The order Peltigerales (with > 1200 known species and accounting for 9% of all known lichenforming fungi) is one of the three main orders recognized within the largest subclass of the Lecanoromycetes – the Lecanoromycetidae. Interestingly, Peltigera malacea is among the three first lichen-forming species selected for genome sequencing. About 100 species of cyanobacteria and algae, classified in fewer than 40 genera, have been found in lichens. Trebouxia, Trentepohlia (green algae) and Nostoc (cyanobacteria) are the most common. The great majority of lichen-forming fungi species (roughly 85%) are associated with green algae, forming bi-membered lichen symbioses. About 10% of the lichenized fungi are associated exclusively with cyanobacteria (most of which are classified within the order Peltigerales; Fig. 1E-G), and a small portion (3-4%) are associated with both photobionts, forming tri-membered lichen symbioses (many of which are found in the genus Peltigera; Fig. 1A-D).
Because photobiont species are shared among many different mycobiont species, the symbiotic lichen association is named after the mycobiont. For example, the lichen Peltigera canina is the name of the ascomycete species forming this lichen. Photobionts found in lichens have their own taxonomic names. For example, the photobiont associated with Peltigera canina belongs to the cyanobacterial genus Nostoc.
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Fig. 1. A. P. aphthosa – cephalodia (ceph) on the upper surface of the thallus. B. P. leucophlebia. C. P. britannica. D. P. latiloba. E. P. neopolydactyla. F. P. didactyla – laminal whitish soralia (sor). G. P. canina – erect apothecia (pale brown). H. P. membranacea – white veins and white, simple, erect rhizines on thallus lower surface. I. P. venosa – cephalodia (ceph) and brown veins on lower surface of the thallus.
Therefore, lichen sexual reproduction is directly associated with fungal meiosis and formation of ascospores, requiring their re-association with a compatible algal or cyanobacterial partner to form new lichen thalli; i.e., horizontal transmission of the photobiont from generation to generation of lichens. For example, the pale brown disks shown in Fig. 1G are ascomata producing ascospores. Sexual reproduction is the dominant reproduction mode of lichens, however, many lichens can disperse their mycobiont and photobiont simultaneously within specialized asexual propagules (e.g., soredia; Fig. 1F) or through thallus fragmentation; i.e., vertical transmission of the photobiont. Lichens reproducing with these bipartite asexual propagules usually do not reproduce sexually.
Evolutionary Importance
The origin of the Peltigerales is unique in being clearly defined by a switch of photobiont from a green alga to a cyanobacterium as the main photobiont. The acquisition of Nostoc, a photoautotrophic nitrogen-fixing bacterium, as the main photobiont in a specific lineage of the Lecanoromycetidae (Ascomycota) was the key innovation that led to the evolution of more than 1200 species currently known within the monophyletic Peltigerales. O’Brien et al. (2005) have shown that the Nostoc found in peltigeralean lichens are part of the same lineage of Nostoc symbiotically associated with plants and that include some of the free-living Nostoc. As it is the case for lichens in general, most Nostoc haplotypes can associate with multiple peltigeralean species, and the latter are found in association with multiple Nostoc haplotypes throughout their distribution.
However, there are some species of Peltigera that have been found associated with only one Nostoc haplotype, which has never been found other than in association with that specific lichen-forming fungal species. This case of one-to-one reciprocal specificity has also been found for four species of cyanolichens in the Collematineae at an intercontinental scale, and seems to be associated with the vertical transmission of Nostoc from one lichen generation to the next through asexual propagules (Fig. 1F) containing both symbionts.
Photobiont switches also occurred during the evolution of Peltigera, where a bipartite lichen ancestor with Nostoc as the sole photobiont acquired a third symbiont, a green alga (Coccomyxa), which replaced Nostoc as the main photobiont, leaving Nostoc in specialized structures (cephalodia, e.g., Fig. 1A, I) to form tripartite lichens.
The current taxon sampling for Peltigera and level of phylogenetic resolution is insufficient to infer the evolutionary history of these switches from bipartite to tripartite lichen symbiosis with confidence. Reversals from tripartite to bipartite are also expected because a relatively frequent phenomenon in the Peltigerineae is the formation of photomorphs – genetically identical mycobionts forming morphologically different or similar symbioses with different photobionts. Working with Peltigera is advantageous because this dynamic evolutionary process of photobiont switching that is visually tractable is an ideal system for determining the importance and role of coevolution in local adaptation and speciation of the mycobiont. The latter concept is of importance to mycologists working on other fungal-plant symbioses, such as endophytic and mycorrhizal fungi.
Ecological Importance
Most lichens grow slowly and, consequently, their primary productivity contribution is fairly small in many ecosystems. However, the Peltigerineae is notorious for including some of the fastest-growing lichens, forming some of the largest thalli, which can be dominant components of ecosystems where they play an important role in mineral cycling. For example, increases in biomass in the realm of 30-50% in a year have been reported for Peltigera. These lichens greatly contribute to nitrogen cycling in their ecosystems through nitrogen-fixation. For example, in the Pacific Northwest, leaching, particularly of organic forms of N from Peltigera spp., may provide as much as 16 kg N hay-1.
From the estimates of leaching and surface area of Peltigera, a potential contribution of 193 kg N leached/yr to the forests of northeastern Minnesota was calculated. In addition to exogenous atmospheric N contributed by decaying thalli of Peltigera, N leached from healthy tissue is likely vital over time to counter losses of N from volatilization, leaching, and denitrification. The potential zone of influence has been reported to be up to 150 cm for bipartite thalli of Peltigera. Members of the Peltigerinae are well known for their sensitivity to pollution. Peltigera has been found to be very sensitive to oxidizing air pollutants such as ozone. Because of their sensitivity to pollution and destruction of old growth forests through rapid timber harvest cycles, Peltigera species are often included in Red Lists and are under official protection in many countries (e.g., Estonia; Latvia; Austria; and Japan). Because many lichen species within the Peltigerineae have the same ecological requirements, several species are probably threatened by extinction, but have not been recognized as such.