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1. Cold adaptations along a range limit in an obligate symbiosis

   https://doi.org/10.1111/1365-2435.14120  

   Senula, Sarah F. ; Scavetta, Joseph T. ; Mueller, Ulrich G. ; Seal, Jon Nicholas ; Kellner, Katrin ( July 2022 , Functional Ecology)

   Symbionts can have profound effects on host fitness, adaptations and range distributions. Stress‐induced evolution is difficult to show in obligate symbioses; however, adaptive evolution within an obligate symbiosis can be investigated experimentally or by correlating trait variation with stress along an ecological cline (i.e. temperature‐stress gradient).

   We investigated the cold tolerance of the fungus‐growing antTrachymyrmex septentrionalisby performing cold tolerance assays comparing two populations collected from either the southernmost range of their distribution (Bastrop, Texas) or from a site that is approximately 600 km further north (Norman, Oklahoma). We first compared isolated fungal symbionts grown on artificial media to determine cold tolerance of fungus alone. Subsequently, we conducted cross‐fostering experiments between northern and southern host and symbionts to test for synergisms between the partners in generating adaptations of cold tolerance.

   Ants of the northern fungal populations were more cold adapted than southern fungal populations. Northern nests were deeper and northern colonies initially rejected fungi from the southern population. The cross‐fostering experiments demonstrated that only one partner must be cold tolerant to confer maximum cold tolerance to the ant–fungus symbiosis, because northern ants growing southern fungus under cold stress performed just as well as northern ants growing northern fungi.

   Our results suggest that cold stress has been an important selective factor during the migration of this ant–fungus symbiosis into northern latitudes during the last 10,000 years, and that cold tolerance likely is an energetically demanding trait that may be traded off with other aspects of the symbiosis' life history. The symbiosis also appears to have evolved several additional adaptations that increase survival in cold environments, such as building deeper nests that insulate the fungi from cold surface.

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2. Cophylogenetic analyses of Trachymyrmex ant‐fungal specificity: “One to one with some exceptions”

   https://doi.org/10.1111/mec.16140  

   Beigel, Katherine ; Matthews, Alix E. ; Kellner, Katrin ; Pawlik, Christine V. ; Greenwold, Matthew ; Seal, Jon N. ( September 2021 , Molecular Ecology)

   Over the past few decades, large‐scale phylogenetic analyses of fungus‐gardening ants and their symbiotic fungi have depicted strong concordance among major clades of ants and their symbiotic fungi, yet within clades, fungus sharing is widespread among unrelated ant lineages. Sharing has been explained using a diffuse coevolution model within major clades. Understanding horizontal exchange within clades has been limited by conventional genetic markers that lack both interspecific and geographic variation. To examine whether reports of horizontal exchange were indeed due to symbiont sharing or the result of employing relatively uninformative molecular markers, samples ofTrachymyrmex arizonensisandTrachymyrmex pomonaeand their fungi were collected from native populations in Arizona and genotyped using conventional marker genes and genome‐wide single nucleotide polymorphisms (SNPs). Conventional markers of the fungal symbionts generally exhibited cophylogenetic patterns that were consistent with some symbiont sharing, but most fungal clades had low support. SNP analysis, in contrast, indicated that each ant species exhibited fidelity to its own fungal subclade with only one instance of a colony growing a fungus that was otherwise associated with a different ant species. This evidence supports a pattern of codivergence betweenTrachymyrmexspecies and their fungi, and thus a diffuse coevolutionary model may not accurately predict symbiont exchange. These results suggest that fungal sharing across host species in these symbioses may be less extensive than previously thought.

    

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3. Transcriptomic basis of genome by genome variation in a legume‐rhizobia mutualism

   https://doi.org/10.1111/mec.14285  

   Burghardt, Liana T. ; Guhlin, Joseph ; Chun, Chan Lan ; Liu, Junqi ; Sadowsky, Michael J. ; Stupar, Robert M. ; Young, Nevin D. ; Tiffin, Peter ( September 2017 , Molecular Ecology)

   In the legume‐rhizobia mutualism, the benefit each partner derives from the other depends on the genetic identity of both host and rhizobial symbiont. To gain insight into the extent of genome × genome interactions on hosts at the molecular level and to identify potential mechanisms responsible for the variation, we examined host gene expression within nodules (the plant organ where the symbiosis occurs) of four genotypes ofMedicago truncatulagrown with eitherEnsifer melilotiorE. medicaesymbionts. These host × symbiont combinations show significant variation in nodule and biomass phenotypes. Likewise, combinations differ in their transcriptomes: host, symbiont and host × symbiont affected the expression of 70%, 27% and 21%, respectively, of the approximately 27,000 host genes expressed in nodules. Genes with the highest levels of expression often varied between hosts and/or symbiont strain and include leghemoglobins that modulate oxygen availability and hundreds of Nodule Cysteine‐Rich (NCR) peptides involved in symbiont differentiation and viability in nodules. Genes with host × symbiont‐dependent expression were enriched for functions related to resource exchange between partners (sulphate/iron/amino acid transport and dicarboxylate/amino acid synthesis). These enrichments suggest mechanisms for host control of the currencies of the mutualism. The transcriptome ofM. truncatulaaccessionHM101 (A17), the reference genome used for most molecular research, was less affected by symbiont identity than the other hosts. These findings underscore the importance of assessing the molecular basis of variation in ecologically important traits, particularly those involved in biotic interactions, in multiple genetic contexts.

    

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4. Symbiont-Mediated Protection of Acromyrmex Leaf-Cutter Ants from the Entomopathogenic Fungus Metarhizium anisopliae

   https://doi.org/10.1128/mBio.01885-21  

   Bruner-Montero, Gaspar ; Wood, Matthew ; Horn, Heidi A. ; Gemperline, Erin ; Li, Lingjun ; Currie, Cameron R. ( December 2021 , mBio)

   Cavanaugh, Colleen M. (Ed.)

   ABSTRACT Many fungus-growing ants engage in a defensive symbiosis with antibiotic-producing ectosymbiotic bacteria in the genus Pseudonocardia , which help protect the ants’ fungal mutualist from a specialized mycoparasite, Escovopsis . Here, using germfree ant rearing and experimental pathogen infection treatments, we evaluate if Acromyrmex ants derive higher immunity to the entomopathogenic fungus Metarhizium anisopliae from their Pseudonocardia symbionts. We further examine the ecological dynamics and defensive capacities of Pseudonocardia against M. anisopliae across seven different Acromyrmex species by controlling Pseudonocardia acquisition using ant-nonnative Pseudonocardia switches, in vitro challenges, and in situ mass spectrometry imaging (MSI). We show that Pseudonocardia protects the ants against M. anisopliae across different Acromyrmex species and appears to afford higher protection than metapleural gland (MG) secretions. Although Acromyrmex echinatior ants with nonnative Pseudonocardia symbionts receive protection from M. anisopliae regardless of the strain acquired compared with Pseudonocardia -free conditions, we find significant variation in the degree of protection conferred by different Pseudonocardia strains. Additionally, when ants were reared in Pseudonocardia -free conditions, some species exhibit more susceptibility to M. anisopliae than others, indicating that some ant species depend more on defensive symbionts than others. In vitro challenge experiments indicate that Pseudonocardia reduces Metarhizium conidiospore germination area. Our chemometric analysis using matrix-assisted laser desorption/ionization mass spectrometry imaging (MALDI-MSI) reveals that Pseudonocardia -carrying ants produce more chemical signals than Pseudonocardia -free treatments, indicating that Pseudonocardia produces bioactive metabolites on the Acromyrmex cuticle. Our results indicate that Pseudonocardia can serve as a dual-purpose defensive symbiont, conferring increased immunity for both the obligate fungal mutualist and the ants themselves. IMPORTANCE In some plants and animals, beneficial microbes mediate host immune response against pathogens, including by serving as defensive symbionts that produce antimicrobial compounds. Defensive symbionts are known in several insects, including some leaf-cutter ants where antifungal-producing Actinobacteria help protect the fungal mutualist of the ants from specialized mycoparasites. In many defensive symbioses, the extent and specificity of defensive benefits received by the host are poorly understood. Here, using “aposymbiotic” rearing, symbiont switching experiments, and imaging mass spectrometry, we explore the ecological and chemical dynamics of the model defensive symbiosis between Acromyrmex ants and their defensive symbiotic bacterium Pseudonocardia . We show that the defensive symbiont not only protects the fungal crop of Acromyrmex but also provides protection from fungal pathogens that infect the ant workers themselves. Furthermore, we reveal that the increased immunity to pathogen infection differs among strains of defensive symbionts and that the degree of reliance on a defensive symbiont for protection varies across congeneric ant species. Taken together, our results suggest that Acromyrmex -associated Pseudonocardia have evolved broad antimicrobial defenses that promote strong immunity to diverse fungal pathogens within the ancient fungus-growing ant-microbe symbiosis. 

