One Name – One Fungus: The Influence of Photosynthetic Partners on the Taxonomy and Systematics of Lichenized Fungi

Lichens are fungi (mycobionts) that form symbiotic associations with photoautotrophic prokaryotes or eukaryotes (photobionts); however, some species can exchange photosynthetic partners during their lifecycles. This phenomenon modifies the morphology of lichens and consequently influences the taxonomy of lichenized fungi. Here, a few such cases in which the photobionts influenced the taxonomy and systematics of lichenized fungi are reviewed. Two different morphotypes of the same species – known as photomorphs – were classified as different species and sometimes different genera. Moreover, different types of photobionts and the absence or presence (optional lichenization) of an alga in the thallus were believed to be diagnostic characters for discriminating genera. However, the taxonomy and systematics of lichens are based always, according to Article F.1.1. of the International Code of Nomenclature for Algae, Fungi, and Plants, on the fungal partner and only one name is applied.

In general, the morphology of the lichen thallus is shaped by the mycobiont, but in a few genera of filamentous lichens (e.g., Cystocoleus Thwaites or Cyphellostereum D. A. Reid), the thallus structure depends upon the photobiont filaments and the fungal hyphae surrounding them (e.g., Dal-Forno et al., 2013;Hawksworth et al., 2011). However, in some lichen groups with nonfilamentous photobionts, the morphology of the thallus depends upon autotrophic partners, but in a different way. In other words, the switch from one type of photobiont to another changes the morphological traits (anatomic structure, color, and size of the thallus) or even propagation modes (asexual versus sexual reproduction). Sometimes, in such cases, two names were applied to different morphotypes of the same species (e.g., Ertz et al., 2018;Heidmarsson et al., 1997;Jørgensen, 1998;Miadlikowska et al., 2018;Moncada, Coca, & Lücking, 2013;Tønsberg & Goward, 2001). Nevertheless, the taxonomy and systematics of lichens are based always, according to Article F.1.1. of the International Code of Nomenclature for Algae, Fungi, and Plants, on the fungal partner, and only one name can be applied (Turland et al., 2018). In this review, some examples of the influence of shift in photosynthetic partners on the taxonomy of lichenized fungi are presented.
The taxonomy of Sticta is based on numerous morphological characteristics (e.g., type of thallus, color of the lower surface, and development of the tomentum); however, the type of photobiont was typically the first characteristic in keys dividing species into groups (Galloway, 1994(Galloway, , 1997(Galloway, , 1998. This morphology-based taxonomy has obscured the diversity and identity of species, with photomorphs recognized as separate taxa and some of them even placed in different genus, Dendriscocaulon Nyl. (e.g., Galloway, 2001;Magain et al., 2012;Moncada, Coca, & Lücking, 2013;Purvis, 2000;Ranft et al., 2018;Tønsberg & Goward, 2001; see also below).
One of the first discoveries that the same Sticta species can recruit either a green alga or a cyanobacterium was based on morphological and ecological studies. It was found that environmental factors (light and humidity) are crucial to the selection of photobiont type for thallus development. In more humid and sheltered habitats with low illumination, a cyanobiont is preferred over a chlorobiont, which is the photosynthetic component of the thallus in more dry and open habitats. In intermediate conditions, composite thalli are found, i.e., thalli with chlorobionts growing on thalli with cyanobionts (James & Henssen, 1976). These observations were later confirmed by laboratory experiments and molecular data, and several additional pairs of cyanomorphs and chloromorphs were detected and described (e.g., Armaleo & Clerc, 1991;Galloway, 2001;James & Henssen, 1976;Magain et al., 2012;Moncada, Coca, & Lücking, 2013;Purvis, 2000;Ranft et al., 2018;Stocker-Wörgötter, 2002). Moreover, different photobionts can be recruited when the environment changes due to natural disasters, e.g., falling of trees to form open habitats. At a few sites in Bolivia, thalli with cyanobacteria were deteriorating and being overgrown by the attached thalli with green algae (Kukwa,unpublished;Figure 1A).
Symbiosis with two different photobionts may also have chemical consequences. James and Henssen (1976) studied 100 free-living Dendriscocaulon-like thalli using thin-layer chromatography or microcrystal tests and found no lichen secondary metabolites. However, the chloromorph may produce a few lichen substances, e.g., scrobiculin present in the chloromorphs of Ricasolia amplissima (Scop.) De Not. s. l. (for the most recent taxonomy of the species, see Cornejo et al., 2017). The nature of this phenomenon is unknown, but perhaps, the presence of cyanobacteria actively inhibits the production of certain lichen substances (James & Henssen, 1976). Meanwhile, this type of photobiont also alters the products of nitrogen metabolism: Ammonia and amines are produced by cyanomorphs and, when the thallus is wet, are released, emitting fish-like odor (James & Henssen, 1976; see also previous section).

