Reciprocal Informants: Using Fungal Bioinformatics, Genomics, and Ecology to tie Mechanisms to Ecosystems

Abstract

Across both wild and human-structured ecosystems, fungi interact with every plant species on earth. From mycorrhizal mutualisms, harmless endophytes, and deadly pathogens, the results of these interactions can mean the difference between a plant’s ability to grow and flourish, or languish and expire. Fungal-host dynamics are not static traits, either over evolutionarily time or during the lifetime of individuals where ecological context dependency shapes the outcomes of fungal-host interactions. Understanding the ecological and genetic factors that structure plant-fungal relationships has wide ranging consequences for ecosystems, agro-ecosystems, and human health. However, it’s not well understood how complex genetic mechanisms and ecological pressures work in concert to structure the outcomes of fungal-host interactions, particularly among fungal mutualists. This dissertation contributes to this understanding by investigating how fungal-host relationships are regulated at two levels: broadly, investigating the ecology of fungal-host systems, and specifically, investigating the genetic and genomic basis of how these interactions are mediated. I begin Chapter 1 from the perspective of fungal ecology, investigating the influence of neighborhood (the surrounding plant community) on host specificity patterns using the host-specialist ectomycorrhizal (ECM) genus Suillus. The number of host species that a given fungal species will associate with, and how closely related these host species are, is the study of fungal host specificity. While some fungi associate with only a single species of host (high host specificity), most associate with tens or hundreds of host species (low host specificity). Fungi in the genus Suillus are famous for their high host specificity, primarily associating with plants in the family Pineaceae (particularly White Pines, Red Pines and Larchs). Using a combination of field sampling, sequencing, and colonization bioassays, I present evidence that one species, S. subaureus, has undergone a novel host-expansion onto Angiosperms, and argue that neighborhood effects influence ECM colonization outcomes over both space and time. In Chapter 2, I expand from fungal ecology into fungal genomes. Using genome mining and comparative genomics, I look for signatures of ECM host specificity using 19 genome sequenced Suillus species in relation to 1) other (non-Suillus) ECM fungi and 2) an intrageneric comparison between Suillus that specialize on Red Pine, White Pine or Larch. I present evidence for the involvement of several molecular classes in regulating Suillus host specificity including species specific small secreted proteins, G-protein coupled receptors, and terpene secondary metabolites. Finally, in Chapter 3, I use the genomic and bioinformatic tool sets developed in Chapters 1 and 2, to expand my analysis across the fungal phylogeny and ask questions about a potential molecular correlate of fungal guild and trophic mode: ribosomal DNA (rDNA) copy number. To do this, I developed a bioinformatic pipeline to estimate rDNA copy number variation from whole genome sequence data, and applied it to a phylogenetically and ecologically diverse set of 91 fungal genomes. I present evidence that rDNA copy number is inversely associated phylogenetic distance, but displays a high level of variation, spanning an order of magnitude in Suillus alone, with no detectable correlation to guild occupation or genome size. Taken together, the work presented here shows that genomic and bioinformatic approaches used in concert with classical ecological methodologies, offer great potential to expand our understanding of the two-way influence of ecosystem-level processes and gene-level mechanisms in structuring plant-fungal interactions.