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 recognized by macroscopic structures formed by a heterotrophic fungus, the mycobiont, which hosts internal autotrophic photosynthetic algal and/or cyanobacterial partners, referred to as the photobiont. We analyzed the structure and functionality of the entire lung lichen Lobaria pulmonaria L. Hoffm. collected from two different sites by state-of-the-art metaproteomics. In addition to the green algae and the ascomycetous fungus, a lichenicolous fungus as well as a complex prokaryotic community (different from the cyanobacteria) was found, the latter dominated by methanotrophic Rhizobiales. Various partner-specific proteins could be assigned to the different lichen symbionts, for example, fungal proteins involved in vesicle transport, algal proteins functioning in photosynthesis, cyanobacterial nitrogenase and GOGAT involved in nitrogen fixation, and bacterial enzymes responsible for methanol/C1-compound metabolism as well as CO-detoxification. Structural and functional information on proteins expressed by the lichen community complemented and extended our recent symbiosis model depicting the functional multiplayer network of single holobiont partners.1 Our new metaproteome analysis strongly supports the hypothesis (i) that interactions within the self-supporting association are multifaceted and (ii) that the strategy of functional diversification within the single lichen partners may support the longevity of L. pulmonaria under certain ecological conditions.
Global climate change is predicted to alter drought–precipitation patterns, which will likely affect soil microbial communities and their functions, ultimately shifting microbially-mediated biogeochemical cycles. The present study aims to investigate the simultaneous variation of microbial community compositions and functions in response to drought and following rewetting events, using a soil metaproteomics approach. For this, an established field experiment located in an Austrian forest with two levels (moderate and severe stress) of precipitation manipulation was evaluated. The results showed that fungi were more strongly influenced by drying and rewetting (DRW) than bacteria, and that there was a drastic shift in the fungal community towards a more Ascomycota-dominated community. In terms of functional responses, a larger number of proteins and a higher functional diversity were observed in both moderate and severe DRW treatments compared to the control. Furthermore, in both DRW treatments a rise in proteins assigned to “translation, ribosomal structure, and biogenesis” and “protein synthesis” suggests a boost in microbial cell growth after rewetting. We also found that the changes within intracellular functions were associated to specific phyla, indicating that responses of microbial communities to DRW primarily shifted microbial functions. Microbial communities seem to respond to different levels of DRW stress by changing their functional potential, which may feed back to biogeochemical cycles.
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