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Inhibition of Symbiote Fungus of the Leaf Cutter Ant Atta

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Inhibition of Symbiote Fungus of the Leaf Cutter Ant Atta AGRICULTURAL MICROBIOLOGY / SCIENTIFIC COMMUNICATION DOI: 10.1590/1808‑1657000172018 Inhibition of symbiote fungus of the leaf cutter ant Atta sexdens by secondary metabolites from the bacterium Xenorhabdus szentirmaii associated with entomopathogenic nematodes Inibição do fungo simbionte da formiga-cortadeira Atta sexdens por metabólitos secundários da bactéria Xenorhabdus szentirmaii associada a nematoides entomopatogênicos Julie Giovanna Chacon Orozco1 , Luis Garrigós Leite1, Bruna Cristina Custódio2 , Raphael Satochi Abe da Silva1, Ana Gabriele Barbosa Casteliani1, Raphael Vacchi Travaglini3* ABSTRACT: Leaf-cutter ants (Hymenoptera: Formicidae) RESUMO: As formigas-cortadeiras (Hymenoptera: Formicidae) evo- have evolved as dominant herbivores on the American continent. luíram estabelecendo-se no continente americano como herbívoros These social insects remove the leaves of economically important dominantes. Esses insetos sociais praticam a desfolha de espécies vege- plant species to maintain their colony’s food reserves, the tais de interesse econômico, com a finalidade de manter a reserva ali- symbiotic fungus Leucocoprinus gongylophorus, a basidiomycete. mentar da colônia, o fungo simbionte Leucocoprinus gongylophorus, Such fungus can be used for applications of fungicide molecules um basidiomiceto. Tal fungo pode ser alvo de aplicações de moléculas from metabolites generated by symbiont bacteria (Xenorhabdus and fungicidas encontradas em metabólitos gerados por bactérias simbion- Photorhabdus) from entomopathogenic nematodes (Steinernema tes (Xenorhabdus e Photorhabdus) de nematoides entomopatogênicos and Heterorhabditis). Through isolation and multiplication in (Steinernema e Heterorhabditis). Por meio do isolamento e da multipli- tryptic soy broth (TSB) medium of the bacteria Xenorhabdus cação em meio caldo triptona de soja (TSB) da bactéria Xenorhabdus szentirmaii isolated PAM 25, we conducted laboratorial tests using szentirmaii (isolado PAM 25), foram realizados testes laboratoriais com treatments with 10, 25, and 50% of the metabolites obtained in tratamentos contendo 10, 25 e 50% do metabólito obtido no sexto dia the sixth day of cultivation. The treatments were centrifuged and de cultivo. Para tanto, o metabólito foi centrifugado e filtrado, gerando filtered to generate a supernatant, which was diluted in potato + um sobrenadante, o qual foi diluído em batata + dextrose + ágar (BDA), dextrose + agar (PDA), to verify the consequences of exposure para verificar as consequências da exposição do fungo L. gongylophorus to the fungus L. gongylophorus in Petri dishes. To confirm em placas de Petri. Os tratamentos de controle apenas com meio BDA metabolite efficiency, the control treatments in PDA only and e misto (BDA + TSB) também foram conduzidos simultaneamente mixed (PDA+TSB) media were conducted simultaneously for por 14 dias, a fim de confirmar a eficiência dos metabólitos. Tanto na 14 days. We observed total inhibition of the symbiont fungus in diluição de 25 e 50% houve total inibição do fungo simbionte já nos both the 25 and 50% dilutions during the first days of the tests. primeiros dias da condução dos testes. Diante dos resultados obtidos, Our results support that these metabolites have inhibitory effect pode-se afirmar que os metabólitos são a causa do efeito inibitório do on the development of symbiont fungus of leaf-cutter ants. desenvolvimento do fungo simbionte das formigas-cortadeiras. KEYWORDS: alternative control; Leucocoprinus gongylophorus; PALAVRAS-CHAVE: controle alternativo; Leucocoprinus entomopathogenic nematodes. gongylophorus; nematoides entomopatogênicos. 1Centro Experimental Central do Instituto Biológico – Campinas (SP), Brazil 2Universidade Estadual Paulista “Júlio de Mesquita Filho” – Rio Claro (SP), Brazil 3Universidade Estadual Paulista “Júlio de Mesquita Filho” – Botucatu (SP), Brazil *Corresponding author: [email protected] Received on: 02/08/2018. Accepted on: 08/03/2018 Arq. Inst. Biol., v.85, 1-6, e0172018, 2018 1 J. Chacon-Orozco et al. Nature presents a variety of organisms that are detrimental to incorporated into the fungal garden by the colony’s garden human agriculture. Chemical pesticides have been widely used operators, and maintains the food reserve (WEBER, 1972). to control such pests, however these pesticides damage the envi- Structured by the queen shortly after the nuptial flight, ronment. To avoid the problems caused by chemical pest control, the colony of Atta leaf-cutter ants originates from the queen’s one alternative is the development of efficient biological control claustral phase in the ground, when she solitarily maintains methods. This phenomenon, also