Evolution of organismal composition and architecture in self-assembling fungal symbioses

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Most forms of multicellular, multi-domain symbiosis recognized today involve large, structurally defining hosts dependent on microbial partners. Some symbioses, by contrast, possess body plans that are only achieved with all-microscopic symbionts. This is the case with lichens, symbiotic architectures based on interplay between a fungal and a photosynthesizing partner, usually single-celled algae or cyanobacteria. The partners are the microscopic equivalent of string (fungal hyphae) and balls (unicellular algae), and unable to form lichens on their own. The macroscopic architecture is effected by the gluing together of partner cells by extracellular polymers in specific motifs, essentially 3D biofilms. However, the cells along the “string” have interconnected cytoplasms and the “balls” are ostensibly autonomous. How they form a macroscopic lichen with conserved patterns and dimensions is unknown.******My research uses modern tools to stress-test some of the most basic assumptions of lichen biology, assumptions that have been essentially unchallenged for 150 years. Application of shotgun DNA-, RNA- and protein sequencing has revealed that the core organismal assemblage found in a single lichen is invariably more than the twosome presented in textbooks. Additional fungi as well as bacteria appear to be constant components. However, identifying the functions of the previously overlooked microbes in turn requires revisiting our basic understanding of the lichen body plan and the glue that holds it together. My DG is dedicated to three main goal areas that aim to significantly close these knowledge gaps:******How do core symbionts change across lichen architectures? I will use metagenomics to map changes in core symbionts over the evolution of an architecturally diverse group of lichens. I will compare individual genomes to understand how gene families changed along with the lichen in which the symbiont occurs. Finally, I will use confocal laser microscopy to visualize the symbionts in situ.******What is the extracellular matrix that holds lichen symbionts in place? I will investigate extracellular polymer composition using specific staining approaches used in study biofilms, as well as targeted sampling of the matrix proteome and glycome.******Which core symbionts contribute to this forming this layer? I will leverage our knowledge of biosynthetic pathways for lichen secondary metabolites to visualize which players are engaged in incorporating isotope-labeled precursors and producing these metabolites. Together with my parallel goal areas, this will be a powerful method of directly tying genomes to the goods and services pool of the total symbiont assemblage.******The methods and approaches I am developing are at directly relevant to understanding complex eukaryote-prokaryote biofilm systems. My focus on cracking the give and take in this complex system will provide inroads for understanding other symbiotic systems that interact in biofilm-like contexts.**