Candicidin-producing Streptomyces support leaf-cutting ants to protect their fungus garden against the pathogenic fungus Escovopsis

Leaf-cutting ants live in mutualistic symbiosis with their garden fungus Leucoagaricus gongylophorus that can be attacked by the specialized pathogenic fungus Escovopsis. Actinomyces symbionts from Acromyrmex leaf-cutting ants contribute to protect L. gongylophorus against pathogens. The symbiont Streptomyces sp. Av25_4 exhibited strong activity against Escovopsis weberi in co-cultivation assays. Experiments physically separating E. weberi and Streptomyces sp. Av25_4 allowing only exchange of volatiles revealed that Streptomyces sp. Av25_4 produces a volatile antifungal. Volatile compounds from Streptomyces sp. Av25_4 were collected by closed loop stripping. Analysis by NMR revealed that Streptomyces sp. Av25_4 overproduces ammonia (up to 8 mM) which completely inhibited the growth of E. weberi due to its strong basic pH. Additionally, other symbionts from different Acromyrmex ants inhibited E. weberi by production of ammonia. The waste of ca. one third of Acomyrmex and Atta leaf-cutting ant colonies was strongly basic due to ammonia (up to ca. 8 mM) suggesting its role in nest hygiene. Not only complex and metabolically costly secondary metabolites, such as polyketides, but simple ammonia released by symbionts of leaf-cutting ants can contribute to control the growth of Escovopsis that is sensitive to ammonia in contrast to the garden fungus L. gongylophorus.

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BIOLOGICAL CONTROL IN LEAF-CUTTING ANTS, Atta sexdens (HYMENOPTERA: FORMICIDAE), USING PATHOGENIC FUNGI

Revista Árvore ◽

10.1590/1806-908820210000016 ◽

2021 ◽

Vol 45 ◽

Author(s):

Tarcísio Marcos Macedo Mota Filho ◽

Luis Eduardo Pontes Stefanelli ◽

Roberto da Silva Camargo ◽

Carlos Alberto Oliveira de Matos ◽

Luiz Carlos Forti

Keyword(s):

Biological Control ◽

Chemical Control ◽

Pathogenic Fungi ◽

Behavioral Changes ◽

The Other ◽

Fungus Garden ◽

Atta Sexdens ◽

Main Method ◽

New Methods ◽

Leaf Cutting

ABSTRACT Chemical control using toxic baits containing the active ingredient sulfluramid at 0.3% (w/w) is the main method for controlling leaf-cutting ants of the genera Atta and Acromyrmex. However, since 2009, when sulfluramid was included in Annex B of the Stockholm Convention on Persistent Organic Pollutants, there has been an intense search for new methods that are efficient in controlling these insects. Among said new methods, biological control using pathogenic fungi has shown promising results in laboratory conditions. The objective of this study, given the context presented, was to assess the potential of the fungi Beauveria bassiana and Trichoderma harzianum in controlling Atta sexdens. Colonies of A. sexdens were exposed to the fungi by means of formulated baits provided in a foraging chamber, or of suspensions sprayed on the fungus garden, and had their behavioral changes recorded for 21 days. For both formulations, concentrations of 10 and 20% (w/w) of the fungi being studied were used. The results allowed concluding that baits containing 10 and 20% (w/w) of the fungi B. bassiana and T. harzianum were not efficient in controlling colonies of A sexdens. On the other hand, spraying suspensions of 20% (w/w) of B. bassiana and 10% and 20% (w/w) of T. harzianum was efficient and resulted in 100% mortality of the colonies 11, 9 and 7 days after application, respectively. These findings indicate that the fungi B. bassiana and T. harzianum are promising as agents for the control of A. sexdens colonies, when sprayed on the fungus garden, although there are still some challenges as to their use related to the development of technologies for the application of the pathogen.

