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Symbiont interactions in a tripartite mutualism: exploring the presence and impact of antagonism between two fungus-growing ant mutualists.

Poulsen M, Currie CR - PLoS ONE (2010)

Bottom Line: We created novel ant-fungus-bacterium pairings in which there was antagonism from one, both, or neither of the ants' microbial mutualists, and evaluated the effect of directional antagonism on cultivar biomass and Pseudonocardia abundance on the cuticle of workers within sub-colonies.Despite the presence of frequent in vitro growth suppression between cultivars and Pseudonocardia, antagonism from Pseudonocardia towards the cultivar did not reduce sub-colony fungus garden biomass, nor did cultivar antagonism towards Pseudonocardia reduce bacteria abundance on the cuticle of sub-colony workers.Our findings suggest that inter-mutualist antagonism does not limit what combinations of cultivar and Pseudonocardia strains Acromyrmex fungus-growing ants can maintain within nests.

View Article: PubMed Central - PubMed

Affiliation: Department of Bacteriology, University of Wisconsin-Madison, Madison, Wisconsin, United States of America. Poulsen@bact.wisc.edu

ABSTRACT
Mutualistic associations are shaped by the interplay of cooperation and conflict among the partners involved, and it is becoming increasingly clear that within many mutualisms multiple partners simultaneously engage in beneficial interactions. Consequently, a more complete understanding of the dynamics within multipartite mutualism communities is essential for understanding the origin, specificity, and stability of mutualisms. Fungus-growing ants cultivate fungi for food and maintain antibiotic-producing Pseudonocardia actinobacteria on their cuticle that help defend the cultivar fungus from specialized parasites. Within both ant-fungus and ant-bacterium mutualisms, mixing of genetically distinct strains can lead to antagonistic interactions (i.e., competitive conflict), which may prevent the ants from rearing multiple strains of either of the mutualistic symbionts within individual colonies. The success of different ant-cultivar-bacterium combinations could ultimately be governed by antagonistic interactions between the two mutualists, either as inhibition of the cultivar by Pseudonocardia or vice versa. Here we explore cultivar-Pseudonocardia antagonism by evaluating in vitro interactions between strains of the two mutualists, and find frequent antagonistic interactions both from cultivars towards Pseudonocardia and vice versa. To test whether such in vitro antagonistic interactions affect ant colonies in vivo, we performed sub-colony experiments using species of Acromyrmex leaf-cutting ants. We created novel ant-fungus-bacterium pairings in which there was antagonism from one, both, or neither of the ants' microbial mutualists, and evaluated the effect of directional antagonism on cultivar biomass and Pseudonocardia abundance on the cuticle of workers within sub-colonies. Despite the presence of frequent in vitro growth suppression between cultivars and Pseudonocardia, antagonism from Pseudonocardia towards the cultivar did not reduce sub-colony fungus garden biomass, nor did cultivar antagonism towards Pseudonocardia reduce bacteria abundance on the cuticle of sub-colony workers. Our findings suggest that inter-mutualist antagonism does not limit what combinations of cultivar and Pseudonocardia strains Acromyrmex fungus-growing ants can maintain within nests.

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Micrographs showing typical extremes in reactions observed between symbiont pairings.(a)–(d) Cultivar (middle) inhibition of Pseudonocardia (edge) (a) No cultivar-induced inhibition of Pseudonocardia, (b) intermediary cultivar-induced inhibition of Pseudonocardia, (c) strong cultivar-induced inhibition of Pseudonocardia, (d) no cultivar-induced inhibition of Pseudonocardia, but strong discoloration indicating antagonistic chemical interactions. (e)–(h) Pseudonocardia (middle) inhibition of the cultivar (edge). (e) No Pseudonocardia-induced inhibition of the cultivar, (f) intermediary Pseudonocardia-induced inhibition of the cultivar, (g) strong Pseudonocardia induced inhibition of the cultivar, and (h) weak Pseudonocardia-induced inhibition of the cultivar, but strong discoloration indicating antagonistic chemical interactions.
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pone-0008748-g002: Micrographs showing typical extremes in reactions observed between symbiont pairings.(a)–(d) Cultivar (middle) inhibition of Pseudonocardia (edge) (a) No cultivar-induced inhibition of Pseudonocardia, (b) intermediary cultivar-induced inhibition of Pseudonocardia, (c) strong cultivar-induced inhibition of Pseudonocardia, (d) no cultivar-induced inhibition of Pseudonocardia, but strong discoloration indicating antagonistic chemical interactions. (e)–(h) Pseudonocardia (middle) inhibition of the cultivar (edge). (e) No Pseudonocardia-induced inhibition of the cultivar, (f) intermediary Pseudonocardia-induced inhibition of the cultivar, (g) strong Pseudonocardia induced inhibition of the cultivar, and (h) weak Pseudonocardia-induced inhibition of the cultivar, but strong discoloration indicating antagonistic chemical interactions.

Mentions: Petri plate bioassay experiments testing for the presence of directional antagonism (cultivar inhibition of Pseudonocardia and vice versa) were performed for both cross-phylogeny and within-Acromyrmex symbiont isolates. See Fig. 2 for examples of observed interactions, including strong inhibition of one symbiont by another. All bioassay experiments were performed at a constant temperature of 25°C in 8.5 cm diameter Petri plates containing YMEA without antibiotics; three replicates were performed for all pairings.