known as biocontrol, involves a fragment of the symbiotic fungus (L. gongylophorus) from other living organisms to control specific populations, which her previous colony matrix (WHEELER, 1906). After lay- are considered plagues. For this, natural enemies are expected ing the first eggs, the first workers emerge and mature, and to be efficient, as they evolved interacting with the target organ- help expand the chambers that act as the garbage and fungal ism and, to some extent, are able to overcome the organism’s garden for the colony (DELLA LUCIA, 2011). defenses (FOLGARAIT et al., 2011). Furthermore, the use of Entomopathogenic fungi are the most commonly studied microorganisms in biological control has been widely encour- and are used as natural sources of insecticides (TRAVAGLINI, aged, as they are easily cultivated and manipulated. 2017). However, several species of entomopathogenic nematodes Controls that use synthetic chemicals in their formula- (NEPs) can be used in pest control, classified in two genera: tions have been increasingly criticized (GILLJAM et al., 2016), Heterorhabditis and Steinernema (ALMENARA et al., 2012). since they lead to the accumulation of persistent waste in the Entomopathogenic bacteria associated with the NEPs present environment. Therefore, society pressures researchers to find an extensive repertoire of genes involved in the production of methods for managing agricultural pests in a more sustainable toxins and secondary metabolites (MS). These molecules are and harmonious way within agroecosystems. Currently, the thought to be responsible for ensuring the pathogenic pro- most widespread method for controlling leaf-cutter ants is cess for the insect and invasion inside the host’s body, as well through attractive granular baits (BRITTO et al., 2016). as the maintenance of symbiosis with nematodes (CLARKE, The use of liquid insecticides, powder insecticides, or those 2008). Recent studies have shown that phytopathogenic fungi applied by thermal foggers are already considered obsolete. (Alternaria, Botrytis, Cochliobolus, Fusarium, Geotrichum, Organic producers lack viable options for controlling leaf- Penicillium, Sclerotina and Phytophthora) damage agriculture cutter ants, since the Agricultural and Food Inspections and (DONG et al., 2006) and are inhibited by metabolites pro- Certifications (Inspeções e Certificações Agropecuárias e duced by bacteria associated with NEPs (FANG et al., 2014; Alimentícias—IBD), the largest certifier in Latin America and HAZIR et al., 2016). Therefore, such bacteria could be a new the only Brazilian certifier of organic products, only approved alternative for attine ant management, as these insects main- Bioisca with the plant Tephrosia chandran for this purpose. tain an intimate symbiotic relationship with fungus. In addition, the effectiveness of botanical extracts to control The inhibitory effect of bacteria from the genus Xenorhabdus ants is questionable (CATALANI et al., 2017). on some phytopathogenic fungi has been recorded in previous The fungus-growing ants belong to the Attini tribe. studies (CHEN et al., 1994; BÖSZÖRMÉNYI et al., 2009). Only taking into account the species that practice such fungi For Photorhabdus spp., antimicrobials 2-isopropyl-5-(3-phe- culture (subtribe Attina, the attines), this group presents nyl-oxiranil)-benzeno-1, 3-diol, 3, 5, di-hydroxy-4-isopropyl- 15 genera and about 300 species (JEŠOVNIK et al., 2016). stilbene and β-lactama carbapenem (HU et al., 2006; BODE, The association between ants and cultivated fungus is considered 2009) have been reported. a compulsory mutualism, because both organisms present There is great potential for cultivation of NEPs through reciprocal adaptations to live, guaranteeing the stability of the fermenters (TAVARES et al., 2007) and associated bacteria interaction. In this mutualism, the fungus provides necessary through liquid cultivation medium, which allows for large scale nutrients for the colony, especially for the ants’ larvae. On production with low costs (SHAPIRO-ILAN et al., 2014). the other hand, ants guarantee the protection and dispersion In addition, the molecules of metabolites produced by bacteria of their fungal partner, as well as provide plant substrate for have already been identified, as is the case for trans-cinnamic- fungal cultivation. These ants are distributed in the Neotropical acid (TCA), a bio-fungicide with proven action (BOEMARE; region, from the southern United States to northern Argentina AKHURST, 2006), along with other antimicrobial compounds (MEHDIABADI; SCHULTZ, 2010). The most derived (MCINERNEY et al., 1991) present in this study. Attines are the leaf-cutter ants, that use fresh leaves and flowers Considering advances in research designed to promote to cultivate mutualist fungus (Leucocoprinus gongylophorus) biological
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