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Escovopsioides As a Fungal Antagonist of the Fungus Cultivated by Leafcutter Ants Julio Flavio Osti1 and Andre Rodrigues1,2*

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Escovopsioides As a Fungal Antagonist of the Fungus Cultivated by Leafcutter Ants Julio Flavio Osti1 and Andre Rodrigues1,2* Osti and Rodrigues BMC Microbiology (2018) 18:130 https://doi.org/10.1186/s12866-018-1265-x RESEARCHARTICLE Open Access Escovopsioides as a fungal antagonist of the fungus cultivated by leafcutter ants Julio Flavio Osti1 and Andre Rodrigues1,2* Abstract Background: Fungus gardens of fungus-growing (attine) ants harbor complex microbiomes in addition to the mutualistic fungus they cultivate for food. Fungi in the genus Escovopsioides were recently described as members of this microbiome but their role in the ant-fungus symbiosis is poorly known. In this study, we assessed the phylogenetic diversity of 21 Escovopsioides isolates obtained from fungus gardens of leafcutter ants (genera Atta and Acromyrmex) and non-leafcutter ants (genera Trachymyrmex and Apterostigma) sampled from several regions in Brazil. Results: Regardless of the sample locality or ant genera, phylogenetic analysis showed low genetic diversity among the 20 Escovopsisoides isolates examined, which prompted the identification as Escovopsioides nivea (the only described species in the genus). In contrast, one Escovopsioides isolate obtained from a fungus garden of Apterostigma megacephala was considered a new phylogenetic species. Dual-culture plate assays showed that Escovopsioides isolates inhibited the mycelium growth of Leucoagaricus gongylophorus, the mutualistic fungus cultivated by somes species of leafcutter ants. In addition, Escovopsioides growth experiments in fungus gardens with and without ant workers showed this fungus is detrimental to the ant-fungus symbiosis. Conclusions: Here, we provide clues for the antagonism of Escovopsioides towards the mutualistic fungus of leafcutter ants. Keywords: Hypocreales, Attine ants, Escovopsis,Symbiosis Background garden. In fact, a diverse and rich microbial community Fungus-growing ants in the tribe Attini are found only on consisting of bacteria, yeasts, and filamentous fungi are also the American continent [1]. These insects cultivate fungi as found in this substrate [5–7]. Some of these microorgan- the main food source for the colony [2]. As a subgroup isms can compete for nutrients with the mutualistic fungus within the higher attines, leafcutter ants in the genera Atta [8], others act as parasites of the fungal cultivar [9]. In and Acromyrmex use fresh leaves and flowers as substrate addition, there are beneficial microbes in the fungus gar- to nourish the fungus cultivar. Leafcutter ants cultivate two dens, which may help the mutualistic fungus against patho- phylogenetic clades of fungi including Leucoagaricus gongy- gens [10]. Actinobacteria present on the workers’ cuticles lophorus (Basidiomycota: Agaricales) [3]. In turn, the fungal also assist in the protection of the colony against invading partner is cultivated on fragments of plant substrate proc- microorganisms [11–13]. essed by the ants in a structure named “fungus garden” [2]. Currie and colleagues [14] showed that fungi in the genus Due to the high amount of leaves that leafcutter ants col- Escovopsis (Ascomycota: Hypocreales) cause negative im- lect, these insects are considered agricultural pests, causing pacts on attine ant colonies. Multiple lines of evidence sug- serious damage to several crops [4]. gest that Escovopsis is a specialized parasite of the ant Contrary to what was proposed by Weber [2], L. gongylo- cultivar, using both chemical and physical mechanisms to phorus is not the only active microorganism in the fungus attack its host [9, 15, 16]. Escovopsis shares an ancient evo- lutionary history with the mutualistic fungus and the ants, * Correspondence: [email protected] indicating that the origin of this parasite occurred concomi- 1Department of Biochemistry and Microbiology, São Paulo State University tantly with the beginning of the ant-fungus association, (UNESP), Rio Claro, Brazil about 50–65 million years ago [17]. 