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Evidence of ancient horizontal gene transfer between fungi and the terrestrial alga Trebouxia

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Abstract

Intimate and long-lasting relationships of fungi and algae have been known for centuries by scientists, and these ancient symbioses might have provided excellent opportunities for horizontal gene transfer (HGT) of protein encoding genes between the two organismal partners. In this study, we sequenced and assembled 451 Mbp of novel genomic DNA from Trebouxia decolorans (Trebouxiaceae, Chlorophyta), the green algal photobiont of the lichen Xanthoria parietina (Teloschistaceae, Lecanoromycetes, Ascomycota). This alga also occurs as a free-living terrestrial organism. The aim of our work was to search for candidate genes pointing to HGT between lichenized fungi and lichen algae. We found evidence for three putative HGT events of fungal genes into the Trebouxia genome, but these are likely more ancient (over 600 mya) than the origin of lichenization within the fungal Ascomycetes. The three transferred genes are part of gene groups that in other species encode a tellurite-resistance dicarboxylate transporter (TDT) family protein, a class-1 nitrilase/cyanide hydratase (CH), and an oxidoreductase/retinol dehydrogenase. In each case, our phylogenomic analyses show orthologs from Trebouxia as sister to orthologs from all fungi or basally placed within Ascomycetes, while the orthologs from green algae and land plants form separate, independent evolutionary lineages. Alternative hypothesis tests significantly support these HGT events. The presence of these genes in Trebouxia was validated by PCR amplification of separately isolated Trebouxia DNA. The ancient incorporation of fungal genes in the genomes of these particular green algae are intriguing and could be early evidence for symbiotic and co-evolutionary relationships among the major eukaryotic branches of algae and fungi present in early terrestrial life on Earth. These genes could have played a pre-disposition role for some fungi and algae in the origin of lichen symbiosis, but further studies are needed to evaluate this in detail.

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Acknowledgments

We sincerely thank Debashish Bhattacharya and Dana Price (both Rutgers) for crucial help with genome sequencing, data analysis, setting up the web page at http://dbdata.rutgers.edu/data/Trebouxia/ and long, fruitful, and encouraging discussions. Divino Rajah (Rutgers) is gratefully acknowledged for technical support. Paul Dyer and the Joint Genome Institute are thanked for access to the Xanthoria parietina fungal genome, Daniele Armaleo and the Joint Genome Institute are thanked for access to the Asterochloris sp. algal genome and Katherine McMahon and the Joint Genome Institute are thanked for access to the Cladonia grayi fungal genome. This work was generously supported by Illumina, Inc., who provided sequencing reagents to the Genome Cooperative at Rutgers University (http://dblab.rutgers.edu/genome_cooperative/) and the German Science Foundation (BE3825/2-1 to AB). PKD thanks the Ministerio de Ciencia e Innovación (Spain) for financial support (CGL2013-42498-P, CGL2010-21646/BOS) and MCM acknowledges support by a research grant from Universidad Rey Juan Carlos (Estancias Breves de Investigación) as Visiting Scientist to Rutgers University. NZ thanks Rutgers University for startup funds. LS was funded by US Department of Agriculture award USDA/NJAES-NJ17112.

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Authors and Affiliations

  1. Botanische Staatssammlung München/Lichenology Department, Menzinger Str. 67, 80638, Munich, Germany

    A. Beck

  2. Center of Geobiology and Biodiversity Research, Ludwig–Maximilians Universität München, Munich, Germany

    A. Beck

  3. Facultad de Farmacia/Departamento de Biología Vegetal II, Universidad Complutense de Madrid, Madrid, Spain

    P. K. Divakar

  4. Department of Plant Biology and Pathology, Rutgers University, New Brunswick, NJ, USA

    N. Zhang & L. Struwe

  5. Departamento de Biología y Geología, Universidad Rey Juan Carlos, ESCET, Madrid, Spain

    M. C. Molina

  6. Department of Ecology, Evolution and Natural Resources, Rutgers University, New Brunswick, NJ, USA

    L. Struwe

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Correspondence to A. Beck.

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Research experiments were done in the labs of the Botanische Staatssammlung München and Rutgers University (see M & M for details)

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Supplement S1

Phylogenetic tree derived from Bayesian analysis of the alignment of the sequences from the sulfite efflux pump/tellurite-resistance dicarboxylate transporter (TDT) family. Fungal sequences (Fungi) are marked in blue, green plants (Viridiplantae) in green, red algae (Rhodophyta) in red, Archaea sequences in purple, and all bacteria in black. The Trebouxia sequence is in bold text, and bolded branches are supported by posterior probability values ≥ 0.90 and bootstrap values ≥ 0.8 (with exact numbers marked by each branch). (EPS 10036 kb)

Supplement S2

Phylogenetic tree derived from Bayesian analysis of the alignment of the sequences from the class-1 nitrilase / cyanide hydratase (CH) family. Fungal sequences (Fungi) are marked in blue, green plants (Viridiplantae) in green, red algae (Rhodophyta) in red, animal (Metazoa) sequences in brown, other eukaryotes in pink, Archaea sequences in purple, and all bacteria in black. The Trebouxia sequence is in bold text, and bolded branches are supported by posterior probability values ≥ 0.90 and RAxML bootstrap values ≥ 0.8 (with exact numbers marked by each branch). (EPS 9882 kb)

Supplement S3

Phylogenetic tree derived from Bayesian analysis of the alignment of the sequences from the oxidoreductase/retinol dehydrogenases family. Fungal sequences (Fungi) are marked in blue, green plants (Viridiplantae) in green, animal (Metazoa) sequences in brown, other eukaryotes in pink, and all bacteria are in black. The Trebouxia sequence is in bold text, and bolded branches are supported by posterior probability values ≥ 0.90 and RAxML bootstrap values ≥ 0.8 (with exact numbers marked by each branch). (EPS 11106 kb)

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Beck, A., Divakar, P.K., Zhang, N. et al. Evidence of ancient horizontal gene transfer between fungi and the terrestrial alga Trebouxia . Org Divers Evol 15, 235–248 (2015). https://doi.org/10.1007/s13127-014-0199-x

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