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5. Burkholderia from Fungus Gardens of Fungus-Growing Ants Produces Antifungals That Inhibit the Specialized Parasite Escovopsis

   https://doi.org/10.1128/AEM.00178-21  

   Francoeur, Charlotte B. ; May, Daniel S. ; Thairu, Margaret W. ; Hoang, Don Q. ; Panthofer, Olivia ; Bugni, Tim S. ; Pupo, Mônica T. ; Clardy, Jon ; Pinto-Tomás, Adrián A. ; Currie, Cameron R. ( June 2021 , Applied and Environmental Microbiology)

   Rudi, Knut (Ed.)

   ABSTRACT Within animal-associated microbiomes, the functional roles of specific microbial taxa are often uncharacterized. Here, we use the fungus-growing ant system, a model for microbial symbiosis, to determine the potential defensive roles of key bacterial taxa present in the ants’ fungus gardens. Fungus gardens serve as an external digestive system for the ants, with mutualistic fungi in the genus Leucoagaricus converting the plant substrate into energy for the ants. The fungus garden is host to specialized parasitic fungi in the genus Escovopsis . Here, we examine the potential role of Burkholderia spp. that occur within ant fungus gardens in inhibiting Escovopsis. We isolated members of the bacterial genera Burkholderia and Paraburkholderia from 50% of the 52 colonies sampled, indicating that members of the family Burkholderiaceae are common inhabitants in the fungus gardens of a diverse range of fungus-growing ant genera. Using antimicrobial inhibition bioassays, we found that 28 out of 32 isolates inhibited at least one Escovopsis strain with a zone of inhibition greater than 1 cm. Genomic assessment of fungus garden-associated Burkholderiaceae indicated that isolates with strong inhibition all belonged to the genus Burkholderia and contained biosynthetic gene clusters that encoded the production of two antifungals: burkholdine1213 and pyrrolnitrin. Organic extracts of cultured isolates confirmed that these compounds are responsible for antifungal activities that inhibit Escovopsis but, at equivalent concentrations, not Leucoagaricus spp. Overall, these new findings, combined with previous evidence, suggest that members of the fungus garden microbiome play an important role in maintaining the health and function of fungus-growing ant colonies. IMPORTANCE Many organisms partner with microbes to defend themselves against parasites and pathogens. Fungus-growing ants must protect Leucoagaricus spp., the fungal mutualist that provides sustenance for the ants, from a specialized fungal parasite, Escovopsis . The ants take multiple approaches, including weeding their fungus gardens to remove Escovopsis spores, as well as harboring Pseudonocardia spp., bacteria that produce antifungals that inhibit Escovopsis. In addition, a genus of bacteria commonly found in fungus gardens, Burkholderia , is known to produce secondary metabolites that inhibit Escovopsis spp. In this study, we isolated Burkholderia spp. from fungus-growing ants, assessed the isolates’ ability to inhibit Escovopsis spp., and identified two compounds responsible for inhibition. Our findings suggest that Burkholderia spp. are often found in fungus gardens, adding another possible mechanism within the fungus-growing ant system to suppress the growth of the specialized parasite Escovopsis . 

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