2Center for the Studies of Social Insects, São Paulo State University (UNESP), Rio Claro, Brazil © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Osti and Rodrigues BMC Microbiology (2018) 18:130 Page 2 of 11 Recently, fungi in the genus Escovopsioides (Ascomy- Acromyrmex, Trachymyrmex and Apterostigma)andposed cota: Hypocreales) were described from fungus gardens the following questions: (i) given that Escovopsioides was de- of the leafcutter ants Acromyrmex niger, Acromyrmex scribed from fungus gardens of Acromyrmex spp., do isolates subterraneus molestans and Acromyrmex subterraneus of this fungus found on colonies of other genera of attine subterraneus [18]. Also, this fungus was found in 24% to ants form a monophyletic clade?, (ii) are Escovopsioides from 72% of the sampled colonies in different localities in different associated attine ant species antagonists of the L. Brazil [18–20]. Escovopsioides shares some morpho- gongylophorus and the fungus gardens?, and (iii) is Escovop- logical characteristics with Escovopsis but differ in others sioides capable to overcome the protective roles of the ant such as terminal vesicles with long (lageniform) phialides workers? We show that Escovopsioides associated with a and hyphae with aleuroconidia. Molecular analysis indi- wide range of ant species from various geographical areas cates that Escovopsioides is phylogenetically related to belong to the same species (E. nivea). Our results also sup- Escovopsis [18]. The discovery of this fungus launched port previous findings [16] of the antagonism of this fungus new research windows on the attine ant-fungus symbiosis. towards the mutualistic cultivar of leafcutter ants. First, nothing is known about the diversity and taxonomy of Escovopsioides. So far, only one species (E. nivea) has Results been described from a very narrow geographical range Escovopsioides phylogeny (“Mata do Paraíso”, Viçosa, state of Minas Gerais, Brazil); Our analysis resolved a single, well-supported monophyletic however, it is likely that other species in the genus still clade of Escovopsiodes, with one isolate falling just outside of await discovery. Second, if Escovopsioides is an antagonist this clade, namely isolate Escovopsioides sp. LESF 602 (Fig. 1). of the mutualistic fungus as suggested by Varanda-Haifig We observed low genetic diversity in the main clade, com- et al. [16], new opportunities will rise to study the dynam- prising isolates associated with the higher-attine ant genera ics of the evolution of additional detrimental fungi to the Atta, Acromyrmex and Trachymyrmex along with the type fungus gardens of attine ants. Third, it is not clear whether species, E. nivea CBS 135749T. A low intraspecific variation Escovopsioides can cause detrimental effects to fungus (99.1 to 100% similarity) among Escovopsioides isolates of gardens of attine ants, or whether the ant workers protect higher-attines was observed in the tef1 marker. Interesting the fungus gardens against Escovopsioides. to note, the genetic similarity in the tef1 gene was observed We obtained several Escovopsioides isolates from fungus for isolates from distant geographic regions, since Escovop- gardens of different associated attine ant genera (Atta, sioides isolates obtained from colonies separated by large Fig. 1 Phylogeny of Escovopsioides isolates obtained from fungus-growing ants. The tree was reconstructed under Bayesian Inference (BI) using concatenated sequences of tef1 and LSU genes as well as ITS. Sequences of type strains of Escovopsis spp. (represented by T) and additional hypocrealean fungi (outgroup) were retrieved from GenBank (Additional file 1: Table S1). Values on branches are posterior probabilities. The entire alignment is composed of 2112 bp in length. The substituion models GTR + G for tef1 and GTR + I + G for ITS and LSU were used in the BI analysis. Escovopsioides species are indicated by LESF Ids and associated ant species are indicated in parentheses. All other sequences are followed by the culture collection accessions Osti and Rodrigues BMC Microbiology (2018) 18:130 Page 3 of 11 distances were similar, such as Rio Grande do Sul and Bahia the inhibition of the mutualistic fungus (Fig. 2). Isolates states (Fig. 1). The low intraspecific variation was also ob- LESF 596 and LESF 602, obtained from Acromyrmex sp. served in the ITS region (99.4 to 100% of similarity). The and A. megacephala, respectively, comprise a group of LSU sequences were identical among 20 out of 21 se- fungi that significantly inhibited the growth of the mutualis- quences. On the other hand, Escovopsioides sp. LESF 602 tic fungus at day 10, but to a lesser extent when compared obtained from fungus gardens of Apterostigma megacephala to the remaining isolates (Tukey-HSD, P < 0.003, Fig. 2). presented similarity between 90 to 91% in relation to the Escovopsis showed the highest inhibiton of the mutualistic other isolates considering the marker tef1; 91% to 92% for fungus (Tukey-HSD, P < 0.001, Fig. 2). ITS and 98% of similarity for LSU. This isolate stands out in the phylogeny as a separate branch and indicates a not
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