Early Diverging Fungi: Diversity and Impact at the Dawn of Terrestrial Life

Abstract

As decomposers or plant pathogens, fungi deploy invasive growth and powerful carbohydrate active enzymes to reduce multicellular plant tissues to humus and simple sugars. Fungi are perhaps also the most important mutualistic symbionts in modern ecosystems, transporting poorly soluble mineral nutrients to plants and thus enhancing the growth of vegetation. However, at their origin over a billion years ago, fungi, like plants and animals, were unicellular marine microbes. Like the other multicellular kingdoms, Fungi evolved increased size, complexity, and metabolic functioning. Interactions of fungi with plants changed terrestrial ecology and geology and modified the Earth's atmosphere. In this review, we discuss the diversification and ecological roles of the fungi over their first 600 million years, from their origin through their colonization of land, drawing on phylogenomic evidence for their relationships and metabolic capabilities and on molecular dating, fossils, and modeling of Earth's paleoclimate.

High-level classification of the Fungi and a tool for evolutionary ecological analyses

“…Berbee et al (2017) proposed to include Nucleariida and Fonticulida within the extended kingdom Fungi. This is not, however, warranted in our opinion, because these taxa have never been considered as Fungi and the constituent taxa have several unique structural (lack of chitin cell walls, discoid mitochondrial cristae) and ecophysiological (amoeboid habit, phagocytotic nutrition) characters as well as specific features in genomic structure such as the lack of division II Chitin synthase gene (James and Berbee 2012;Torruella et al 2015).…”

On plant defense signaling networks and early land plant evolution

“…But the algal progenitors of land plants would have encountered (terrestrial and/or non-terrestrial) microbes even before this time. Berbee and colleagues [47] recently argued that the occurrence of pectinases (enzymes used for the degradation of pectin in plant cell walls) in even the earliest-diverging fungi [see [48]] argues for the antiquity of the fungal ability to exploit plant material. How so?…”

“…Pectin is a cell wall component characteristic of land plants and streptophyte algae (reviewed in [49]). Berbee et al [47] argue that since pectinase-harboring fungal lineages are older than the land plant clade, these fungi used their pectinases for the degradation of streptophyte algal cell walls. This is corroborated by the fact that i) phytoplankton are readily attacked by chytrid fungi [50] and ii) chytrid fungi have been found associated with streptophyte algal microbiomes [37].…”

Animal origins and the Tonian Earth system

“…the evolution of animal multicellularity) is an evolutionary singularity [19]. In contrast, fungi have obtained complex multicellularity at least two times from unicellular osmotrophs with cell walls [20], and algae have evolved complex multicellularity at least three times from unicellular phototrophs with cell walls [21]. Although the unicellular ancestors of multicellular animals were probably capable of osmotrophy -some choanoflagellates, for instance, can subsist off dissolved organics in culture [22] and in nature [23,24] -flagellates and other protozoa rely primarily on the phagocytosis of other cells for nutrition [25,26].…”

“…The earliest multicellular stem-group metazoans, like modern sponges, most probably retained and relied on this ancestral phagotrophic feeding mode before the advent of gut-bearing animals, which feed osmotrophically at the cellular level and utilize phagocytosis for non-trophic functions, such as programmed cell death and immune defense [6,18,19]. In contrast, multicellular basidiomycetes and ascomycetes, the only other complex multicellular heterotrophs (the other complex multicellular lineages are all phototrophs), evolved directly from obligate osmotrophs with chitinous cell walls [20]. Indeed, the unique trophic and cytological ancestry of animals exemplifies the uniqueness of animal multicellularity and potentially explains why animal-grade multicellularity evolved only once in the history of life [19].…”