You don\u2019t have the guts: a diverse set of fungi survive passage through Macrotermes bellicosus termite guts

N.’golo Abdoulaye Koné,Nick Bos,Michael Poulsen,Leandro Guimaraes,Simon Kolotchèlèma Silue,Lorrie Maccario,Justinn Renelies-Hamilton,Romen Palenzuela

doi:10.1186/s12862-020-01727-z

N.’golo Abdoulaye Koné, Nick Bos

Open Access

https://doi.org/10.1186/s12862-020-01727-z

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Abstract

BackgroundMonoculture farming poses significant disease challenges, but fungus-farming termites are able to successfully keep their monoculture crop free from contamination by other fungi. It has been hypothesised that obligate gut passage of all plant substrate used to manure the fungal symbiont is key to accomplish this. Here we refute this hypothesis in the fungus-farming termite species Macrotermes bellicosus.ResultsWe first used ITS amplicon sequencing to show that plant substrate foraged on by termite workers harbour diverse fungal communities, which potentially could challenge the farming symbiosis. Subsequently, we cultivated fungi from dissected sections of termite guts to show that fungal diversity does not decrease during gut passage. Therefore, we investigated if healthy combs harboured these undesirable fungal genera, and whether the presence of workers affected fungal diversity within combs. Removal of workers led to a surge in fungal diversity in combs, implying that termite defences must be responsible for the near-complete absence of other fungi in functioning termite gardens.ConclusionsThe rapid proliferation of some of these fungi when colonies are compromised indicates that some antagonists successfully employ a sit-and-wait strategy that allows them to remain dormant until conditions are favourable. Although this strategy requires potentially many years of waiting, it prevents these fungi from engaging in an evolutionary arms race with the termite host, which employs a series of complementary behavioural and chemical defences that may prove insurmountable.

Highlights

Monoculture farming poses significant disease challenges, but fungus-farming termites are able to successfully keep their monoculture crop free from contamination by other fungi
We restrict our main text presentation of results to M. bellicosus, but show results for all species in Additional file 1: Table S2 and Additional file 2: Figure S2. 1,403,519 clean reads were used to assess worker impact on fungus comb health. Sequences from both experiments were assigned to 1,970 unique Amplicon Sequence Variants (ASVs), of which 96.4% were identified to phylum, 94.9% to class, 93.0% to order, 89.5% to family and 86.2% to genus level
Our findings strongly suggest that this is not the case: substrates harbour a high diversity of fungi, and we find no evidence that fungal diversity decreases as we move from the middle to the latter section of the gut

Summary

Introduction

Monoculture farming poses significant disease challenges, but fungus-farming termites are able to successfully keep their monoculture crop free from contamination by other fungi. Monoculture farming predictably increases risks of epidemic infections [1, 2], while high genetic diversity buffers resistance against disease [3] This ‘monoculture effect’ is well-documented in human agriculture [4] and in leaf-cutting ant monocultures, where specialized and potentially virulent fungal pathogens tend to invade the fungal cultivar [5,6,7]. The manuring of fungus combs is through a strict process, where older workers forage on decaying plant biomass outside the nest, which is passed on to younger workers within the nest, who ingest it along with asexual Termitomyces spores in a ‘first gut passage’ [15, 16]. This gut passage is rapid and serves to efficiently mix Termitomyces spores with the macerated substrate, and this mix is deposited as fresh fungus comb [15], on which Termitomyces grows to decompose the plant substrate, produce mycelium and new asexual spores

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