Fottea 2025, 25(1):68-80 | DOI: 10.5507/fot.2024.010

Trebouxia barrenoae sp. nov. (Trebouxiophyceae, Chlorophyta), a new lichenized microalga widespread in temperate ecosystems

Tamara Pazos1*, Patricia Moya1, Isaac Garrido-Benavent2, César D. Bordenave1, Ayelén Gazquez3, Salvador Chiva1
1 Instituto Cavanilles de Biodiversidad y Biologîa Evolutiva (ICBiBE)- Botànica, Universitat de València, C/ Dr. Moliner, 50, E-46100 Burjassot, València, Spain; *Corresponding author e-mail: tamara.pazos@uv.es
2 Departament de Botànica i Geologia, Universitat de València, C/ Dr. Moliner, 50, E-46100 Burjassot, València, Spain
3 Instituto de Biotecnología y Biomedicina (BIOTECMED), Universitat de València, E-46100 Burjassot, València, Spain

The genus Trebouxia includes the most widespread green microalgae inhabiting lichen thalli worldwide. Nonetheless, the vast majority of species-level phylogenetic lineages within this genus lack a formal taxonomic description and, to date, only 31 species have been accepted. In this study, we utilized an integrative taxonomic approach to describe the new species Trebouxia barrenoae Pazos, Chiva, Garrido-Benavent et Moya, a frequent symbiont in different lichens which is phylogenetically circumscribed to Trebouxia clade S. The ultrastructural features of the new microalga were studied through light, confocal, and electron microscopies; phylogenetic, physiological, and ecological niche analyses were carried out to characterize this new taxon as well. Our findings revealed a more frequent association of T. barrenoae sp. nov. with vegetatively reproducing lichens that thrive in temperate forest habitats and showed a preference for those growing on acidic substrates. The description of this species fosters progress in the systematics and taxonomy of the genus Trebouxia and enhances precise characterization of lichen phycobionts.

Keywords: chlorophyll fluorescence, epiphytic lichen, niche hypervolume, photobiont, symbiosis, taxonomic integrative approach, transmission electron microscopy (TEM)

Received: April 24, 2024; Revised: July 26, 2024; Accepted: October 1, 2024; Prepublished online: January 24, 2025; Published: April 1, 2025  Show citation

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Pazos, T., Moya, P., Garrido-Benavent, I., Bordenave, C.D., Gazquez, A., & Chiva, S. (2025). Trebouxia barrenoae sp. nov. (Trebouxiophyceae, Chlorophyta), a new lichenized microalga widespread in temperate ecosystems. Fottea, 25(1), 68-80. doi: 10.5507/fot.2024.010
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    References

    1. Archibald, P. A. (1975): Trebouxia Puymaly (Chlorophyceae, Chlorococcales) and Pseudotrebouxia gen. nov. (Chlorophyceae, Chlorosarcinales). - Phycologia 14 : 125-137. Go to original source...
    2. Baèkor M.; Peksa O.; ©kaloud P. & Baèkorová M. (2010): Photobiont diversity in lichens from metal-rich substrata based on ITS rDNA sequences. - Ecotoxicology and Environmental Safety 73: 603-12. Go to original source...
    3. Barreno, E.; