A mechanistic explanation of the transition to simple multicellularity in fungi

Abstract

Development of multicellularity was one of the major transitions in evolution and occurred independently multiple times in algae, plants, animals, and fungi. However recent comparative genome analyses suggest that fungi followed a different route to other eukaryotic lineages. To understand the driving forces behind the transition from unicellular fungi to hyphal forms of growth, we develop a comparative model of osmotrophic resource acquisition. This predicts that whenever the local resource is immobile, hard-to-digest, and nutrient poor, hyphal osmotrophs outcompete motile or autolytic unicellular osmotrophs. This hyphal advantage arises because transporting nutrients via a contiguous cytoplasm enables continued exploitation of remaining resources after local depletion of essential nutrients, and more efficient use of costly exoenzymes. The model provides a mechanistic explanation for the origins of multicellular hyphal organisms, and explains why fungi, rather than unicellular bacteria, evolved to dominate decay of recalcitrant, nutrient poor substrates such as leaf litter or wood.

Syncytia in Fungi

“…Germlings or young colonies can share genetic resources or nutrients through cell fusion, but the process can be restricted as colonies age and undergo hyphal differentiation [ 17 ]. The advantages of interconnected syncytial hyphae lie in their ability to transport nutrients through a continuous cytoplasm, allowing the efficient use of the nutrients once a local source has been exhausted [ 23 ].…”

Fungal taste for minerals: the ectomycorrhizal fungusPaxillus involutustriggers specific genes when extracting potassium from different silicates

“…Many soil environments can be cation-poor and therefore the ability of P. involutus to access K from minerals would give an ecological advantage. Therefore, the fungi might have even evolved specific cellular and metabolic mechanisms [48, 63]. An adaptation of the fungi to low K conditions could help to explain the observed down regulation of many genes in the positive control microcosms experiments.…”

Wood species identity alters dominant factors driving fine wood decomposition along a tree diversity gradient in subtropical plantation forests

“…negative) of tree species diversity on fine wood mass-loss rates in the early decay stage. The bundle approach (i.e., samples in close proximity) in our study might have masked the bidirectional nutrient transfers by cord-forming fungi among different wood substrates, with the net translocation dependent on a source (i.e., high nutrient availability)-sink (i.e., high nutrient demand) relationship (Heaton et al, 2020;Lindahl et al, 2001). Furthermore, invertebrate grazing could be deterministic in shaping fungal translocation processes, driving higher levels of nutrient transfer and mycelial growth into ungrazed patches than in grazed patches (Tordoff et al, 2011).…”