Disease-free monoculture farming by fungus-growing termites

Saria Otani; Victoria L. Challinor; Nina B. Kreuzenbeck; Sara Kildgaard; Søren Krath Christensen; Louise Lee Munk Larsen; Duur K. Aanen; Silas Anselm Rasmussen; Christine Beemelmanns; Michael Poulsen

doi:10.1038/s41598-019-45364-z

Disease-free monoculture farming by fungus-growing termites

Saria Otani, Victoria L. Challinor, Nina B. Kreuzenbeck, Sara Kildgaard, Søren Krath Christensen, Louise Lee Munk Larsen, Duur K. Aanen, Silas Anselm Rasmussen, Christine Beemelmanns, Michael Poulsen^*

^*Corresponding author for this work

11 Citations (Scopus)

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Abstract

Fungus-growing termites engage in an obligate mutualistic relationship with Termitomyces fungi, which they maintain in monocultures on specialised fungus comb structures, without apparent problems with infectious diseases. While other fungi have been reported in the symbiosis, detailed comb fungal community analyses have been lacking. Here we use culture-dependent and -independent methods to characterise fungus comb mycobiotas from three fungus-growing termite species (two genera). Internal Transcribed Spacer (ITS) gene analyses using 454 pyrosequencing and Illumina MiSeq showed that non-Termitomyces fungi were essentially absent in fungus combs, and that Termitomyces fungal crops are maintained in monocultures as heterokaryons with two or three abundant ITS variants in a single fungal strain. To explore whether the essential absence of other fungi within fungus combs is potentially due to the production of antifungal metabolites by Termitomyces or comb bacteria, we performed in vitro assays and found that both Termitomyces and chemical extracts of fungus comb material can inhibit potential fungal antagonists. Chemical analyses of fungus comb material point to a highly complex metabolome, including compounds with the potential to play roles in mediating these contaminant-free farming conditions in the termite symbiosis.

Original language	English
Article number	8819
Journal	Scientific Reports
Volume	9
Pages (from-to)	1-10
ISSN	2045-2322
DOIs	https://doi.org/10.1038/s41598-019-45364-z
Publication status	Published - 2019

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title = "Disease-free monoculture farming by fungus-growing termites",

abstract = "Fungus-growing termites engage in an obligate mutualistic relationship with Termitomyces fungi, which they maintain in monocultures on specialised fungus comb structures, without apparent problems with infectious diseases. While other fungi have been reported in the symbiosis, detailed comb fungal community analyses have been lacking. Here we use culture-dependent and -independent methods to characterise fungus comb mycobiotas from three fungus-growing termite species (two genera). Internal Transcribed Spacer (ITS) gene analyses using 454 pyrosequencing and Illumina MiSeq showed that non-Termitomyces fungi were essentially absent in fungus combs, and that Termitomyces fungal crops are maintained in monocultures as heterokaryons with two or three abundant ITS variants in a single fungal strain. To explore whether the essential absence of other fungi within fungus combs is potentially due to the production of antifungal metabolites by Termitomyces or comb bacteria, we performed in vitro assays and found that both Termitomyces and chemical extracts of fungus comb material can inhibit potential fungal antagonists. Chemical analyses of fungus comb material point to a highly complex metabolome, including compounds with the potential to play roles in mediating these contaminant-free farming conditions in the termite symbiosis.",

author = "Saria Otani and Challinor, {Victoria L.} and Kreuzenbeck, {Nina B.} and Sara Kildgaard and Christensen, {S{\o}ren Krath} and Larsen, {Louise Lee Munk} and Aanen, {Duur K.} and Rasmussen, {Silas Anselm} and Christine Beemelmanns and Michael Poulsen",

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AU - Challinor, Victoria L.

AU - Kreuzenbeck, Nina B.

AU - Kildgaard, Sara

AU - Christensen, Søren Krath

AU - Larsen, Louise Lee Munk

AU - Aanen, Duur K.

AU - Rasmussen, Silas Anselm

AU - Beemelmanns, Christine

AU - Poulsen, Michael

PY - 2019

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N2 - Fungus-growing termites engage in an obligate mutualistic relationship with Termitomyces fungi, which they maintain in monocultures on specialised fungus comb structures, without apparent problems with infectious diseases. While other fungi have been reported in the symbiosis, detailed comb fungal community analyses have been lacking. Here we use culture-dependent and -independent methods to characterise fungus comb mycobiotas from three fungus-growing termite species (two genera). Internal Transcribed Spacer (ITS) gene analyses using 454 pyrosequencing and Illumina MiSeq showed that non-Termitomyces fungi were essentially absent in fungus combs, and that Termitomyces fungal crops are maintained in monocultures as heterokaryons with two or three abundant ITS variants in a single fungal strain. To explore whether the essential absence of other fungi within fungus combs is potentially due to the production of antifungal metabolites by Termitomyces or comb bacteria, we performed in vitro assays and found that both Termitomyces and chemical extracts of fungus comb material can inhibit potential fungal antagonists. Chemical analyses of fungus comb material point to a highly complex metabolome, including compounds with the potential to play roles in mediating these contaminant-free farming conditions in the termite symbiosis.

AB - Fungus-growing termites engage in an obligate mutualistic relationship with Termitomyces fungi, which they maintain in monocultures on specialised fungus comb structures, without apparent problems with infectious diseases. While other fungi have been reported in the symbiosis, detailed comb fungal community analyses have been lacking. Here we use culture-dependent and -independent methods to characterise fungus comb mycobiotas from three fungus-growing termite species (two genera). Internal Transcribed Spacer (ITS) gene analyses using 454 pyrosequencing and Illumina MiSeq showed that non-Termitomyces fungi were essentially absent in fungus combs, and that Termitomyces fungal crops are maintained in monocultures as heterokaryons with two or three abundant ITS variants in a single fungal strain. To explore whether the essential absence of other fungi within fungus combs is potentially due to the production of antifungal metabolites by Termitomyces or comb bacteria, we performed in vitro assays and found that both Termitomyces and chemical extracts of fungus comb material can inhibit potential fungal antagonists. Chemical analyses of fungus comb material point to a highly complex metabolome, including compounds with the potential to play roles in mediating these contaminant-free farming conditions in the termite symbiosis.

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DO - 10.1038/s41598-019-45364-z

M3 - Journal article

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VL - 9

SP - 1

EP - 10

JO - Scientific Reports

JF - Scientific Reports

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Disease-free monoculture farming by fungus-growing termites

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