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Tagirdzhanova, G.

Publications and source records attributed to Tagirdzhanova, G..

7 recordsLinked to original sources

Tangerine: a Starship-like element in the genomes of Xanthoria lichen-forming fungi

Lichens are symbiotic associations between filamentous fungi and photosynthetic micro-organisms, such as green algae and/or cyanobacteria, that result in a single anatomically-complex structure that can thrive in environments inhospitable to most organisms, including arctic tundra, high mountains, and deserts. Recent evidence suggests that lichens may be even more complex than previously appreciated, containing multiple microbial constituents, but how genomes of the principal fungal symbiont (which provides the majority of biomass in lichen tissue) have been shaped during evolution is largely unexplored. Recently, giant transposable elements called Starships have been found in many genomes of filamentous fungi, but to which extent they occur in lichen-forming fungi is not known. In this report, we describe a Starship element from the lichen fungus Xanthoria parietina. This element, named Tangerine, contains several genes that have signatures of horizontal gene transfer from non-lichen-forming fungi, most likely from black yeasts of the Chaetothyriales, that are often lichen-associated. Repetitive sequences carried by Tangerine, and found in other sites in Xanthoria genomes, are affected by repeat-induced point mutation (RIP), a mechanism of genome defense against transposable elements, consistent with fungal sexual reproduction which always precedes new lichen formation by Xanthoria. Tangerines "captain" belongs to a newly defined family of tyrosine recombinases specific to lichen-forming Lecanoromycetes. Several other captain clades have signatures of horizontal gene transfer between distantly related lichen-forming fungi and non-mycobiont lichen-associated fungi. We speculate that Starships may play a significant, yet hitherto unrecognized role, in lichen genome evolution and provide a roadmap for further investigation.

genomics↗

Chromosome-level genome assembly of the photobiont alga Trebouxia sp. 'A48' from Xanthoria parietina provides new insight into the lichen symbiosis

O_LILichens are symbiotic assemblies consisting of multiple organisms, chiefly a fungus and a photosynthetic microorganism or the photobiont. Among diverse photobionts, the most prevalent is the chlorophyte alga Trebouxia. C_LIO_LIWe produced a chromosome-level assembly of Trebouxia sp. A48, a photobiont of Xanthoria parietina. The genome was assembled into 20 contigs, of which 16 had telomeric repeats on both ends and likely represent complete chromosomes. We compared the genome to genomes of other Trebouxia species and analyzed it to investigate the biology of the species, including its lifecycle and adaptations to lichen lifestyle. C_LIO_LITrebouxia sp. A48 genome is haploid and encodes genes involved in sexual reproduction and meiosis. The predicted secretome is enriched in hydrolases and redox enzymes and contains carbohydrate-binding proteins potentially involved in cell-to-cell recognition and adhesion. We identified genes potentially involved in carbon concentrating and confirmed two instances of ancient horizontal gene transfer from fungi. C_LIO_LIThe genome and the strain of Trebouxia sp. A48 are available for the community for research on algal evolution and lichen symbiosis. C_LI

genomics↗

Multipartite complexity of the lichen symbiosis revealed by metagenome and transcriptome analysis of Xanthoria parietina

Lichens are composite symbiotic associations of fungi, algae, and bacteria that result in large, anatomically complex organisms adapted to many of the worlds most challenging environments. How such intricate, self-replicating lichen architectures develop from simple microbial components remains unknown because of their recalcitrance to experimental manipulation. Here we report a metagenomic and metatranscriptomic analysis of the lichen Xanthoria parietina at different developmental stages. We identified 168 genomes of symbionts and lichen-associated microbes within a lichen thallus, including representatives of green algae, three different classes of fungi, and 14 bacterial phyla. By analyzing occurrence of individual species across lichen thalli from diverse environments, we defined both substrate-specific and core microbial components of the lichen. Meta-transcriptomic analysis of the principal fungal symbiont from three different developmental stages of a lichen, compared to axenically grown fungus, revealed differential gene expression profiles indicative of lichen-specific transporter functions, specific cell signalling, transcriptional regulation and secondary metabolic capacity. Putative immunity-related proteins and lichen-specific structurally conserved secreted proteins resembling fungal pathogen effectors were also identified, consistent with a role for immunity modulation in lichen morphogenesis.

bioinformatics↗

Genomic analysis of Coccomyxa viridis, a common low-abundance alga associated with lichen symbioses

