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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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Diversity of interactions in bioassays examining the presence and degree of cultivar inhibition of Pseudonocardia for symbionts isolated from across the phylogenetic diversity of the ant-fungus-bacterium association.Each box represents the average zone of inhibition (ZOI; n = 3) of a given pairing and different shades of grey indicate the degree of inhibition: White: ZOI = 0 cm, Light grey: ZOI = 0.01−0.29 cm, Grey: ZOI = 0.30−0.59 cm, Darker grey: ZOI = 0.60−0.89 cm, and Darkest grey: ZOI>0.90 cm.
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pone-0008748-g003: Diversity of interactions in bioassays examining the presence and degree of cultivar inhibition of Pseudonocardia for symbionts isolated from across the phylogenetic diversity of the ant-fungus-bacterium association.Each box represents the average zone of inhibition (ZOI; n = 3) of a given pairing and different shades of grey indicate the degree of inhibition: White: ZOI = 0 cm, Light grey: ZOI = 0.01−0.29 cm, Grey: ZOI = 0.30−0.59 cm, Darker grey: ZOI = 0.60−0.89 cm, and Darkest grey: ZOI>0.90 cm.

Mentions: Inhibition of Pseudonocardia by the fungal cultivar was observed in 68.4% and 72.9% of the bioassay pairings in our cross-phylogeny (Fig. 3) and within-Acromyrmex experiments (Fig. 4), respectively. The extent of inhibition of Pseudonocardia by cultivars ranged from 0 to 2.83 cm ZOI (Fig. 2A–D), but inhibition was generally low (mean±SE: 0.28±0.05 cm and 0.36±0.06 cm for the cross-phylogeny and within-Acromyrmex bioassays, respectively; Figs. 3 and 4). In the cross-phylogeny bioassay, individual strains of the cultivar inhibited on average 10 Pseudonocardia strains (range 2 to 14) and individual Pseudonocardia strains were on average susceptible to inhibition from 10 cultivar strains (range 6 to 12). Similarly, in the within-Acromyrmex bioassay, individual cultivars inhibited on average nine Pseudonocardia strains (range 1 to 12), while individual Pseudonocardia strains were susceptible to inhibition by an average of 9 cultivars (range 6 to 11). In the within-Acromyrmex bioassay, discoloration was observed in 31.3% of pairings. This occurred primarily in pairings with little growth inhibition, and mainly involved a few specific strains of cultivar, which frequently exhibited discoloration across several of the strains of Pseudonocardia (Fig. 5).


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)

Diversity of interactions in bioassays examining the presence and degree of cultivar inhibition of Pseudonocardia for symbionts isolated from across the phylogenetic diversity of the ant-fungus-bacterium association.Each box represents the average zone of inhibition (ZOI; n = 3) of a given pairing and different shades of grey indicate the degree of inhibition: White: ZOI = 0 cm, Light grey: ZOI = 0.01−0.29 cm, Grey: ZOI = 0.30−0.59 cm, Darker grey: ZOI = 0.60−0.89 cm, and Darkest grey: ZOI>0.90 cm.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0008748-g003: Diversity of interactions in bioassays examining the presence and degree of cultivar inhibition of Pseudonocardia for symbionts isolated from across the phylogenetic diversity of the ant-fungus-bacterium association.Each box represents the average zone of inhibition (ZOI; n = 3) of a given pairing and different shades of grey indicate the degree of inhibition: White: ZOI = 0 cm, Light grey: ZOI = 0.01−0.29 cm, Grey: ZOI = 0.30−0.59 cm, Darker grey: ZOI = 0.60−0.89 cm, and Darkest grey: ZOI>0.90 cm.
Mentions: Inhibition of Pseudonocardia by the fungal cultivar was observed in 68.4% and 72.9% of the bioassay pairings in our cross-phylogeny (Fig. 3) and within-Acromyrmex experiments (Fig. 4), respectively. The extent of inhibition of Pseudonocardia by cultivars ranged from 0 to 2.83 cm ZOI (Fig. 2A–D), but inhibition was generally low (mean±SE: 0.28±0.05 cm and 0.36±0.06 cm for the cross-phylogeny and within-Acromyrmex bioassays, respectively; Figs. 3 and 4). In the cross-phylogeny bioassay, individual strains of the cultivar inhibited on average 10 Pseudonocardia strains (range 2 to 14) and individual Pseudonocardia strains were on average susceptible to inhibition from 10 cultivar strains (range 6 to 12). Similarly, in the within-Acromyrmex bioassay, individual cultivars inhibited on average nine Pseudonocardia strains (range 1 to 12), while individual Pseudonocardia strains were susceptible to inhibition by an average of 9 cultivars (range 6 to 11). In the within-Acromyrmex bioassay, discoloration was observed in 31.3% of pairings. This occurred primarily in pairings with little growth inhibition, and mainly involved a few specific strains of cultivar, which frequently exhibited discoloration across several of the strains of Pseudonocardia (Fig. 5).

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