Understanding Microbial Multi-Species Symbioses

Abstract

Lichens are commonly recognized as a symbiotic association of a fungus and a chlorophyll containing partner, either green algae or cyanobacteria, or both. The fungus provides a suitable habitat for the partner, which provides photosynthetically fixed carbon as energy source for the system. The evolutionary result of the self-sustaining partnership is a unique joint structure, the lichen thallus, which is indispensable for fungal sexual reproduction. The classical view of a dual symbiosis has been challenged by recent microbiome research, which revealed host-specific bacterial microbiomes. The recent results about bacterial associations with lichens symbioses corroborate their notion as a multi-species symbiosis. Multi-omics approaches have provided evidence for functional contribution by the bacterial microbiome to the entire lichen meta-organism while various abiotic and biotic factors can additionally influence the bacterial community structure. Results of current research also suggest that neighboring ecological niches influence the composition of the lichen bacterial microbiome. Specificity and functions are here reviewed based on these recent findings, converging to a holistic view of bacterial roles in lichens. Finally we propose that the lichen thallus has also evolved to function as a smart harvester of bacterial symbionts. We suggest that lichens represent an ideal model to study multi-species symbiosis, using the recently available omics tools and other cutting edge methods.

Keywords: Alphaproteobacteria host-associated bacteria; lichens; microbiome; symbiosis.

FIGURE 1

A holistic view of the lichen microbiome diversity and identified functions in the environmental context. Lichen-associated bacterial communities were shown to share substantial fractions of identified taxa with adjacent microhabitats (blue circle). This suggests a dynamic acquisition and exchange of beneficial species. Specific proportions of the microbiome are vertically transmitted to the next generation and used for the establishment of novel populations (red circle and arrows). Highly diverse bacterial populations primarily colonize outer lichen layers, but some can also enter the inter-hyphal matrix (green circle). External factors provide a shared microbial ‘core assembly’ of the habitat, but host-specific factors (gray circle) determine the lichen-specific bacterial community, which contributes a variety of beneficial functions for the host symbiosis (purple circle).