Symbioses represent a frequent and successful lifestyle on earth and lichens are one of their classic examples. Recently, bacterial communities were identified as stable, specific and structurally integrated partners of the lichen symbiosis, but their role has remained largely elusive in comparison to the well-known functions of the fungal and algal partners. We have explored the metabolic potentials of the microbiome using the lung lichen Lobaria pulmonaria as the model. Metagenomic and proteomic data were comparatively assessed and visualized by Voronoi treemaps. The study was complemented with molecular, microscopic and physiological assays. We have found that more than 800 bacterial species have the ability to contribute multiple aspects to the symbiotic system, including essential functions such as (i) nutrient supply, especially nitrogen, phosphorous and sulfur, (ii) resistance against biotic stress factors (that is, pathogen defense), (iii) resistance against abiotic factors, (iv) support of photosynthesis by provision of vitamin B 12 , (v) fungal and algal growth support by provision of hormones, (vi) detoxification of metabolites, and (vii) degradation of older parts of the lichen thallus. Our findings showed the potential of lichenassociated bacteria to interact with the fungal as well as algal partner to support health, growth and fitness of their hosts. We developed a model of the symbiosis depicting the functional multi-player network of the participants, and argue that the strategy of functional diversification in lichens supports the longevity and persistence of lichens under extreme and changing ecological conditions.
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.
According to recent research, bacteria contribute as recurrent associates to the lichen symbiosis. Yet, the variation of the microbiomes within species and across geographically separated populations remained largely elusive. As a quite common dispersal mode, lichens evolved vertical transmission of both fungal and algal partners in specifically designed mitotic propagules. Bacteria, if co-transmitted with these symbiotic propagules, could contribute to a geographical structure of lichen-associated microbiomes. The lung lichen was sampled from three localities in eastern Austria to analyse their associated bacterial communities by bar-coded pyrosequencing, network analysis and fluorescence in situ hybridization. For the first time, bacteria were documented to colonize symbiotic propagules of lichens developed for short-distance transmission of the symbionts. The propagules share the overall bacterial community structure with the thalli at class level, except for filamentous Cyanobacteria (Nostocophycideae), and with Alphaproteobacteria as predominant group. All three sampling sites share a core fraction of the microbiome. Bacterial communities of lichen thalli from the same sampling site showed higher similarity than those of distant populations. This variation and the potential co-dispersal of a microbiome fraction with structures of the host organism contribute new aspects to the 'everything is everywhere' hypothesis.
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