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Communication between the fungus garden and workers of the leaf‐cutting ant, Atta sexdens rubropilosa , regarding choice of substrate for the fungus

Physiological Entomology ◽

10.1046/j.1365-3032.1999.00122.x ◽

1999 ◽

Vol 24 (2) ◽

pp. 127-133 ◽

Cited By ~ 31

Author(s):

R. D. North ◽

C. W. Jackson ◽

P. E. Howse

Keyword(s):

Fungus Garden ◽

Atta Sexdens ◽

Atta Sexdens Rubropilosa ◽

Leaf Cutting

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Social Carrying and Defensive Behavior During Colony Emigration in the Leaf-cutting Ant Atta sexdens

Sociobiology ◽

10.13102/sociobiology.v64i4.2087 ◽

2017 ◽

Vol 64 (4) ◽

pp. 492

Author(s):

Lohan Valadares ◽

Fábio S. Nascimento

Keyword(s):

Body Surface ◽

Defensive Behavior ◽

The Body ◽

Fungus Garden ◽

Atta Sexdens ◽

Defensive Strategies ◽

Laboratory Conditions ◽

Nesting Site ◽

Leaf Cutting ◽

First Time

In this work, we describe for the first time and under laboratory conditions, the behaviors related to social carrying and defensive strategies during colony emigration in the leaf-cutting ant Atta sexdens. Once colonies were laid on a tray under suboptimal conditions, groups of workers aggregated all over the body surface of the queen and brood, with mandibles half open and legs widely open in a ‘entangle’ formation. Queens were the first caste to be reallocated, followed respectively by the transportation of brood, newly-emerged workers, and pieces of fungus garden to the new nesting site. Contrary to what have been reported to the Myrmicinae species, adult transport followed a stereotyped sequence of acts involving approach, seize and transportation of newly-emerged workers to new target areas. Our results suggest that, in front of rapid unfavorable changes, leaf-cutting ants are capable of reorganize the nest in order to protect their members and resources.

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Carbon dioxide levels and ventilation in Acromyrmex nests: significance and evolution of architectural innovations in leaf-cutting ants

Royal Society Open Science ◽

10.1098/rsos.210907 ◽

2021 ◽

Vol 8 (11) ◽

Author(s):

Martin Bollazzi ◽

Daniela Römer ◽

Flavio Roces

Keyword(s):

Soil Surface ◽

Fungus Garden ◽

Ant Colonies ◽

Gas Exchanges ◽

Selective Pressures ◽

Leaf Cutting ◽

Single Opening ◽

Carbon Dioxide Levels ◽

Nesting Habits ◽

Ancestral Type

Leaf-cutting ant colonies largely differ in size, yet all consume O 2 and produce CO 2 in large amounts because of their underground fungus gardens. We have shown that in the Acromyrmex genus, three basic nest morphologies occur, and investigated the effects of architectural innovations on nest ventilation. We recognized (i) serial nests, similar to the ancestral type of the sister genus Trachymyrmex , with chambers excavated along a vertical tunnel connecting to the outside via a single opening, (ii) shallow nests, with one/few chambers extending shallowly with multiple connections to the outside, and (iii) thatched nests, with an above-ground fungus garden covered with plant material. Ventilation in shallow and thatched nests, but not in serial nests, occurred via wind-induced flows and thermal convection. CO 2 concentrations were below the values known to affect the respiration of the symbiotic fungus, indicating that shallow and thatched nests are not constrained by harmful CO 2 levels. Serial nests may be constrained depending on the soil CO 2 levels. We suggest that in Acromyrmex , selective pressures acting on temperature and humidity control led to nesting habits closer to or above the soil surface and to the evolution of architectural innovations that improved gas exchanges.

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Symbiotic bacteria on the cuticle of the leaf-cutting ant Acromyrmex subterraneus subterraneus protect workers from attack by entomopathogenic fungi

Biology Letters ◽

10.1098/rsbl.2011.0963 ◽

2011 ◽

Vol 8 (3) ◽

pp. 461-464 ◽

Cited By ~ 60

Author(s):

Thalles C. Mattoso ◽

Denise D. O. Moreira ◽

Richard I. Samuels

Keyword(s):

Direct Evidence ◽

Fungus Garden ◽

Defensive Strategy ◽

Fungal Entomopathogen ◽

Leaf Cutting ◽

The Subject ◽

Anti Fungal ◽

First Time ◽

Intense Research

Although only discovered in 1999, the symbiotic filamentous actinobacteria present on the integument of certain species of leaf-cutting ants have been the subject of intense research. These bacteria have been shown to specifically suppress fungal garden parasites by secretion of antibiotics. However, more recently, a wider role for these bacteria has been suggested from research revealing their generalist anti-fungal activity. Here we show, for the first time, evidence for a role of these bacteria in the defence of young worker ants against a fungal entomopathogen. Experimental removal of the bacterial bio-film using an antibiotic resulted in a significant increase in susceptibility of worker ants to infection by the entomopathogenic fungus Metarhizium anisopliae . This is the first direct evidence for the advantage of maintaining a bacterial bio-film on the cuticle as a defensive strategy of the ants themselves and not exclusively for protection of the fungus garden.

