An official website of the United States government
Bacterial interactions with animals and plants have been examined for over a century; by contrast, the study of bacterial-fungal interactions has received less attention. Bacteria interact with fungi in diverse ways, and endobacteria that reside inside fungal cells represent the most intimate interaction. The most significant bacterial endosymbionts that have been studied are associated with Mucoromycota and include two main groups: Burkholderia-related and Mycoplasma-related endobacteria (MRE). Examples of Burkholderia-related endobacteria have been reported in the three Mucoromycota subphyla. By contrast, MRE have only been identified in Glomeromycotina and Mucoromycotina. This study aims to understand whether MRE dwell in Mortierellomycotina and, if so, to determine their impact on the fungal host. We carried out a large-scale screening of 394 Mortierellomycotina strains and employed a combination of microscopy, molecular phylogeny, next-generation sequencing and qPCR. We detected MRE in 12 strains. These endosymbionts represent novel bacterial phylotypes and show evidence of recombination. Their presence in Mortierellomycotina demonstrates that MRE occur within fungi across Mucoromycota and they may have lived in their common ancestor. We cured the fungus of its endosymbionts with antibiotics and observed improved biomass production in isogenic lines lacking MRE, demonstrating that these endobacteria impose some fitness costs to their fungal host. Here we provided the first functional insights into the lifestyle of MRE. Our findings indicate that MRE may be antagonistic to their fungal hosts, and adapted to a non-lethal parasitic lifestyle in the mycelium of Mucoromycota. However, context-dependent adaptive benefits to their host at minimal cost cannot not be excluded. Finally, we conclude that Mortierellomycotina represent attractive model organisms for exploring interactions between MRE and fungi.
more »
« less
Comparative genomics of Mollicutes-related endobacteria supports a late invasion into Mucoromycota fungi
Abstract Diverse members of early-diverging Mucoromycota, including mycorrhizal taxa and soil-associated Mortierellaceae, are known to harbor Mollicutes-related endobacteria (MRE). It has been hypothesized that MRE were acquired by a common ancestor and transmitted vertically. Alternatively, MRE endosymbionts could have invaded after the divergence of Mucoromycota lineages and subsequently spread to new hosts horizontally. To better understand the evolutionary history of MRE symbionts, we generated and analyzed four complete MRE genomes from two Mortierellaceae genera:Linnemannia(MRE-L) andBenniella(MRE-B). These genomes include the smallest known of fungal endosymbionts and showed signals of a tight relationship with hosts including a reduced functional capacity and genes transferred from fungal hosts to MRE. Phylogenetic reconstruction including nine MRE from mycorrhizal fungi revealed that MRE-B genomes are more closely related to MRE from Glomeromycotina than MRE-L from the same host family. We posit that reductions in genome size, GC content, pseudogene content, and repeat content in MRE-L may reflect a longer-term relationship with their fungal hosts. These data indicateLinnemanniaandBenniellaMRE were likely acquired independently after their fungal hosts diverged from a common ancestor. This work expands upon foundational knowledge on minimal genomes and provides insights into the evolution of bacterial endosymbionts.
more »
« less
- Award ID(s):
- 1737898
- PAR ID:
- 10463646
- Publisher / Repository:
- Nature Publishing Group
- Date Published:
- Journal Name:
- Communications Biology
- Volume:
- 6
- Issue:
- 1
- ISSN:
- 2399-3642
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Sarrocco, Sabrina (Ed.)Harnessing the plant microbiome has the potential to improve agricultural yields and protect plants against pathogens and/or abiotic stresses, while also relieving economic and environmental costs of crop production. While previous studies have gained valuable insights into the underlying genetics facilitating plant-fungal interactions, these have largely been skewed towards certain fungal clades (e.g. arbuscular mycorrhizal fungi). Several different phyla of fungi have been shown to positively impact plant growth rates, including Mortierellaceae fungi. However, the extent of the plant growth promotion (PGP) phenotype(s), their underlying mechanism(s), and the impact of bacterial endosymbionts on fungal-plant interactions remain poorly understood for Mortierellaceae. In this study, we focused on the symbiosis between soil fungus Linnemannia elongata (Mortierellaceae) and Arabidopsis thaliana (Brassicaceae), as both organisms have high-quality reference genomes and transcriptomes available, and their lifestyles and growth requirements are conducive to research conditions. Further, L . elongata can host bacterial endosymbionts related to Mollicutes and Burkholderia . The role of these endobacteria on facilitating fungal-plant associations, including potentially further promoting plant growth, remains completely unexplored. We measured Arabidopsis aerial growth at early and late life stages, seed production, and used mRNA sequencing to characterize differentially expressed plant genes in response to fungal inoculation with and without bacterial endosymbionts. We found that L . elongata improved aerial plant growth, seed mass and altered the