Host Susceptibility Modulates Escovopsis Pathogenic Potential in the Fungiculture of Higher Attine Ants

Irina Jiménez-Gómez,Andre Rodrigues,Quimi V Montoya,Aryel C Goes,Mariana O Barcoto,Lana S V E Monteiro,Odair C Bueno

doi:10.3389/fmicb.2021.673444

Irina Jiménez-Gómez, Andre Rodrigues + Show 5 more

Open Access

https://doi.org/10.3389/fmicb.2021.673444

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Abstract

Health and disease emerge from intricate interactions between genotypes, phenotypes, and environmental features. The outcomes of such interactions are context-dependent, existing as a dynamic continuum ranging from benefits to damage. In host-microbial interactions, both the host and environmental conditions modulate the pathogenic potential of a microorganism. Microbial interactions are the core of the agricultural systems of ants in the subtribe Attina, which cultivate basidiomycete fungi for food. The fungiculture environment harbors a diverse microbial community, including fungi in the genus Escovopsis that has been studied as damage-causing agent. Here, we consider the ant colony as a host and investigate to what extent its health impacts the dynamics and outcomes of host-Escovopsis interactions. We found that different ant fungal cultivars vary in susceptibility to the same Escovopsis strains in plate-assays interactions. In subcolony-Escovopsis interactions, while healthy subcolonies gradually recover from infection with different concentrations of Escovopsis conidia, insecticide-treated subcolonies evidenced traits of infection and died within 7 days. The opportunistic nature of Escovopsis infections indicates that diseases in attine fungiculture are a consequence of host susceptibility, rather than the effect of a single microbial agent. By addressing the host susceptibility as a major modulator of Escovopsis pathogenesis, our findings expand the understanding of disease dynamics within attine colonies.

Highlights

Dynamics in microbial interactions derive from trade-offs between the interacting organisms, modulated by diverse environmental variables (Gonze et al, 2018)
Both fungal cultivars had their mycelial growth inhibited in the presence of all the 21 Escovopsis strains in comparison to the control (t test, p < 0.05; Figure 1A; Supplementary Tables 1, 2)
MT was significantly inhibited by seven Escovopsis strains after the first day in dual-culture (Supplementary Table 1), while L. gongylophorus AS inhibition was observed after 2 days (Supplementary Table 2)

Summary

Introduction

Dynamics in microbial interactions derive from trade-offs between the interacting organisms, modulated by diverse environmental variables (Gonze et al, 2018). Outcomes that emerge from interacting genotypes, phenotypes, and environmental conditions, exist as a dynamic continuum (Méthot and Alizon, 2014) This includes benefits, damage, or be neutral to the interacting organisms, resulting in ecological states of mutualism, commensalism, colonization, Host Susceptibility Modulates Escovopsis Pathogenesis and disease (Frey-Klett et al, 2011; Casadevall and Pirofski, 2015). Susceptibility refers to environmental attributes within and outside the host that favor the establishment, development, and maturation of a pathogen (Wakelin, 1978; Méthot and Alizon, 2014; Casadevall and Pirofski, 2018) These variables include host genetics, health status, and microbiome, as well as climatic conditions and chance of being infected (Casadevall and Pirofski, 2018). While a tolerant host might employ mechanisms to improve its own health to tolerate the infection (without interfering directly with the pathogen), a resistant host might directly target the pathogen and its derived toxins (Vale et al, 2014)

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