Cytology and molecular phylogenetics of Monoblepharidomycetes provide evidence for multiple independent origins of the hyphal habit in the Fungi

Abstract

The evolution of filamentous hyphae underlies an astounding diversity of fungal form and function. We studied the cellular structure and evolutionary origins of the filamentous form in the Monoblepharidomycetes (Chytridiomycota), an early-diverging fungal lineage that displays an exceptional range of body types, from crescent-shaped single cells to sprawling hyphae. To do so, we combined light and transmission electron microscopic analyses of hyphal cytoplasm with molecular phylogenetic reconstructions. Hyphae of Monoblepharidomycetes lack a complex aggregation of secretory vesicles at the hyphal apex (i.e. Spitzenkörper), have centrosomes as primary microtubule organizing centers and have stacked Golgi cisternae instead of tubular/fenestrated Golgi equivalents. The cytoplasmic distribution of actin in Monoblepharidomycetes is comparable to the arrangement observed previously in other filamentous fungi. To discern the origins of Monoblepharidomycetes hyphae, we inferred a phylogeny of the fungi based on 18S and 28S ribosomal DNA sequence data with maximum likelihood and Bayesian inference methods. We focused sampling on Monoblepharidomycetes to infer intergeneric relationships within the class and determined 78 new sequences. Analyses showed class Monoblepharidomycetes to be monophyletic and nested within Chytridiomycota. Hyphal Monoblepharidomycetes formed a clade sister to the genera without hyphae, Harpochytrium and Oedogoniomyces. A likelihood ancestral state reconstruction indicated that hyphae arose independently within the Monoblepharidomycetes lineage and in at least two other lineages. Cytological differences among monoblepharidalean and other fungal hyphae are consistent with these convergent origins.

Comparative genomics reveals the origin of fungal hyphae and multicellularity

“…16,50,54 . In spite of these intermediate forms, the unicellular dominance in these phyla aligns well with a unicellular ancestry and potential convergent origins of hypha-like structures 17 .…”

“…An alternative hypothesis designates hypha-like connections in the thalli of polycentric chytrid fungi (e.g. Physocladia ) as intermediates to true hyphae 17 . Like chytrids, most Blastocladiomycota form mono-or polycentric, unicellular thalli, although some species form wide, apically growing structures resembling true hyphae (e.g.…”

Complex multicellularity in fungi: evolutionary convergence, single origin, or both?

“…Hyphae are hypothesized to have evolved by the gradual elongation of substrate‐anchoring rhizoids of unicellular ancestors resembling extant Chytridiomycota (Harris, ), although alternative routes may exist in convergently evolved hyphal forms [e.g. Monoblepharidomycetes (Dee et al ., )]. Nevertheless, the evolution of fungal hyphae likely did not involve the modification of cell wall biogenesis for daughter cells to remain together, as seen in filamentous bacteria and algae (Claessen et al ., ; Niklas, ; Herrero, Stavans, & Flores, ) or snowflake yeast (Ratcliff et al ., , ).…”

The Golgi apparatus: insights from filamentous fungi

“…Studies in other Dikarya (such as Coprinopsis cinerea [McLaughlin 1974], Armillaria melea [Grove and Bracker 1970], Aspergillus niger and Verticilium alboatrum [Grove and Bracker 1970] and Neurospora crassa [Girbardt 1969]), although realized before the introduction of freeze-substitution for fixation of hyphae, also had suggested that elements that are not organized in stacks possibly are Golgi bodies. However, using the more distant fungal group of Monoblepharomycetes, it was shown that hyphal growth is not exclusively linked to dispersed Golgi, as hyphae of Monoblepharis macrandra were shown to possess Golgi stacks (Dee et al 2015) (FIG. 1C).…”