plant transcriptome, including the upregulation of genes involved in plant hormones and “response to oxidative stress”, “defense response to bacterium”, and “defense response to fungus”. Furthermore, the expression of genes in certain phytohormone biosynthetic pathways were found to be modified in plants treated with L . elongata . Notably, the presence of Mollicutes- or Burkholderia- related endosymbionts in Linnemannia did not impact the expression of genes in Arabidopsis or overall growth rates. Together, these results indicate that beneficial plant growth promotion and seed mass impacts of L . elongata on Arabidopsis are likely driven by plant hormone and defense transcription responses after plant-fungal contact, and that plant phenotypic and transcriptional responses are independent of whether the fungal symbiont is colonized by Mollicutes or Burkholderia -related endohyphal bacteria.more » « less
-
Abstract Arbuscular mycorrhizal (AM) fungi are root symbionts that can facilitate plant growth and influence plant communities by altering plant interactions with herbivores. Therefore, AM fungi could be critical for the conservation of certain rare plants and herbivores. For example, North American milkweed species are crucial hosts for monarch butterflies (Danaus plexippus). Understanding how mycorrhizal composition affects milkweeds will have direct impacts on the conservation and restoration of both increasingly threatened guilds. We present data from three studies on the effect of AM fungal composition on milkweed growth, latex production, and establishment. First, we grew seven milkweed species with and without a mixture of native mycorrhizal fungi. We assessed how important fungal composition is to milkweed growth and latex production by growing four milkweed species with seven fungal compositions, as single‐species inoculations with four native fungi, a mixture of native fungi, a single commercial fungus of presumably non‐native origin, and noninoculated controls. Finally, we assessed the field establishment of two milkweed species with and without native mycorrhizal inoculation. Milkweed species grew 98% larger and produced 82% more latex after inoculation with native mycorrhizae. Milkweeds were strongly affected by fungal composition; milkweeds were inhibited by commercial fungi (average of −14% growth) and showed variable but positive responses to native fungal species (average of +3% to +38% biomass). Finally, we found that restoration establishment was dependent on inoculation with native fungi and milkweed species. Overall, our findings indicate that some milkweed species (i.e.,Asclepias syriacaandA. incarnata) are not responsive to mycorrhizal fungal presence or sensitive to mycorrhizal composition while others are, including endangered species (A. meadii) and species of high conservation value (A. tuberosa). We conclude that the reintroduction of native AM fungi could improve the establishment of desirable milkweed species and should be considered within strategies for plantings for monarch conservation.more » « less
-
null (Ed.)Most genomes within the species complex of Fusarium oxysporum are organized into two compartments: the core chromosomes (CCs) and accessory chromosomes (ACs). As opposed to CCs, which are conserved and vertically transmitted to carry out essential housekeeping functions, lineage- or strain-specific ACs are believed to be initially horizontally acquired through unclear mechanisms. These two genomic compartments are different in terms of gene density, the distribution of transposable elements, and epigenetic markers. Although common in eukaryotes, the functional importance of ACs is uniquely emphasized among fungal species, specifically in relationship to fungal pathogenicity and their adaptation to diverse hosts. With a focus on the cross-kingdom fungal pathogen F. oxysporum, this review provides a summary of the differences between CCs and ACs based on current knowledge of gene functions, genome structures, and epigenetic signatures, and explores the transcriptional crosstalk between the core and accessory genomes.more » « less
-
Abstract While the relationship between plant and microbial diversity has been well studied in grasslands, less is known about similar relationships in forests, especially for obligately symbiotic arbuscular mycorrhizal (AM) fungi. To assess the effect of varying tree diversity on microbial alpha- and beta-diversity, we sampled soil from plots in a high-density tree diversity experiment in Minnesota, USA three years after establishment. Three of 12 tree species are AM hosts; the other nine primarily associate with ectomycorrhizal fungi. We used phospho- and neutral lipid fatty acid analysis to characterize the biomass and functional identity of the whole soil bacterial and fungal community and high throughput sequencing to identify the species-level richness and composition of the AM fungal community. We found that plots of differing tree composition had different bacterial and fungal communities; plots with conifers, and especially Juniperus virginiana, had lower densities of several bacterial groups. In contrast, plots with a higher density or diversity of AM hosts showed no sign of greater AM fungal abundance or diversity. Our results indicate that early responses to plant diversity vary considerably across microbial groups, with AM fungal communities potentially requiring longer timescales to respond to changes in host tree diversity.more » « less
