohydrate-degrading profiles between Arthromyces and Termitomyces. We describe a set of traits that may have predisposed the ancestor of Termitomyces toward domestication, with each trait found scattered in related taxa outside of the termite-domesticated clade. This pattern indicates that the origin of the termite-fungus symbiosis may not have required large-scale changes of the fungal partner.http://www.cell.com/current-biology/homeam2022BiochemistryForestry and Agricultural Biotechnology Institute (FABI)GeneticsMicrobiology and Plant Patholog

High diversity and low host-specificity of Termitomyces symbionts cultivated by Microtermes spp. indicate frequent symbiont exchange

Fungus-growing termites (subfamily Macrotermitinae) live in an obligate mutualistic symbiosis with species of the fungal genus Termitomyces (Basidiomycota). Although the species that build large mounds are the most conspicuous, termites of the genus Microtermes construct large underground networks of tunnels connecting many fungus gardens. They are also the only entire genus within the Macrotermitinae in which vertical transmission of the fungal symbiont has evolved. To study patterns of genetic diversity in species of the genus Microtermes and their Termitomyces symbionts, we sampled at three different locations in South Africa and sequenced COI for the termites and ITS for the fungi. We discovered high genetic diversity in both termites and fungal symbionts but very low interaction specificity. This implies that frequent horizontal exchange of fungal symbionts occurs between species, despite vertical transmission across generations. We also estimated colony size based on termite haplotype and fungal genotype combinations and found indications that colonies may extend over large areas.</p

Evolution : Ant trail pheromones promote ant-aphid mutualisms

A new study shows that trail pheromones produced by an invasive ant species suppress the dispersal and stimulate the reproduction of cotton aphids that the ants can 'milk' for honeydew. Aphids use these pheromones as a signal of ant presence and respond adaptively, analogous to early stages of animal husbandry where animals were attracted to human settlements

Termitomyces cryptogamus sp. nov. associated with Macrotermes natalensis in Africa

A new species of Termitomyces symbiotic with the termite Macrotermes natalensis is described from Africa. As there are no records of field collected basidiocarps within this lineage, traditional basidiocarp-based morphological taxonomy is not practical. While basidiocarps may be obtained rarely from incubation of fungal comb fragments, their practical use for taxonomical purposes is limited. Therefore, the species is described based on an ITS nucleotide sequence, with comparisons to an asexual culture. Based on samples with similar ITS sequences, this species is likely associated with multiple termite hosts across a large part of Africa

Enrichment of G4DNA and a Large Inverted Repeat Coincide in the Mitochondrial Genomes of Termitomyces

Mitochondria retain their own genome, a hallmark of their bacterial ancestry. Mitochondrial genomes (mtDNA) are highly diverse in size, shape, and structure, despite their conserved function across most eukaryotes. Exploring extreme cases of mtDNA architecture can yield important information on fundamental aspects of genome biology. We discovered that the mitochondrial genomes of a basidiomycete fungus (Termitomyces spp.) contain an inverted repeat (IR), a duplicated region half the size of the complete genome. In addition, we found an abundance of sequences capable of forming G-quadruplexes (G4DNA); structures that can disrupt the double helical formation of DNA. G4DNA is implicated in replication fork stalling, double-stranded breaks, altered gene expression, recombination, and other effects. To determine whether this occurrence of IR and G4DNA was correlated within the genus Termitomyces, we reconstructed the mitochondrial genomes of 11 additional species including representatives of several closely related genera. We show that the mtDNA of all sampled species of Termitomyces and its sister group, represented by the species Tephrocybe rancida and Blastosporella zonata, are characterized by a large IR and enrichment of G4DNA. To determine whether high mitochondrial G4DNA content is common in fungi, we conducted the first broad survey of G4DNA content in fungal mtDNA, revealing it to be a highly variable trait. The results of this study provide important direction for future research on the function and evolution of G4DNA and organellar IRs.</p

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

The ancestor of termites relied on gut symbionts for degradation of plant material, an association that persists in all termite families.1,2 However, the single-lineage Macrotermitinae has additionally acquired a fungal symbiont that complements digestion of food outside the termite gut.3 Phylogenetic analysis has shown that fungi grown by these termites form a clade-the genus Termitomyces-but the events leading toward domestication remain unclear.4 To address this, we reconstructed the lifestyle of the common ancestor of Termitomyces using a combination of ecological data with a phylogenomic analysis of 21 related non-domesticated species and 25 species of Termitomyces. We show that the closely related genera Blastosporella and Arthromyces also contain insect-associated species. Furthermore, the genus Arthromyces produces asexual spores on the mycelium, which may facilitate insect dispersal when growing on aggregated subterranean fecal pellets of a plant-feeding insect. The sister-group relationship between Arthromyces and Termitomyces implies that insect association and asexual sporulation, present in both genera, preceded the domestication of Termitomyces and did not follow domestication as has been proposed previously. Specialization of the common ancestor of these two genera on an insect-fecal substrate is further supported by similar carbohydrate-degrading profiles between Arthromyces and Termitomyces. We describe a set of traits that may have predisposed the ancestor of Termitomyces toward domestication, with each trait found scattered in related taxa outside of the termite-domesticated clade. This pattern indicates that the origin of the termite-fungus symbiosis may not have required large-scale changes of the fungal partner

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

The ancestor of termites relied on gut symbionts for degradation of plant material, an association that persists in all termite families.1,2 However, the single-lineage Macrotermitinae has additionally acquired a fungal symbiont that complements digestion of food outside the termite gut.3 Phylogenetic analysis has shown that fungi grown by these termites form a clade—the genus Termitomyces—but the events leading toward domestication remain unclear.4 To address this, we reconstructed the lifestyle of the common ancestor of Termitomyces using a combination of ecological data with a phylogenomic analysis of 21 related non-domesticated species and 25 species of Termitomyces. We show that the closely related genera Blastosporella and Arthromyces also contain insect-associated species. Furthermore, the genus Arthromyces produces asexual spores on the mycelium, which may facilitate insect dispersal when growing on aggregated subterranean fecal pellets of a plant-feeding insect. The sister-group relationship between Arthromyces and Termitomyces implies that insect association and asexual sporulation, present in both genera, preceded the domestication of Termitomyces and did not follow domestication as has been proposed previously. Specialization of the common ancestor of these two genera on an insect-fecal substrate is further supported by similar carbohydrate-degrading profiles between Arthromyces and Termitomyces. We describe a set of traits that may have predisposed the ancestor of Termitomyces toward domestication, with each trait found scattered in related taxa outside of the termite-domesticated clade. This pattern indicates that the origin of the termite-fungus symbiosis may not have required large-scale changes of the fungal partner