Opening the Gap: Rare Lichens With Rare Cyanobionts – Unexpected Cyanobiont Diversity in Cyanobacterial Lichens of the Order Lichinales

The last decades of research led to a change in understanding of lichens that are now seen as self-sustaining micro-ecosystems, harboring diverse microbial organisms in tight but yet not fully understood relationships. Among the diverse interdependencies, the relationship between the myco- and photobiont is the most crucial, determining the shape, and ecophysiological properties of the symbiotic consortium. Roughly 10% of lichens associate with cyanobacteria as their primary photobiont, termed cyanolichens. Up to now, the diversity of cyanobionts of bipartite lichens resolved by modern phylogenetic approaches is restricted to the filamentous and heterocytous genera of the order Nostocales. Unicellular photobionts were placed in the orders Chroococcales, Pleurocapsales, and Chroococcidiopsidales. However, especially the phylogeny and taxonomy of the Chroococcidiopsidales genera remained rather unclear. Here we present new data on the identity and phylogeny of photobionts from cyanolichens of the genera Gonohymenia, Lichinella, Peccania, and Peltula from a broad geographical range. A polyphasic approach was used, combining morphological and cultivation-depending characteristics (microscopy, staining techniques, life cycle observation, baeocyte motility, and nitrogen fixation test) with phylogenetic analyses of the 16S rRNA and 16S–23S ITS gene region. We found an unexpectedly high cyanobiont diversity in the cyanobacterial lichens of the order Lichinales, including two new genera and seven new species, all of which were not previously perceived as lichen symbionts. As a result, we describe the novel unicellular Chroococcidiopsidales genera Pseudocyanosarcina gen. nov. with the species Pseudocyanosarcina phycocyania sp. nov. (from Peltula clavata, Australia) and Compactococcus gen. nov. with the species Compactococcus sarcinoides sp. nov. (from Gonohymenia sp., Australia) and the new Chroococcidiopsidales species Aliterella compacta sp. nov. (from Peltula clavata, Australia), Aliterella gigantea sp. nov. (from Peltula capensis; South Africa), Sinocapsa ellipsoidea sp. nov. (from Peccania cerebriformis, Austria), as well as the two new Nostocales species Komarekiella gloeocapsoidea sp. nov. (from Gonohymenia sp., Czechia) and Komarekiella globosa sp. nov. (from Lichinella cribellifera, Canary Islands, Spain). Our study highlights the role of cyanolichens acting as a key in untangling cyanobacterial taxonomy and diversity. With this study, we hope to stimulate further research on photobionts, especially of rare cyanolichens.

Vahliellaceae, a new family of cyanobacterial lichens (Peltigerales, Ascomycetes)

The recently described genus Vahliella (Peltigerales, Ascomycetes) has repeatedly appeared outside the Pannariaceae in molecular phylogenies. Here we include data from additional species of the genus and utilize mtSSU rDNA and RPB1 sequences to confirm its placement as the sister to a group consisting of Lobariaceae, Massalongiaceae, Nephromataceae and Peltigeraceae, in the Peltigerales. The new family Vahliellaceae Wedin, P. M. Jørg. & S. Ekman is described for the genus, and its morphological characteristics are briefly discussed.

Massalongiaceae fam. nov., an overlooked monophyletic group among the cyanobacterial lichens (Peltigerales, Lecanoromycetes, Ascomycota)

In this investigation we utilized parsimony and Bayesian analyses of mtSSU and nuLSU rDNA sequence datasets to show that the lichenized ascomycete genera Leptochidium and Polychidium (formerly classified in Placynthiaceae) form a well-supported monophyletic group with Massalongia (Peltigerales, Lecanoromycetes, Ascomycota). This group is also supported by morphological characteristics (ascus type, ascoma ontogeny and anatomy), but does not have a formal name on any level. We describe it here as the family Massalongiaceae. Massalongiaceae is related to a group consisting of Peltigeraceae-Nephromataceae, and Lobariaceae, but the detailed relationships within this group are not resolved with convincing support.

Gregorella, a new genus to accommodate Moelleropsis humida and a molecular phylogeny of Arctomiaceae

The phylogenetic position of the European crustose pioneer lichen Moelleropsis (Biatora) humida (Kullhem) Coppins & P. M. Jørg. is studied using partial sequences of the mitochondrial SSU and nuclear LSU rDNA of 64 ascomycetes, including sequences of all known species of Arctomiaceae. The analysis places M. humida in the Arctomiaceae with strong support as sister to the Tasmanian genus Wawea. The genus Arctomia is monophyletic and sister-group to the Wawea+Moelleropsis humida clade. The new genus Gregorella is described to accommodate Moelleropsis humida and the new combination Gregorella humida (Kullhem) Lumbsch is proposed. The ontogeny of the ascomata of Gregorella humida is similar to that of other Arctomiaceae, in that the generative tissue is formed on a thallus outgrowth. The Arctomiaceae did not cluster with the bulk of cyanobacterial lichens in the Lecanorales suborder Peltigerineae (or Peltigerales), but is part of Ostropomycetidae. The closest relative of Arctomiaceae could not be identified, since the relationships of major clades within Ostropomycetidae lacked support.