Lichen symbiosis is centered around a relationship between a fungus and a photosynthetic microbe, usually a green alga. In addition to their main photosynthetic partner (the photobiont), lichen symbioses can contain additional algae present in low abundance. The biology of these algae and the way they interact with the rest of lichen symbionts remains largely unknown. Here we present the first genome sequence of a non-photobiont lichen-associated alga. Coccomyxa viridis was unexpectedly found in 12% of publicly available lichen metagenomes. With few exceptions, members of the Coccomyxa viridis clade occur in lichens as non-photobionts, potentially growing in thalli endophytically. The 45.7 Mbp genome of C. viridis was assembled into 18 near chromosome-level contigs, making it one of the most contiguous genomic assemblies for any lichen-associated algae. Comparing the C. viridis genome to its close relatives revealed the presence of traits associated with the lichen lifestyle. The genome of C. viridis provides a new resource for exploring the evolution of the lichen symbiosis, and how symbiotic lifestyles shaped evolution in green algae.

microbiology↗

Evidence for a core set of microbial lichen symbionts from a global survey of metagenomes

Lichens are the archetypal symbiosis and the one for which the term was coined. Although application of shotgun sequencing techniques has shown that many lichen symbioses can harbour more symbionts than the canonically recognized fungus and photobiont, no global census of lichen organismal composition has been undertaken. Here, we analyze the genome content of 437 lichen metagenomes from six continents, and show that four bacterial lineages occur in the majority of lichen symbioses, at a frequency on par with algal photobionts. A single bacterial genus, Lichenihabitans, occurs in nearly one-third of all lichens sampled. Genome annotations from the most common lichen bacterial symbionts suggest they are aerobic anoxygenic photoheterotrophs and produce essential vitamins, but do not fix nitrogen. We also detected secondary basidiomycete symbionts in about two-thirds of analyzed metagenomes. Our survey suggests a core set of four to seven microbial symbionts are involved in forming and maintaining lichen symbioses.

microbiology↗

Large differences in carbohydrate degradation and transport potential in the genomes of lichen fungal symbionts

Lichen symbioses are generally thought to be stabilized by the transfer of fixed carbon compounds from a photosynthesizing unicellular symbiont to a fungus. In other fungal symbioses, carbohydrate subsidies correlate with genomic reductions in the number of genes for plant cell wall-degrading enzymes (PCWDEs), but whether this is the case with lichen fungal symbionts (LFSs) is unknown. We predicted genes encoding carbohydrate-active enzymes (CAZymes) and sugar transporters in 17 existing and 29 newly sequenced genomes from across the class Lecanoromycetes, the largest extant clade of LFSs. Despite possessing lower mean numbers of PCWDE genes compared to non-symbiont Ascomycota, all LFS genomes possessed a robust suite of predicted PCWDEs. The largest CAZyme gene numbers, on par with model species such as Penicillium, were retained in genomes from the subclass Ostropomycetidae, which are found in crust lichens with highly specific ecologies. The lowest numbers were in the subclass Lecanoromycetidae, which are symbionts of many generalist macrolichens. Our results suggest that association with phototroph symbionts does not in itself result in functional loss of PCWDEs and that PCWDE losses may have been driven by adaptive processes within the evolution of specific LFS lineages. The inferred capability of some LFSs to access a wide range of carbohydrates suggests that some lichen symbioses may augment fixed CO2 with carbon from external sources. SignificanceLichen symbioses are considered self-contained autotrophic systems in which the total carbon economy is the sum of phototroph-fixed CO2, supplied to a fungus as sugars. In other fungal-plant symbioses, such as mycorrhizae, plant-derived sugar subsidies are associated with loss of plant cell wall-degrading enzymes (PCWDEs). We compared PCWDE inventories in 46 genomes from the largest group of lichen fungal symbionts (LFSs) with non-symbionts from across Ascomycota. We found that despite lower overall gene numbers, all LFSs retain PCWDEs, and some possess gene numbers and functional diversity on par with non-symbionts. Our results suggest that association with a phototroph does not necessarily result in PCWDE loss, and some lichens may obtain carbon from sources other than CO2 fixation.

genomics↗

Lichen fungi do not depend on the alga for ATP production

Lichen fungi live in a symbiotic association with unicellular phototrophs and have no known aposymbiotic stage. A recent study postulated that some of them have lost mitochondrial oxidative phosphorylation and rely on their algal partners for ATP. This claim originated from an apparent lack of ATP9, a gene encoding one subunit of ATP synthase, from a few mitochondrial genomes. Here we show that while these fungi indeed have lost the mitochondrial ATP9, each retain a nuclear copy of this gene. Our analysis reaffirms that lichen fungi produce their own ATP.

genomics↗