Lichen algae: the photosynthetic partners in lichen symbioses

A review of algal (including cyanobacterial) symbionts associated with lichen-forming fungi is presented. General aspects of their biology relevant to lichen symbioses are summarized. The genera of algae currently believed to include lichen symbionts are outlined; approximately 50 can be recognized at present. References reporting algal taxa in lichen symbiosis are tabulated, with emphasis on those published since the 1988 review by Tschermak-Woess, and particularly those providing molecular evidence for their identifications. This review is dedicated in honour of Austrian phycologist Elisabeth Tschermak-Woess (1917–2001), for her numerous and significant contributions to our knowledge of lichen algae (some published under the names Elisabeth Tschermak and Liesl Tschermak).

Towards a Systems Biology Approach to Understanding the Lichen Symbiosis: Opportunities and Challenges of Implementing Network Modelling

Lichen associations, a classic model for successful and sustainable interactions between micro-organisms, have been studied for many years. However, there are significant gaps in our understanding about how the lichen symbiosis operates at the molecular level. This review addresses opportunities for expanding current knowledge on signalling and metabolic interplays in the lichen symbiosis using the tools and approaches of systems biology, particularly network modelling. The largely unexplored nature of symbiont recognition and metabolic interdependency in lichens could benefit from applying a holistic approach to understand underlying molecular mechanisms and processes. Together with ‘omics’ approaches, the application of signalling and metabolic network modelling could provide predictive means to gain insights into lichen signalling and metabolic pathways. First, we review the major signalling and recognition modalities in the lichen symbioses studied to date, and then describe how modelling signalling networks could enhance our understanding of symbiont recognition, particularly leveraging omics techniques. Next, we highlight the current state of knowledge on lichen metabolism. We also discuss metabolic network modelling as a tool to simulate flux distribution in lichen metabolic pathways and to analyse the co-dependence between symbionts. This is especially important given the growing number of lichen genomes now available and improved computational tools for reconstructing such models. We highlight the benefits and possible bottlenecks for implementing different types of network models as applied to the study of lichens.

The Lichens’ Microbiota, Still a Mystery?

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.

In vitro resynthesis of lichenization reveals the genetic background of symbiosis-specific fungal-algal interaction in Usnea hakonensis

Background Symbiosis is central to ecosystems and has been an important driving force of the diversity of life. Close and long-term interactions are known to develop cooperative molecular mechanisms between the symbiotic partners and have often given them new functions as symbiotic entities. In lichen symbiosis, mutualistic relationships between lichen-forming fungi and algae and/or cyanobacteria produce unique features that make lichens adaptive to a wide range of environments. Although the morphological, physiological, and ecological uniqueness of lichens has been described for more than a century, the genetic mechanisms underlying this symbiosis are still poorly known. Results This study investigated the fungal-algal interaction specific to the lichen symbiosis using Usnea hakonensis as a model system. The whole genome of U. hakonensis, the fungal partner, was sequenced by using a culture isolated from a natural lichen thallus. Isolated cultures of the fungal and the algal partners were co-cultured in vitro for 3 months, and thalli were successfully resynthesized as visible protrusions. Transcriptomes of resynthesized and natural thalli (symbiotic states) were compared to that of isolated cultures (non-symbiotic state). Sets of fungal and algal genes up-regulated in both symbiotic states were identified as symbiosis-related genes. Conclusion From predicted functions of these genes, we identified genetic association with two key features fundamental to the symbiotic lifestyle in lichens. The first is establishment of a fungal symbiotic interface: (a) modification of cell walls at fungal-algal contact sites; and (b) production of a hydrophobic layer that ensheaths fungal and algal cells;. The second is symbiosis-specific nutrient flow: (a) the algal supply of photosynthetic product to the fungus; and (b) the fungal supply of phosphorous and nitrogen compounds to the alga. Since both features are widespread among lichens, our result may indicate important facets of the genetic basis of the lichen symbiosis.

In vitro resynthesis of lichenization reveals the genetic background of symbiosis-specific fungal-algal interaction in Usnea hakonensis.

Background: Symbiosis is central to ecosystems and has been an important driving force of the diversity of life. Close and long-term interactions are known to develop cooperative molecular mechanisms between the symbiotic partners and have often given them new functions as symbiotic entities. In lichen symbiosis, mutualistic relationships between lichen-forming fungi and algae and/or cyanobacteria produce unique features that make lichens adaptive to a wide range of environments. Although the morphological, physiological, and ecological uniqueness of lichens has been described for more than a century, the genetic mechanisms underlying this symbiosis are still poorly known.Results: This study investigated the fungal-algal interaction specific to the lichen symbiosis using Usnea hakonensis as a model system. The whole genome of U. hakonensis, the fungal partner, was sequenced by using a culture isolated from a natural lichen thallus. Isolated cultures of the fungal and the algal partners were co-cultured in vitro for three months, and thalli were successfully resynthesized as visible protrusions. Transcriptomes of resynthesized and natural thalli (symbiotic states) were compared to that of isolated cultures (non-symbiotic state). Sets of fungal and algal genes up-regulated in both symbiotic states were identified as symbiosis-related genes.Conclusion: From predicted functions of these genes, we identified genetic association with two key features fundamental to the symbiotic lifestyle in lichens. The first is establishment of a fungal symbiotic interface: (a) modification of cell walls at fungal-algal contact sites; and (b) production of a hydrophobic layer that ensheaths fungal and algal cells;. The second is symbiosis-specific nutrient flow: (a) the algal supply of photosynthetic product to the fungus; and (b) the fungal supply of phosphorous and nitrogen compounds to the alga. Since both features are widespread among lichens, our result may indicate important facets of the genetic basis of the lichen symbiosis.