3D biofilms: in search of the polysaccharides holding together lichen symbioses

Abstract

Stable, long-term interactions between fungi and algae or cyanobacteria, collectively known as lichens, have repeatedly evolved complex architectures with little resemblance to their component parts. Lacking any central scaffold, the shapes they assume are casts of secreted polymers that cement cells into place, determine the angle of phototropic exposure and regulate water relations. A growing body of evidence suggests that many lichen extracellular polymer matrices harbor unicellular, non-photosynthesizing organisms (UNPOs) not traditionally recognized as lichen symbionts. Understanding organismal input and uptake in this layer is key to interpreting the role UNPOs play in lichen biology. Here, we review both polysaccharide composition determined from whole, pulverized lichens and UNPOs reported from lichens to date. Most reported polysaccharides are thought to be structural cell wall components. The composition of the extracellular matrix is not definitively known. Several lines of evidence suggest some acidic polysaccharides have evaded detection in routine analysis of neutral sugars and may be involved in the extracellular matrix. UNPOs reported from lichens include diverse bacteria and yeasts for which secreted polysaccharides play important biological roles. We conclude by proposing testable hypotheses on the role that symbiont give-and-take in this layer could play in determining or modifying lichen symbiotic outcomes.

Metagenomic data reveal diverse fungal and algal communities associated with the lichen symbiosis

“…It wasn't until the late twentieth century that in vitro studies began to look at other fungi as potentially lichen-associated organisms rather than mere contaminants (Petrini et al 1990;Crittenden et al 1995;Girlanda et al 1997). It is now apparent that lichens are ecologically complex, internally consistent, and self-sustaining symbiotic phenotypes composed of evolutionarily diverse microbes (Goward 2008;Honegger 1993;Honegger 2001;Spribille et al 2020).…”

The beauty and the yeast: can the microalgae Dunaliella form a borderline lichen with Hortaea werneckii?

“…With increased integration of the fungal-algal interaction and higher specialisation, the criteria of a broderline lichen are thus fulfilled ( Kohlmeyer et al 2004 ). From there, a stepwise transition may have lead to typical lichen symbioses as self-sustaining ecosystems ( Hawksworth and Grube 2020 ), where fungi usually represent the exhabitant partner forming a covering structure of hyphal cells embedded in extracellular polysaccharides ( Grube and Wedin 2016 ; Spribille et al 2020 ). Recent findings showed that the evolutionary success of lichen symbioses may be assisted by the interplay of additional symbionts, (photosynthetic algae, bacteria and yeasts) that co-inhabit the lichen thalli, and potentially contribute to their structural integrity ( Spribille et al 2020 ).…”

Unraveling the sugar code: the role of microbial extracellular glycans in plant–microbe interactions

“…When hydrated, the lichen thallus expands to many times its desiccated volume. The hydrophilic properties of the EPS matrix in the outmost layer account for this effect and determine the point at which surface tension is broken and water is taken up from the environment and retained ( Spribille et al ., 2020 ). Biochemical remodeling of the EPS matrix in desiccation-tolerant lichens is species-specific and seems to play a role in the response to changes in environmental water availability.…”

“…The EPS matrix also acts as substrate for colonization by bacteria and basidiomycetous yeasts commonly found in lichens. As in biofilms, the lichen EPS matrix functions as the main medium by which cell–cell communication between different microbial partners takes place ( Spribille et al ., 2020 ).…”

“…In the few basidiomycete-based lichen symbioses, different cell wall components have been found with linear α-1,3-glucan (pseudonigeran). A comprehensive review of lichen EPSs is provided by Spribille et al . (2020) .…”