Discovery of novel intermediate forms redefines the fungal tree of life

Abstract

Fungi are the principal degraders of biomass in terrestrial ecosystems and establish important interactions with plants and animals. However, our current understanding of fungal evolutionary diversity is incomplete and is based upon species amenable to growth in culture. These culturable fungi are typically yeast or filamentous forms, bound by a rigid cell wall rich in chitin. Evolution of this body plan was thought critical for the success of the Fungi, enabling them to adapt to heterogeneous habitats and live by osmotrophy: extracellular digestion followed by nutrient uptake. Here we investigate the ecology and cell biology of a previously undescribed and highly diverse form of eukaryotic life that branches with the Fungi, using environmental DNA analyses combined with fluorescent detection via DNA probes. This clade is present in numerous ecosystems including soil, freshwater and aquatic sediments. Phylogenetic analyses using multiple ribosomal RNA genes place this clade with Rozella, the putative primary branch of the fungal kingdom. Tyramide signal amplification coupled with group-specific fluorescence in situ hybridization reveals that the target cells are small eukaryotes of 3-5 μm in length, capable of forming a microtubule-based flagellum. Co-staining with cell wall markers demonstrates that representatives from the clade do not produce a chitin-rich cell wall during any of the life cycle stages observed and therefore do not conform to the standard fungal body plan. We name this highly diverse clade the cryptomycota in anticipation of formal classification.

Evolution of a morphological novelty occurred before genome compaction in a lineage of extreme parasites

“…A phylogenetic analysis of 53 conserved concatenated genes supports a topology in which microsporidia is the most basal branch in the fungal tree (5). Another phylogenetic analysis based on 200 genes included the endoparasite Rozella allomycis, a representative of the recently discovered basal fungal lineage Cryptomycota (15,16), and placed microsporidia and Cryptomycota together on the most basal fungal branch (4). One of the shared genomic elements between microsporidia and R. allomycis is the nucleotide transporter that is used by microsporidia for stealing energy in the form of ATP from their hosts; Significance Intracellular obligate parasitism results in extreme adaptations, whose evolutionary history is difficult to understand, because intermediate forms are hardly ever found.…”

Fungal Morphogenesis

“…It seems likely that the cell morphology of ancestral fungi resembled protists (Jones et al 2011), and hyphal growth emerged as the dominant growth form that facilitated the colonization of terrestrial habitats (Stajich et al 2009). Yet, many filamentous fungi also show yeast-like patterns of cellular morphogenesis, particularly during development (Cole and Samson 1979).…”

Lineage-specific molecular probing reveals novel diversity and ecological partitioning of haplosporidians

“…Although this approach is appropriate for many studies, screening a wide range of potential hosts is not generally feasible and is therefore not a good way to estimate the diversity or size of the group. We hypothesised that there are many undetected haplosporidian lineages, as has been demonstrated in free-living protists (Bass and Cavalier-Smith, 2004;Bråte et al, 2010;Howe et al, 2011;Jones et al, 2011). Because haplosporidians are important pathogens with global impacts on aquaculture, it is important to appreciate their diversity, particularly as changing climates and intensifying farming activities may provoke previously non-problematic parasites to emerge, causing outbreaks, high mortalities and threats to aquaculture (Okamura and Feist, 2011).…”