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Direct ingestion of plant sap from cut leaves by the leaf-cutting ants Atta cephalotes (L.) and acromyrmex octospinosus (reich) (Formicidae, Attini)

Bulletin of Entomological Research ◽

10.1017/s0007485300006647 ◽

1976 ◽

Vol 66 (2) ◽

pp. 205-217 ◽

Cited By ~ 72

Author(s):

M. Littledyke ◽

J. M. Cherrett

Keyword(s):

Plant Material ◽

Atta Cephalotes ◽

Fungus Garden ◽

Acromyrmex Octospinosus ◽

Substrate Preparation ◽

Fungus Culture ◽

Large Numbers ◽

Leaf Cutting ◽

Laboratory Colonies ◽

Reduced Drinking

AbstractIngestion of radiolabelled plant juices from cut surfaces of leaves during foraging and during substrate preparation for the fungus garden was demonstrated for laboratory colonies of the leaf-cutting ants Atta cephalotes (L.) and Acromyrmex octospinosus (Reich). Using P32 isotope, up to one-third of the radioactivity in the leaves was taken in directly by the colony as a whole, but this was much less when C14 was used. Additional plant material was taken in by the ants via the fungus garden. Large numbers of ants spend time in investigating cut surfaces of leaves and also in cutting and crimping leaves. Ingestion of plant material during these processes could play an important nutritional role in the colony and this may explain why many ants return from foraging apparently unladen. Large ants obtained most of their plant juice intake during foraging and the medium and small ants took much of theirs during substrate preparation. Inhibitory chemicals did not affect cutting but they reduced drinking and also reduced the intake of P32 from leaves during substrate preparation. The ants also ingested different amounts of P32 from leaves of different acceptability. It is suggested that leaf-cutting ants use fungus culture as a means of ‘sidestepping’ plant inhibitors. Nutrients are ingested directly from leaves when these are palatable, and the less palatable components are made available to the ants via the fungus.

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Use of Seeds as Fungus Garden Substrate Changes the Organization of Labor Among Leaf-Cutting Ant Workers

Neotropical Entomology ◽

10.1007/s13744-015-0299-0 ◽

2015 ◽

Vol 44 (4) ◽

pp. 351-356

Author(s):

I N Hastenreiter ◽

T A Sales ◽

R S Camargo ◽

L C Forti ◽

J F S Lopes

Keyword(s):

Fungus Garden ◽

Leaf Cutting

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Competition-based screening secures the evolutionary stability of a defensive microbiome

10.1101/2020.11.24.395384 ◽

2020 ◽

Author(s):

Sarah F. Worsley ◽

Tabitha M. Innocent ◽

Neil A. Holmes ◽

Mahmoud M. Al-Bassam ◽

Barrie Wilkinson ◽

...

Keyword(s):

Game Theory ◽

Stable Isotope ◽

Rna Sequencing ◽

Growth Rates ◽

Evolutionary Stability ◽

Stable Isotope Probing ◽

Fungus Garden ◽

Bacterial Strains ◽

Leaf Cutting ◽

Microbial Symbionts

AbstractCuticular microbiomes of Acromyrmex leaf-cutting ants are exceptional because they are freely colonizable, and yet the prevalence of Pseudonocardia, a native vertically transmitted symbiont that controls Escovopsis fungus-garden disease, is never compromised. Game theory suggests that competition-based screening can allow the selective recruitment of antibiotic-producing bacteria from the environment, by fomenting and biasing competition for abundant host resources. Mutual symbiont aggression benefits the host and also maintains native symbiont viability. Here we use RNA-stable isotope probing (RNA-SIP) to confirm predictions that Acromyrmex cuticles can maintain a range of microbial symbionts. We then used dual-RNA-sequencing and bioassays to show that vertically transmitted Pseudonocardia strains produce antibacterials that differentially reduce the growth rates of other microbes, ultimately eliminating non-antibiotic-producing strains that might parasitize the symbiosis while still allowing antibiotic-producing Streptomyces strains to survive. Open cuticular microbiomes can thus maintain a specific co-evolved mutualism by restricting access for other bacterial strains.

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