The fungus-growing termite Macrotermes natalensis harbors bacillaene-producing Bacillus sp. that inhibit potentially antagonistic fungi

Soohyun Um,Antoine Fraimout,Michael Poulsen,Panagiotis Sapountzis,Dong-Chan Oh

doi:10.1038/srep03250

Abstract

The ancient fungus-growing termite (Mactrotermitinae) symbiosis involves the obligate association between a lineage of higher termites and basidiomycete Termitomyces cultivar fungi. Our investigation of the fungus-growing termite Macrotermes natalensis shows that Bacillus strains from M. natalensis colonies produce a single major antibiotic, bacillaene A (1), which selectively inhibits known and putatively antagonistic fungi of Termitomyces. Comparative analyses of the genomes of symbiotic Bacillus strains revealed that they are phylogenetically closely related to Bacillus subtilis, their genomes have high homology with more than 90% of ORFs being 100% identical, and the sequence identities across the biosynthetic gene cluster for bacillaene are higher between termite-associated strains than to the cluster previously reported in B. subtilis. Our findings suggest that this lineage of antibiotic-producing Bacillus may be a defensive symbiont involved in the protection of the fungus-growing termite cultivar.

Highlights

The ancient fungus-growing termite (Mactrotermitinae) symbiosis involves the obligate association between a lineage of higher termites and basidiomycete Termitomyces cultivar fungi
Comparative analyses of the genomes of symbiotic Bacillus strains revealed that they are phylogenetically closely related to Bacillus subtilis, their genomes have high homology with more than 90% of ORFs being 100% identical, and the sequence identities across the biosynthetic gene cluster for bacillaene are higher between termite-associated strains than to the cluster previously reported in B. subtilis
Through bioassay-guided chemical analyses of Bacillus strains isolated from different colonies of Macrotermes natalensis, we show that termiteassociated Bacillus strains produce a single major compound, bacillaene (1), which selectively inhibits known (Pseudoxylaria and Trichoderma) and potentially competitive or antagonistic (Coriolopsis, Umbelopsis and Fusarium) fungi that had been obtained in culture from M. natalensis colonies and, may represent potential competitors or antagonists of Termitomyces

Summary

Introduction

The ancient fungus-growing termite (Mactrotermitinae) symbiosis involves the obligate association between a lineage of higher termites and basidiomycete Termitomyces cultivar fungi. Our investigation of the fungus-growing termite Macrotermes natalensis shows that Bacillus strains from M. natalensis colonies produce a single major antibiotic, bacillaene A (1), which selectively inhibits known and putatively antagonistic fungi of Termitomyces. B eneficial symbiotic associations between prokaryotes and eukaryotes are widespread in nature[1] Such mutualistic relationships include defensive symbioses, which often involve selective antibiotics produced by prokaryotes against host antagonists[2,3]. The fungus is housed on a special substrate (fungus comb) in the nest, which is maintained by the termites through the continuous addition of partially digested plant material that has passed through the termite gut along with asexual Termitomyces spores[16,17] (Fig. 1b). Obligate gut passage of the substrate prior to incorporation in the fungus comb may aid this, because this mode of substrate incorporation may allow for the selective inhibition of antagonists before entry to the fungus comb[17]

Methods

Results

Conclusion