Pisolithus tinctorius, Fungal Extremophile and Modern Analog to an Early Earth Environment; An Unlikely Harbor for Deeply Diverging and Novel Chemoautrophic Microbes

Abstract:

Endosymbioses have given rise to some of the most important innovations in Earth’s history. Indeed, ecological facilitation has been pivotal to the creation of higher order complexity, and in driving evolutionary transitions at every level of organization from cellular organelles to multicellularity. In this study we address a newly discovered endosymbiosis between prokaryotes and a eukaryote growing with no apparent external energy source in soils associated with acid-sulfate hydrothermal springs. Hydrothermal sites are relevant to origin of life because they provide a chemical and energetic environment that may have provided energy for pre-biotic synthesis in the absence of photosynthesis through chemoautotrophy.

Pisolithus (genus, picture 1 below) is a terrestrial fungal extremophile that can grow in thermally altered soils of acid-thermal hot springs at extreme low pH and elevated temperature, thriving in conditions that are beyond the threshold of survivability for most other organisms. Fruiting bodies of this fungus accumulate elemental sulfur into the spore producing tissues (gleba) of the fruiting body. The gleba is encased in a thick peridium, or shell. Further, Pisolithus is capable of enzymatic conversion of elemental S to sulfate. The fruiting bodies are rich in hydrocarbons, contain water through much of their development and are also likely to contain CO₂ from fungal cellular respiration. Further, our data indicate the presence of anaerobic zones within. Thus, the internal environment of Pisolithus contains many conditions relevant to early Earth environments in which life is thought to have originated.

We used 16S rDNA sequences to test the hypothesis that Pisolithus individuals contain novel and/or ancient microbial lineages. Our data reveal lineages comprised of novel relatives of known aerobic and anaerobic chemoautrophic Bacteria (85-90% BLAST search matches), several deeply divergent and novel Bacterial lineages, and a newly discovered lineage that branches at the base of the Archaeal clade indicating the presence of, at the very least, a new Phylum/Division within this group. Thus, the data provide a model for furthering our understanding of the diversification of life, in a novel modern analog to an early Earth environment.