Abstract

Mutualistic interactions between free-living algae and fungi are widespread in nature and are hypothesized to have facilitated the evolution of land plants and lichens. In all known algal-fungal mutualisms, including lichens, algal cells remain external to fungal cells. Here, we report on an algal-fungal interaction in which Nannochloropsis oceanica algal cells become internalized within the hyphae of the fungus Mortierella elongata. This apparent symbiosis begins with close physical contact and nutrient exchange, including carbon and nitrogen transfer between fungal and algal cells as demonstrated by isotope tracer experiments. This mutualism appears to be stable, as both partners remain physiologically active over months of co-cultivation, leading to the eventual internalization of photosynthetic algal cells, which persist to function, grow and divide within fungal hyphae. Nannochloropsis and Mortierella are biotechnologically important species for lipids and biofuel production, with available genomes and molecular tool kits. Based on the current observations, they provide unique opportunities for studying fungal-algal mutualisms including mechanisms leading to endosymbiosis.

Highlights

  • Mutualistic symbioses are defined as those in which partners interact physically and metabolically in mutually beneficial ways

  • After 6 days co-cultivation, scanning electron microscopy (SEM) revealed a wall-to-wall fungal-algal interface between the organisms grown in coculture, (Figure 1C) with the morphology of N. oceanica cells differing from those of cells grown in the absence of fungus

  • Further SEM revealed that the fibrous extensions only were exposed in N. oceanica cells that were in physical contact with live fungal hyphae

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Summary

Introduction

Mutualistic symbioses are defined as those in which partners interact physically and metabolically in mutually beneficial ways. Mutualisms underlie many evolutionary and ecological innovations including the acquisition of plastids and mitochondria, and evolution of symbiotic mutualisms such as mycorrhizas, lichens and corals (Little et al, 2004; Service, 2011; Tisserant et al, 2013; Spribille et al, 2016). An understanding of the underlying principles that govern microbial mutualisms informs microbial ecology and efforts to engineer synthetic microbiomes for biotechnological applications (Egede et al, 2016). Terrestrialization of Earth has been associated with lineages of early diverging fungi belonging to the Mucoromycota. Recent analyses indicate that fungal colonization of land was associated with multiple origins of green algae prior to the origin of embryophytes (Lutzoni et al, 2018)

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