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Hidden diversity of marine borderline lichens and a new order of fungi: Collemopsidiales (Dothideomyceta)

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Abstract

The fungal genus Collemopsidium comprises species that develop so-called borderline lichen symbioses with algae or cyanobacteria. Together with morphologically similar pyrenocarpous fungi it has been assigned to the family Xanthopyreniaceae. The adscription of this family to higher taxonomic ranks remain uncertain. Using sequence data of five nuclear genomic regions (nuLSU, nuSSU, tef1-α, rpb1 and rpb2) and one mitochondrial locus (mtSSU) we found that the studied representatives of this family are placed in the Dothideomyceta, yet relationships with the classes Dothideomycetes and Arthoniomycetes remain uncertain. We describe the new order Collemopsidiales to accommodate the genus Collemopsidium (paraphyletic as currently understood) and the lichenicolous genus Zwackhiomyces. Using five fungal fossils as calibrations points, we infer an age of c. 230 Mya for the crown of Collemopsidiales. Based on two molecular markers, we also provide insight into the global diversity of marine species of the genus Collemopsidium. According to the species delimitation algorithm GMYC, c. 26 putative species exist, far more than the six species recognized hitherto. We have confirmed this result by comparing the two alternative species models by means of Bayes factors, using path sampling and stepping-stone sampling algorithms to estimate the marginal likelihood of each model. Finally, our observations suggest rock-boring ability evolved in parallel in the different lineages within this group of fungi.

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Acknowledgments

The authors would like to thank Javier Etayo (Navarra), Victor J. Rico (Madrid), Mercedes Vivas (Concepción), María Arróniz-Crespo (Madrid), Cécile Gueidan (Canberra) for collecting fresh specimens, Toby Spribille (Graz), Alan Orange (Cardiff) and Karen Dillman (Petersburg) for assistance during field work, María José Malo (Madrid) for her help with lab work and Ana Burton for improving English. SPO, IGB and AdR were supported by grant CTM2012-38222-C02-02, IGB was supported by grant FPU AP2012-3556, SPO is currently supported by the grant RYC-2014-16784, all from the Spanish Ministry of Economy and Competitiveness. We also thank the staff of the microscopy facility of the ICA (CSIC, Madrid) for technical assistance and the three anonymous reviewers for their suggestions and insightful comments.

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Authors and Affiliations

  1. Museo Nacional de Ciencias Naturales (CSIC), Serrano 115 dpdo, E-28006, Madrid, Spain

    Sergio Pérez-Ortega, Isaac Garrido-Benavent, Rocío Olmo & Asunción de los Ríos

  2. Real Jardín Botánico de Madrid (CSIC), Plaza Murillo 2, E-28014, Madrid, Spain

    Sergio Pérez-Ortega

  3. Institute of Plant Sciences, University of Graz, Holteigasse 6, A-8010, Graz, Austria

    Martin Grube

  4. Facultad de Ciencias Ambientales y Bioquímica, Universidad de Castilla-La Mancha, Avenida de Carlos III s/n, 45071, Toledo, Spain

    Rocío Olmo

Authors
  1. Sergio Pérez-Ortega
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  2. Isaac Garrido-Benavent
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  3. Martin Grube
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  4. Rocío Olmo
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  5. Asunción de los Ríos
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Corresponding author

Correspondence to Sergio Pérez-Ortega.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Suppl. Table 1

Specimen information and accession numbers for the Xanthopyreniaceae material used in the phylogenetic designations. (DOCX 16 kb)

Suppl. Table 2

Specimen information and accession numbers for the marine Collemopsidium specimens. (DOC 240 kb)

Suppl. Table 3

Accession numbers for the Ascomycota dataset (AC). (DOC 128 kb)

Suppl. Table 4

Accession numbers for the Dothideomyceta dataset (DO). (DOCX 30 kb)

Suppl. Table 5

Nodes and divergences times (DOC 41 kb)

Suppl. Fig. 1

Six-locus phylogeny (50 % majority rule consensus tree) depicting phylogenetic relationships among clades of Dothideomyceta including species of Xanthopyreniaceae (Collemopsidiales). Filled in circles on branches indicate Bayesian posterior probability (PP) ≥ 95 % and ML bootstrap values (B) ≥ 70 %. Left filled circles represent only PP support. Right filled circles represent only ML bootstrap support. Members of the Dothideomyceta are indicated in colour: red for Dothiodeomycetes, green for Arthoniomycetes and blue for Xanthopyreniaceae (Collemopsidiales). (GIF 116 kb)

High resolution image (TIF 25136 kb)

Suppl. Fig. 2

Maximum clade credibility (MCC) cartoon tree with divergence times estimates for main clades of Ascomycota. Estimates were obtained using a Bayesian approach (BEAST) and five fossil calibration points. Bars correspond to 95 % highest posterior density intervals (HPD). Filled in circles on branches indicate Bayesian posterior probability (PP) ≥ 95 %. Estimated ages (median and HPD) for the nodes (1-12) are available in Suppl. Table 5. Abbreviations for geologic periods read as follow: Cam. = Cambrian, Ord. = Ordovician, Sil. = Silurian, Dev. = Devonian, Carb. = Carboniferous, Perm. = Permian, Trias. = Triassic; Jura. = Jurassic, Cenoz. = Cenozoic. (GIF 194 kb)

High resolution image (TIF 506 kb)

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Pérez-Ortega, S., Garrido-Benavent, I., Grube, M. et al. Hidden diversity of marine borderline lichens and a new order of fungi: Collemopsidiales (Dothideomyceta). Fungal Diversity 80, 285–300 (2016). https://doi.org/10.1007/s13225-016-0361-1

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