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The puzzle of lichen symbiosis: Pieces from Thamnolia
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology. (Johannesson Lab)
2017 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Symbiosis brought important evolutionary novelties to life on Earth. Lichens, the symbiotic entities formed by fungi, photosynthetic organisms and bacteria, represent an example of a successful adaptation in surviving hostile environments. Yet many aspects of the lichen symbiosis remain unexplored. This thesis aims at bringing insights into lichen biology and the importance of symbiosis in adaptation. I am using as model system a successful colonizer of tundra and alpine environments, the worm lichens Thamnolia, which seem to only reproduce vegetatively through symbiotic propagules. When the genetic architecture of the mating locus of the symbiotic fungal partner was analyzed with genomic and transcriptomic data, a sexual self-incompatible life style was revealed. However, a screen of the mating types ratios across natural populations detected only one of the mating types, suggesting that Thamnolia has no potential for sexual reproduction because of lack of mating partners. Genetic data based on molecular markers revealed the existence of three morphologically cryptic Thamnolia lineages. One lineage had a clear recombination structure and was found in the tundra region of Siberia, shorelines of Scandinavia, and Aleutian Islands. The other lineage was allopatric with the previous, and was highly clonal; only two haplotypes were found across the alpine region of central and southeastern Europe. However, the third lineage was sympatric with the other two, had a worldwide distribution, and although highly clonal, showed a recombinant population structure. Our data could not reveal whether the signs of recombination resulted from rare recombination events due to the extreme low frequency of the other mating type or ancestral variation before the loss of sexual reproduction. However, investigation of Thamnolia’s green algal population showed that in different localities, different algal genotypes were associated with the same fungal genotype. Furthermore, data suggest that Thamnolia carried several algal genotypes within its thalli and shared them with other distantly related but ecologically similar fungal species.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2017. , p. 62
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1503
Keywords [en]
Thamnolia, lichen, symbiosis, photobiont, mycobiont, phylogeography, MAT-loci, barcoding, NGS, genome, transcriptome, Ice Age
National Category
Natural Sciences
Research subject
Biology with specialization in Systematics
Identifiers
URN: urn:nbn:se:uu:diva-319639ISBN: 978-91-554-9887-0 (print)OAI: oai:DiVA.org:uu-319639DiVA, id: diva2:1087397
Public defence
2017-06-01, Lindhalsalen, EBC, Norbyvägen 14, Uppsala, 09:15 (English)
Opponent
Supervisors
Available from: 2017-05-08 Created: 2017-04-06 Last updated: 2017-05-29
List of papers
1. A worldwide phylogeography of the whiteworm lichens Thamnolia reveals three lineages with distinct habitats and evolutionary histories
Open this publication in new window or tab >>A worldwide phylogeography of the whiteworm lichens Thamnolia reveals three lineages with distinct habitats and evolutionary histories
2017 (English)In: Ecology and Evolution, ISSN 2045-7758, E-ISSN 2045-7758, Vol. 7, no 10, p. 3602-3615Article in journal (Refereed) Published
Abstract [en]

Thamnolia is a lichenized fungus with an extremely wide distribution, being encountered in arctic and alpine environments in most continents. In this study, we used molecular markers to investigate the population structure of the fungal symbiont and the associated photosynthetic partner of Thamnolia. By analyzing molecular, morphological, and chemical variation among 253 specimens covering the species distribution range, we revealed the existence of three mycobiont lineages. One lineage (Lineage A) is confined to the tundra region of Siberia and the Aleutian Islands, a second (Lineage B) is found in the high alpine region of the Alps and the Carpathians Mountains, and a third (Lineage C) has a worldwide distribution and covers both the aforementioned ecosystems. Molecular dating analysis indicated that the split of the three lineages is older than the last glacial maximum, but the distribution ranges and the population genetic analyses suggest an influence of last glacial period on the present-day population structure of each lineage. We found a very low diversity of Lineage B, but a higher and similar one in Lineages A and C. Demographic analyses suggested that Lineage C has its origin in the Northern Hemisphere, possibly Scandinavia, and that it has passed through a bottleneck followed by a recent population expansion. While all three lineages reproduce clonally, recombination tests suggest rare or past recombination in both Lineages A and C. Moreover, our data showed that Lineage C has a comparatively low photobiont specificity, being found associated with four widespread Trebouxia lineages (three of them also shared with other lichens), while Lineages A and B exclusively harbor T. simplex s. lat. Finally, we did not find support for the recognition of taxa in Thamnolia based on either morphological or chemical characters.

