A Phylogenetic Estimation of Trophic Transition Networks for Ascomycetous Fungi: Are Lichens Cradles of Symbiotrophic Fungal Diversification?

Abstract

Fungi associated with photosynthetic organisms are major determinants of terrestrial biomass, nutrient cycling, and ecosystem productivity from the poles to the equator. Whereas most fungi are known because of their fruit bodies (e.g., saprotrophs), symptoms (e.g., pathogens), or emergent properties as symbionts (e.g., lichens), the majority of fungal diversity is thought to occur among species that rarely manifest their presence with visual cues on their substrate (e.g., the apparently hyperdiverse fungal endophytes associated with foliage of plants). Fungal endophytes are ubiquitous among all lineages of land plants and live within overtly healthy tissues without causing disease, but the evolutionary origins of these highly diverse symbionts have not been explored. Here, we show that a key to understanding both the evolution of endophytism and the diversification of the most species-rich phylum of Fungi (Ascomycota) lies in endophyte-like fungi that can be isolated from the interior of apparently healthy lichens. These "endolichenic" fungi are distinct from lichen mycobionts or any other previously recognized fungal associates of lichens, represent the same major lineages of Ascomycota as do endophytes, largely parallel the high diversity of endophytes from the arctic to the tropics, and preferentially associate with green algal photobionts in lichen thalli. Using phylogenetic analyses that incorporate these newly recovered fungi and ancestral state reconstructions that take into account phylogenetic uncertainty, we show that endolichenism is an incubator for the evolution of endophytism. In turn, endophytism is evolutionarily transient, with endophytic lineages frequently transitioning to and from pathogenicity. Although symbiotrophic lineages frequently give rise to free-living saprotrophs, reversions to symbiosis are rare. Together, these results provide the basis for estimating trophic transition networks in the Ascomycota and provide a first set of hypotheses regarding the evolution of symbiotrophy and saprotrophy in the most species-rich fungal phylum. [Ancestral state reconstruction; Ascomycota; Bayesian analysis; endolichenic fungi; fungal endophytes; lichens; pathogens; phylogeny; saprotrophy; symbiotrophy; trophic transition network.].

Coral-associated marine fungi form novel lineages and heterogeneous assemblages

“…For this reason, the fact that many of the fungi detected in our study belong to clades of parasitic fungi, including plant pathogenic fungi such as Pleosporaceae and dermatophytes such as Malassezia, may not necessarily indicate parasitism in this particular environmental context. Lichenic symbioses, for example, show evidence of repeated shifts from symbiosis to pathogen (Arnold et al, 2009), and mutation in a single gene has been shown to convert a plant endosymbiotic fungus from a mutualist to a parasite (Takemoto et al, 2006).…”

Endolichenic fungi: the lesser known fungal associates of lichens

“…The endolichenic fungi are akin to the endophytic fungi of vascular plants in many aspects; they occur internally in the lichens, do not produce any visible disease symptoms and are transmitted horizontally (Arnold et al 2009; Kannangara et al 2009; U’Ren et al 2012). Furthermore, like the endophytic fungi, they produce an array of secondary metabolites such as alkaloids, quinones, furanones, pyrones, benzopyranoids, xanthones, terpenes, steroids, peptides and allycylic compounds (Paranagama et al 2007; He et al 2012; Yang et al 2012, 2016; Li et al 2015; Samanthi et al 2015; Kellogg and Raja 2016; Yuan et al 2016).…”

“…These metabolites exhibit many novel bioactivities including antibacterial, antifungal, cytotoxic and antioxidant activities (Kellogg and Raja 2016; Suryanarayanan et al 2017). All lichens, from the Arctic to the tropics, studied for their endolichenic fungi have been shown to harbour these fungi (Arnold et al 2009; Suryanarayanan et al 2005, 2017; Li et al 2007; Kannangara et al 2009; Tripathi and Joshi 2015) (Table 1). As only a tiny fraction of the estimated 18,500 lichen species (Nash 2008) has been studied for their endolichenic fungal assemblages, information regarding this ecological group of fungi is limited (Tripathi et al 2014).…”

“…Endolichenic fungi belong to the major lineages of Ascomycota to which the endophytic fungi of plants also belong (Arnold et al 2009). They are distinct from the other fungal associates of lichen, namely the mycobiont (Lutzoni and Miadlikowska 2009) and the lichenicolous fungi associated with the lichens (Arnold et al 2009). A molecular study by U’Ren et al (2010) confirms that endolichenic fungi are a distinct ecological group and are not accidental colonisers of lichens.…”

“…The endolichenic fungi are closely associated with the photobiont of the lichen. It is suggested that such an association could have led to the evolution of plant endophytes (Arnold et al 2009). However, it appears that endolichenic fungi are distinct from the current endophytic fungi harboured by plants (U’Ren et al 2012; Zhang et al 2015).…”