Symbiont interactions in a tripartite mutualism: exploring the presence and impact of antagonism between two fungus-growing ant mutualists.

Poulsen M, Currie CR - PLoS ONE (2010)

Micrographs showing typical extremes in reactions observed between symbiont pairings.(a)–(d) Cultivar (middle) inhibition of Pseudonocardia (edge) (a) No cultivar-induced inhibition of Pseudonocardia, (b) intermediary cultivar-induced inhibition of Pseudonocardia, (c) strong cultivar-induced inhibition of Pseudonocardia, (d) no cultivar-induced inhibition of Pseudonocardia, but strong discoloration indicating antagonistic chemical interactions. (e)–(h) Pseudonocardia (middle) inhibition of the cultivar (edge). (e) No Pseudonocardia-induced inhibition of the cultivar, (f) intermediary Pseudonocardia-induced inhibition of the cultivar, (g) strong Pseudonocardia induced inhibition of the cultivar, and (h) weak Pseudonocardia-induced inhibition of the cultivar, but strong discoloration indicating antagonistic chemical interactions.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2806923&req=5

pone-0008748-g002: Micrographs showing typical extremes in reactions observed between symbiont pairings.(a)–(d) Cultivar (middle) inhibition of Pseudonocardia (edge) (a) No cultivar-induced inhibition of Pseudonocardia, (b) intermediary cultivar-induced inhibition of Pseudonocardia, (c) strong cultivar-induced inhibition of Pseudonocardia, (d) no cultivar-induced inhibition of Pseudonocardia, but strong discoloration indicating antagonistic chemical interactions. (e)–(h) Pseudonocardia (middle) inhibition of the cultivar (edge). (e) No Pseudonocardia-induced inhibition of the cultivar, (f) intermediary Pseudonocardia-induced inhibition of the cultivar, (g) strong Pseudonocardia induced inhibition of the cultivar, and (h) weak Pseudonocardia-induced inhibition of the cultivar, but strong discoloration indicating antagonistic chemical interactions.
Mentions: Petri plate bioassay experiments testing for the presence of directional antagonism (cultivar inhibition of Pseudonocardia and vice versa) were performed for both cross-phylogeny and within-Acromyrmex symbiont isolates. See Fig. 2 for examples of observed interactions, including strong inhibition of one symbiont by another. All bioassay experiments were performed at a constant temperature of 25°C in 8.5 cm diameter Petri plates containing YMEA without antibiotics; three replicates were performed for all pairings.

Bottom Line: We created novel ant-fungus-bacterium pairings in which there was antagonism from one, both, or neither of the ants' microbial mutualists, and evaluated the effect of directional antagonism on cultivar biomass and Pseudonocardia abundance on the cuticle of workers within sub-colonies.Despite the presence of frequent in vitro growth suppression between cultivars and Pseudonocardia, antagonism from Pseudonocardia towards the cultivar did not reduce sub-colony fungus garden biomass, nor did cultivar antagonism towards Pseudonocardia reduce bacteria abundance on the cuticle of sub-colony workers.Our findings suggest that inter-mutualist antagonism does not limit what combinations of cultivar and Pseudonocardia strains Acromyrmex fungus-growing ants can maintain within nests.

View Article: PubMed Central - PubMed

Affiliation: Department of Bacteriology, University of Wisconsin-Madison, Madison, Wisconsin, United States of America. Poulsen@bact.wisc.edu

ABSTRACT
Mutualistic associations are shaped by the interplay of cooperation and conflict among the partners involved, and it is becoming increasingly clear that within many mutualisms multiple partners simultaneously engage in beneficial interactions. Consequently, a more complete understanding of the dynamics within multipartite mutualism communities is essential for understanding the origin, specificity, and stability of mutualisms. Fungus-growing ants cultivate fungi for food and maintain antibiotic-producing Pseudonocardia actinobacteria on their cuticle that help defend the cultivar fungus from specialized parasites. Within both ant-fungus and ant-bacterium mutualisms, mixing of genetically distinct strains can lead to antagonistic interactions (i.e., competitive conflict), which may prevent the ants from rearing multiple strains of either of the mutualistic symbionts within individual colonies. The success of different ant-cultivar-bacterium combinations could ultimately be governed by antagonistic interactions between the two mutualists, either as inhibition of the cultivar by Pseudonocardia or vice versa. Here we explore cultivar-Pseudonocardia antagonism by evaluating in vitro interactions between strains of the two mutualists, and find frequent antagonistic interactions both from cultivars towards Pseudonocardia and vice versa. To test whether such in vitro antagonistic interactions affect ant colonies in vivo, we performed sub-colony experiments using species of Acromyrmex leaf-cutting ants. We created novel ant-fungus-bacterium pairings in which there was antagonism from one, both, or neither of the ants' microbial mutualists, and evaluated the effect of directional antagonism on cultivar biomass and Pseudonocardia abundance on the cuticle of workers within sub-colonies. Despite the presence of frequent in vitro growth suppression between cultivars and Pseudonocardia, antagonism from Pseudonocardia towards the cultivar did not reduce sub-colony fungus garden biomass, nor did cultivar antagonism towards Pseudonocardia reduce bacteria abundance on the cuticle of sub-colony workers. Our findings suggest that inter-mutualist antagonism does not limit what combinations of cultivar and Pseudonocardia strains Acromyrmex fungus-growing ants can maintain within nests.

Show MeSH
Related in: MedlinePlus