An official website of the United States government
The metabolic intimacy of symbiosis often demands the work of specialists. Natural products and defensive secondary metabolites can drive specificity by ensuring infection and propagation across host generations. But in contrast to bacteria, little is known about the diversity and distribution of natural product biosynthetic pathways among fungi and how they evolve to facilitate symbiosis and adaptation to their host environment. In this study, we define the secondary metabolism of Escovopsis and closely related genera, symbionts in the gardens of fungus-farming ants. We ask how the gain and loss of various biosynthetic pathways correspond to divergent lifestyles. Long-read sequencing allowed us to define the chromosomal features of representative Escovopsis strains, revealing highly reduced genomes composed of seven to eight chromosomes. The genomes are highly syntenic with macrosynteny decreasing with increasing phylogenetic distance, while maintaining a high degree of mesosynteny. An ancestral state reconstruction analysis of biosynthetic pathways revealed that, while many secondary metabolites are shared with non-ant-associated Sordariomycetes, 56 pathways are unique to the symbiotic genera. Reflecting adaptation to diverging ant agricultural systems, we observe that the stepwise acquisition of these pathways mirrors the ecological radiations of attine ants and the dynamic recruitment and replacement of their fungal cultivars. As different clades encode characteristic combinations of biosynthetic gene clusters, these delineating profiles provide important insights into the possible mechanisms underlying specificity between these symbionts and their fungal hosts. Collectively, our findings shed light on the evolutionary dynamic nature of secondary metabolism in Escovopsis and its allies, reflecting adaptation of the symbionts to an ancient agricultural system.Microbial symbionts interact with their hosts and competitors through a remarkable array of secondary metabolites and natural products. Here, we highlight the highly streamlined genomic features of attine-associated fungal symbionts. The genomes of Escovopsis species, as well as species from other symbiont genera, many of which are common with the gardens of fungus-growing ants, are defined by seven chromosomes. Despite a high degree of metabolic conservation, we observe some variation in the symbionts’ potential to produce secondary metabolites. As the phylogenetic distribution of the encoding biosynthetic gene clusters coincides with attine transitions in agricultural systems, we highlight the likely role of these metabolites in mediating adaptation by a group of highly specialized symbionts.
more »
« less
Masters of the manipulator: two new hypocrealean genera, Niveomyces ( Cordycipitaceae ) and Torrubiellomyces ( Ophiocordycipitaceae ), parasitic on the zombie ant fungus Ophiocordyceps camponoti-floridani
During surveys in central Florida of the zombie-ant fungus Ophiocordyceps camponoti-floridani , which manipulates the behavior of the carpenter ant Camponotus floridanus , two distinct fungal morphotypes were discovered associated with and purportedly parasitic on O. camponoti-floridani . Based on a combination of unique morphology, ecology and phylogenetic placement, we discovered that these morphotypes comprise two novel lineages of fungi. Here, we propose two new genera, Niveomyces and Torrubiellomyces , each including a single species within the families Cordycipitaceae and Ophiocordycipitaceae , respectively. We generated de novo draft genomes for both new species and performed morphological and multi-loci phylogenetic analyses. The macro-morphology and incidence of both new species, Niveomyces coronatus and Torrubiellomyces zombiae , suggest that these fungi are mycoparasites since their growth is observed exclusively on O. camponoti-floridani mycelium, stalks and ascomata, causing evident degradation of their fungal hosts. This work provides a starting point for more studies into fungal interactions between mycopathogens and entomopathogens, which have the potential to contribute towards efforts to battle the global rise of plant and animal mycoses.
more »
« less
- Award ID(s):
- 1941546
- PAR ID:
- 10422875
- Date Published:
- Journal Name:
- Persoonia - Molecular Phylogeny and Evolution of Fungi
- Volume:
- 49
- Issue:
- 1
- ISSN:
- 0031-5850
- Page Range / eLocation ID:
- 171 to 194
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Estimating stomatopod species diversity using morphology alone has long been difficult; though over 450 species have been described, new species are still being discovered regularly despite the cryptic behaviors of adults. However, the larvae of stomatopods are more easily obtained due to their pelagic habitat, and have been the focus of recent studies of diversity. Studies of morphological diversity describe both conserved and divergent traits in larval stomatopods, but generally cannot be linked to a particular species. Conversely, genetic studies of stomatopod larvae using DNA barcoding can be used to estimate species diversity, but are generally not linked to known species by analyses of morphological characters. Here we combine these two approaches, larval morphology and genetics, to estimate stomatopod species diversity in the Hawaiian Islands. Over 22 operational taxonomic units (OTUs) were identified genetically, corresponding to 20 characterized morphological types. Species from three major superfamilies of stomatopod were identified: Squilloidea (4 OTUs, 3 morphotypes), Gonodactyloidea (9, 8), and Lysiosquilloidea (6, 7). Among these, lysiosquilloids were more diverse based on larval morphotypes and OTUs as compared to previously documented Hawaiian species (3), while squilloids had a lower diversity of species represented by collected larvae as compared to the seven species previously documented. Two OTUs / morphotypes could not be identified to superfamily as their molecular and morphological features did not closely match any available information, suggesting they belong to poorly sampled superfamilies. The pseudosquillid, Pseudosquillana richeri, was discovered for the first time from Hawaiʻi. This study contributes an updated estimate for Hawaiian stomatopod diversity for a total of 24 documented species, provides references for identification of larval stomatopods across the three major superfamilies, and emphasizes the lack of knowledge of species diversity in more cryptic stomatopod superfamilies, such as Lysiosquilloidea.more » « less
-
Abstract Complete chromosomal-level assemblies of fungal genomes are rare. The intimate ecological symbioses and complex reproduction strategies utilized by fungi make highly contiguous, gapless genome assemblies particularly difficult. Here, we use long-read sequencing on the Oxford Nanopore Technology MinION platform to sequence and assemble the genome of Lepraria neglecta ( Ascomycota , Lecanorales ). In addition to eight contigs ascribable to chromosomes, six of which are assembled telomere-to-telomere, we discovered the presence of a complete MAT locus with two conserved MAT1-2 genes and a putative MAT1-1 pseudogene. The full genome assembly of a widespread, common species presents an opportunity for new insights into lichen reproduction while the presence of the mating-type locus in the genome of an asexual lichen raises fundamental questions about reproductive biology in fungi generally.more » « less
-
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 .more » « less
-
Chiang, Tzen-Yuh (Ed.)Eukaryotic hosts harbor tremendously diverse microbiomes that affect host fitness and response to environmental challenges. Fungal endophytes are prominent members of plant microbiomes, but we lack information on the diversity in functional traits affecting their interactions with their host and environment. We used two culturing approaches to isolate fungal endophytes associated with the widespread, dominant prairie grassAndropogon gerardiiand characterized their taxonomic diversity using rDNA barcode sequencing. A randomly chosen subset of fungi representing the diversity of each leaf was then evaluated for their use of different carbon compound resources and growth on those resources. Applying community phylogenetic analyses, we discovered that these fungal endophyte communities are comprised of phylogenetically distinct assemblages of slow- and fast-growing fungi that differ in their use and growth on differing carbon substrates. Our results demonstrate previously undescribed and cryptic functional diversity in carbon resource use and growth in fungal endophyte communities ofA.gerardii.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript
- Journal Article:
- https://doi.org/10.3767/persoonia.2022.49.05