Buellia violacefusca and Lecanographa amylacea -When Two Become One
A single lichen thallus of the same species can contain numerous species or OTUs of closely related photobionts, and different thalli may also be associated with different phylogenetic lineages of photobionts of the same genus (e.g., del Campo et al., 2013;Dal Grande et al., 2017;Friedl, 1987;Guzow-Krzemińska, 2006;Moya et al., 2017;Muggia et al., 2014;Nelsen & Gargas, 2008;Onut , -Brännström et al., 2018). Occasionally, although a lichen recruits photobionts of two closely related green algal genera (Engelen et al., 2010), there are no changes in morphology, reproductive methods, or secondary metabolites. However, the shift in the symbiont from the green algal genus Trebouxia in the class Trebouxiophyceae Friedl to Trentepohlia s. l. in the class Ulvophyceae K. R. Mattox & K. D. Stewart may alter the reproductive mode and phenotypic dimorphism .
Buellia violaceofusca G. Thor & Muhr was described as a sterile, sorediate lichen with blue-brown soralia and green algae as the photobiont. Due to the absence of apothecia, its taxonomic position was unclear, but owing to morphological similarity to Buellia griseovirens (Turner & Borrer ex Sm.), it was tentatively placed in the genus Buellia De Not. (Thor & Muhr, 1991)   . Sequences appeared to be identical to Lecanographa amylacea (Ehrh. ex Pers.) Egea & Torrente, which lacks soredia, but reproduces sexually, forming thalli with a trentepohlioid photobiont that contains large amounts of carotenoid pigments, causing the algae to appear yellow-orange . Buellia violaceofusca and Lecanographa amylacea are conspecific, the latter being the oldest available name for this lichenized fungus . This is a well-documented example of a lichen species recruiting two different green algae of distantly related genera. A switch between these unrelated photosynthetic partners is obviously responsible for thallus dimorphism and has a major impact on the anatomy, morphology, and reproductive strategy of the species. The Trebouxiamorphotype of Lecanographa amylacea is always sterile and sorediate, contrary to its trentepohlioid morphotype, which never produces soredia. When Lecanographa amylacea is fertile, its ascospores can capture Trebouxia algae from other lichens (or perhaps also from free-living, nonlichenized Trebouxia) to form the sorediate thallus, but when trentepohlioid algae are recruited, it develops esorediate, fertile thalli. This flexibility can be considered as a strategy to increase habitat tolerance, which allows the lichen to withstand environmental changes. Examination of numerous specimens revealed that the sorediate component developed when the esorediate morphotype of Lecanographa amylacea grew in proximity to Chrysothrix candelaris (L.) J. R. Laundon; soredia developed in the areas where hyphae of the former invaded the thallus of the latter. Molecular data showed that both species often share the same Trebouxia strain .
Lecanographa amylacea is a rare lichen, but its sorediate morphotype is more common and reported from stands where fertile thalli do not grow (e.g., Kukwa et al., 2012;Poelt, 1994;Thor & Muhr, 1991). This observation indicates that the strategy to recruit two different photobionts and the shift of the reproductive mode can be evolutionarily advantageous. This is the first and thus far the only documented case of a single lichen species recruiting Trebouxia and Trentepohlia s. l. photobionts, which have altered its morphology and reproductive mode. However, by studying sterile sorediate or isidiate lichens of the family Graphidaceae in Bolivia, we found that this phenomenon may exist in a few cases within this group of lichenized fungi. Most members of Graphidaceae form thalli with trentepohlioid photobionts (e.g., Kosecka et al., 2020;Rivas Plata et al., 2010;Staiger, 2002), but in some sterile Bolivian samples of this group, Trebouxiophyceae photobionts were detected using morphological and molecular approaches. However, their fertile photomorph with Trentepholia-like algae have not been found yet. More details will be presented in a forthcoming article.