Place, publisher, year, edition, pages
John Wiley & Sons, 2017
National Category
Evolutionary Biology Ecology Other Biological Topics
Identifiers
urn:nbn:se:uu:diva-319636 (URN)10.1002/ece3.2917 (DOI)000402554700030 ()28515896 (PubMedID)
Available from: 2017-04-06 Created: 2017-04-06 Last updated: 2018-03-29Bibliographically approved
2. Thamnolia tundrae sp nov., a cryptic species and putative glacial relict
Open this publication in new window or tab >>Thamnolia tundrae sp nov., a cryptic species and putative glacial relict
2018 (English)In: The Lichenologist, ISSN 0024-2829, E-ISSN 1096-1135, Vol. 50, no 1, p. 59-75Article in journal (Refereed) Published
Abstract [en]

The lichen species of the genus Thamnolia, with their striking wormlike thalli and frequent occurrence in arctic and tundra environments, have often been debated with regard to the use of chemistry in lichen taxonomy. Phylogenetic studies have arrived at different conclusions as to the recognition of species in the genus, but in a recent study based on the analyses of six nuclear markers (genes or noncoding regions) of a worldwide sample of Thamnolia, we showed the existence of three well-supported lineages with two different chemistries and geographical distributions. Here, we present two analyses based on ITS and three markers, respectively, which were extended from the study mentioned above to include type specimens and additional Thamnolia strains and taxa. In these analyses the same three clades were retrieved. A putative DEAD-box helicase is used here for the first time as an informative phylogenetic marker to provide taxonomic resolution at species level. The distribution of morphological and chemical characters across the phylogeny was analyzed and it was concluded that three morphologically cryptic, but genetically well supported, species occur: T. vermicularis s. str., T. subuliformis s. str. and T. tundrae sp. nov. Thamnolia vermicularis s. str. contains individuals with uniform secondary chemistry (producing thamnolic acid) and a rather limited distribution in the European Alps, Tatra Mts and the Western Carpathians, a distribution which might result from glacial survival in an adjacent refugium/refugia. Thamnolia subuliformis s. str. is widely distributed in all hemispheres and the samples contain two chemotypes (either with thamnolic or squamatic acids). Thamnolia tundrae is described as new; it produces baeomycesic and squamatic acids, and has a distribution limited to the arctic tundra of Eurasia extending to the Aleutian Islands in North America. It may have survived the latest glaciation in coastal refugia near its present distribution. Thus, secondary chemistry alone is not suitable for characterizing species in Thamnolia, secondary chemistry and geographical origin are informative, and the ITS region can be confidently used for species recognition. Nomenclatural notes are given on several other names that have been used in Thamnolia.

Keywords
lichens, molecular phylogeny, new species, nomenclature, secondary chemistry, taxonomy
National Category
Biological Systematics
Identifiers
urn:nbn:se:uu:diva-319635 (URN)10.1017/S0024282917000615 (DOI)
Note

Title in Thesis list of papers: Thamnolia tundrae n. sp., a cryptic species and putative glacial relict

Available from: 2017-04-06 Created: 2017-04-06 Last updated: 2018-05-31Bibliographically approved
3. Sharing of photobionts in sympatric populations of Thamnolia and Cetraria lichens: evidence from high-throughput sequencing
Open this publication in new window or tab >>Sharing of photobionts in sympatric populations of Thamnolia and Cetraria lichens: evidence from high-throughput sequencing
Show others...
2018 (English)In: Scientific Reports, ISSN 2045-2322, E-ISSN 2045-2322, Vol. 8, article id 4406Article in journal (Refereed) Published
Abstract [en]

In this study, we explored the diversity of green algal symbionts (photobionts) in sympatric populations of the cosmopolitan lichen-forming fungi Thamnolia and Cetraria. We sequenced with both Sanger and Ion Torrent High-Throughput Sequencing technologies the photobiont ITS-region of 30 lichen thalli from two islands: Iceland and Öland. While Sanger recovered just one photobiont genotype from each thallus, the Ion Torrent data recovered 10–18 OTUs for each pool of 5 lichen thalli, suggesting that individual lichens can contain heterogeneous photobiont populations. Both methods showed evidence for photobiont sharing between Thamnolia and Cetraria on Iceland. In contrast, our data suggest that on Öland the two mycobionts associate with distinct photobiont communities, with few shared OTUs revealed by Ion Torrent sequencing. Furthermore, by comparing our sequences with public data, we identified closely related photobionts from geographically distant localities. Taken together, we suggest that the photobiont composition in Thamnolia and Cetraria results from both photobiont-mycobiont codispersal and local acquisition during mycobiont establishment and/or lichen growth. We hypothesize that this is a successful strategy for lichens to be flexible in the use of the most adapted photobiont for the environment.

National Category
Ecology Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-319634 (URN)10.1038/s41598-018-22470-y (DOI)000427241500007 ()
Funder
Swedish National Infrastructure for Computing (SNIC), b2013277The Royal Swedish Academy of SciencesHelge Ax:son Johnsons stiftelse Lars Hierta Memorial FoundationSwedish National Infrastructure for Computing (SNIC), b2013277
Note

Title in thesis list of papers: Differential sharing of photobionts in sympatric populations of Thamnolia and Cetraria lichens: evidence from next generation sequencing

Available from: 2017-04-06 Created: 2017-04-06 Last updated: 2018-05-31Bibliographically approved
4. Constraints to sex by a single mating type? Genomic and population analyses reveal insight into the reproductive biology of Thamnolia
Open this publication in new window or tab >>Constraints to sex by a single mating type? Genomic and population analyses reveal insight into the reproductive biology of Thamnolia
Show others...
(English)Manuscript (preprint) (Other academic)
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-319638 (URN)
Available from: 2017-04-06 Created: 2017-04-06 Last updated: 2017-04-18

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