Symbiotic Interplay of Fungi, Algae, and Bacteria within the Lung Lichen Lobaria pulmonaria L. Hoffm. as Assessed by State-of-the-Art Metaproteomics

Abstract

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.

Marine cyanolichens from different littoral zones are associated with distinct bacterial communities

“…Several roles of lichen-associated bacteria have been suggested and include nutrient supply (e.g., by nitrogen fixation and phosphate scavenging), nutrient recycling, protection against UV radiation, resistance to abiotic and biotic environmental stressors, and thallus degradation ( Eymann et al, 2017 ). Unlike terrestrial lichens, marine lichens would need to be adapted to much more variable gradients of UV light, salinity (osmotic) stress, heat, desiccation and mechanical stresses from wave action and therefore we would expect the associated bacteria to play a role in resisting these particularly variable conditions.…”

Adaptions of Lichen Microbiota Functioning Under Persistent Exposure to Arsenic Contamination

“…Moreover, various lichen-associated bacteria can provide essential nutrients to the symbiosis ( Sigurbjörnsdóttir et al, 2015 ). These and various other findings related to the composition and functioning of the lichen microbiota contribute to the accumulating evidence that bacteria other than cyanobionts are an essential part of the symbiosis ( Hodkinson and Lutzoni, 2009 ; Cardinale et al, 2012 ; Hodkinson et al, 2012 ; Aschenbrenner et al, 2016 ; Eymann et al, 2017 ). The identified ancillary mechanisms provided by highly abundant and diversified microorganisms contribute to the persistence and longevity of the lichen symbiosis ( Grube et al, 2015 ).…”

“…Such adaptations facilitate persistence of the microbiota and thus might be crucial to preserve symbiosis-relevant functioning (Figure 5 ). By enduring unfavorable conditions in typical lichen habitats, which primarily include high fluctuations in humidity and temperature, the associated bacteria can fulfill their main roles as (i) protectors against biotic and abiotic stresses, (ii) providers of nutrients, vitamins and co-factors, and (iii) detoxifiers of organic and inorganic compounds ( Grube et al, 2015 ; Cernava et al, 2017 ; Eymann et al, 2017 ).…”

Lichen-Associated Bacterium, a Novel Bioresource of Polyhydroxyalkanoate (PHA) Production and Simultaneous Degradation of Naphthalene and Anthracene

“…The metaproteome analysis of L. pulmonaria also supports the hypothesis. Eymann et al [26] established that the functional diversities of the symbionts of L. pulmonaria assist the lichen in longevity.…”

“…Besides the elimination of stress, the lichen-associated microbiomes showed evidence in the detoxification of inorganic and organic matters such as arsenic, copper, and zinc as well as xenobiotic/PAH substances [24,25]. Moreover, a comprehensive proteomic study on lung lichen Lobaria pulmonaria showed that bacterial enzymes identified from L. pulmonaria are responsible for the metabolism of methanol/C1compounds and CO-detoxification [26]. On the other hand, it has been strongly believed that PHA synthesis is one of the survival mechanisms of the bacteria to live in stressful and unstable environments [27].…”