Ionaspis/Hymenelia complex -Is the Photobiont Not Enough to Distinguish Genera?
The genera Ionaspis Th. Fr. and Hymenelia Kremp. (Hymeneliaceae Körb.) were traditionally separated on the basis of their different photobionts, trentepohlioid or trebouxioid, respectively. However, Eigler (1969) showed heterogeneity within this complex, with some Ionaspis species being more similar to Hymenelia species than to their congeners. Therefore, the distinction of these genera based on the photobiont was questioned by numerous lichenologists (e.g., Eigler, 1969;Jørgensen, 1989;Lutzoni & Brodo, 1995). By employing cladistic analyses of morphological, anatomical, and allozyme data, Lutzoni and Brodo (1995) reviewed North American taxa within the Ionaspis/Hymenelia complex and reclassified some species. They treated the photobiont as a minor character and separated these two genera on the basis of differences in epihymenial pigments, ascospore width, and hymenium thickness (Lutzoni & Brodo, 1995). Although their new classification is generally accepted, the distinction between these two genera was claimed to be practically difficult and artificial compared to the photobiont-based classification, and the need for morphological and molecular revisions of these taxa was thus highlighted (Fryday & McCarthy, 2018;Kantvilas, 2014). However, this complex has not been studied in more detail using DNA data, with the exception of a study based on limited sampling from Alaska, which showed that this group of lichens warrants further investigation (McCune et al., 2018).

Stictidaceae and Optional Lichenization
The family Stictidaceae Fr. comprises 28 genera (Wijayawardene et al., 2020) of lichenized, lichenicolous, and saprotrophic fungi (e.g., Diederich et al., 2018;Wedin et al., 2004Wedin et al., , 2005Wedin et al., , 2006. This also includes the genus Stictis Pers., which originally comprised epixylic, nonlichenized saprotrophic fungi (Wedin et al., 2004(Wedin et al., , 2005(Wedin et al., , 2006. However, molecular data also placed species of the former Conotrema Tuck., which are lichenized and epiphytic fungi, within the genus Stictis (Wedin et al., 2004(Wedin et al., , 2005(Wedin et al., , 2006. Although such a situation is not an exception in fungi, it is remarkable in this case. Using molecular markers, Wedin et al. (2004Wedin et al. ( , 2005Wedin et al. ( , 2006 discovered that neither the genera nor the species are monophyletic. Moreover, the same species, depending on the substrate (bark or wood), either formed a lichenized Conotrema-like thallus or lived as a saprotroph without symbiotic algae (Stictis-like thallus) and completed its lifecycle. The phenomenon that a single species can exist as a lichen or a saprotroph is called optional lichenization (Wedin et al., 2004(Wedin et al., , 2005(Wedin et al., , 2006. Individuals of Stictis species that can form lichenized and nonlichenized thalli differ in their morphology. Ascomata of both forms are very similar, but as saprotrophs, they have generally more heavily pigmented ascomatal walls and are more exposed on the substrate. Additionally, individuals living in symbiosis with algae form highly visible, whitish, lichenized thalli on tree barks, whereas thalli of individuals lacking photobionts are less evident, completely immersed in the substratum and only their ascomata are visible. A very similar situation, with two nutritional modes (lichenized and saprotrophic), is also known in another member of Stictidaceae: Schizoxylon albescens Gilenstam, H. Döring & Wedin (Fernández-Brime et al., 2019;Wedin et al., 2006).
Optional lichenization may play important roles in the evolution of Stictidaceae, representing an advantageous adaptive strategy allowing the species to grow on different substrates. It enables the species to colonize tree barks (mostly Populus tremula) when there is no lignum available for the nonlichenized form in the habitat or when the lignum is already present but the host trees are too young for colonization of the lichenized form (Wedin et al., 2004). Moreover, species with two different nutritional modes may be more common and widespread than species lacking this potential (Wedin et al., 2004(Wedin et al., , 2006.