The Lichens' Microbiota, Still a Mystery?

Abstract

Lichens represent self-supporting symbioses, which occur in a wide range of terrestrial habitats and which contribute significantly to mineral cycling and energy flow at a global scale. Lichens usually grow much slower than higher plants. Nevertheless, lichens can contribute substantially to biomass production. This review focuses on the lichen symbiosis in general and especially on the model species Lobaria pulmonaria L. Hoffm., which is a large foliose lichen that occurs worldwide on tree trunks in undisturbed forests with long ecological continuity. In comparison to many other lichens, L. pulmonaria is less tolerant to desiccation and highly sensitive to air pollution. The name-giving mycobiont (belonging to the Ascomycota), provides a protective layer covering a layer of the green-algal photobiont (Dictyochloropsis reticulata) and interspersed cyanobacterial cell clusters (Nostoc spec.). Recently performed metaproteome analyses confirm the partition of functions in lichen partnerships. The ample functional diversity of the mycobiont contrasts the predominant function of the photobiont in production (and secretion) of energy-rich carbohydrates, and the cyanobiont's contribution by nitrogen fixation. In addition, high throughput and state-of-the-art metagenomics and community fingerprinting, metatranscriptomics, and MS-based metaproteomics identify the bacterial community present on L. pulmonaria as a surprisingly abundant and structurally integrated element of the lichen symbiosis. Comparative metaproteome analyses of lichens from different sampling sites suggest the presence of a relatively stable core microbiome and a sampling site-specific portion of the microbiome. Moreover, these studies indicate how the microbiota may contribute to the symbiotic system, to improve its health, growth and fitness.

Keywords: Lobaria pulmonaria; lichen-associated bacteria; lichens; microbiome; omics; symbiosis.

FIGURE 1

Schematic anatomical structure of lichens, with Lobaria pulmonaria as an example. Algae are hosted in a layered fungal scaffold structure delimited by an upper and a lower cortex. Green algae form a layer under the upper cortex. Below the algal layer, a hydrophobic medulla facilitates gas exchange within the thallus. As a tripartite lichen, L. pulmonaria hosts clusters of cyanobacteria inside the thallus in addition to the algae.

FIGURE 2

Lobaria pulmonaria. (A) Specimen growing on Fagus sylvatica (photographed in May 2016 near Viborg, Denmark); (B) Microscopic cross section. The upper cortex forms the habitat of the microbiome. Image produced with dry, sectioned material using a Keyence Digital VHX-5000 microscope with automated image stacking.

FIGURE 3

Distribution map of L. pulmonaria created with ArcGIS 10. Colors indicate the different vegetation zones. Strongly colored areas – general distribution regions. Solid dots – single occurrence spots. Open dots – occurrence not clarified. L. pulmonaria has a worldwide distribution mainly occurring in the Northern Hemisphere.

FIGURE 4

Overview about ‘-omics’ technologies used for lichen microbiome research. Green – metabolomics, yellow – proteomics, blue – transcriptomics, pink – genomics. Colored arrows indicate interactions between metabolome, proteome, transcriptome and genome and how they are affecting each other. Circle sizes illustrate estimated complexity. Gray arrow direction (right hand side) implies an increase.

FIGURE 5

Microbiome and symbiotic partner’s functions in the lichen L. pulmonaria. The mycobiont is responsible for the holobionts’ morphology, mechanical stability and reproduction, protects and supports the photo- and cyanobiont and shapes the microbial community. The photobiont is in charge of the photosynthetic carbon fixation. The cyanobiont is responsible for nitrogen and carbon fixation. The detailed role of the lichenicolous fungi is unclear. The microbiome plays a role in nutrient, vitamin and trace element supply, in resistance to abiotic factors and in antagonizing biotic impact.

FIGURE 6

The main factors affecting the microbiome composition in lichens.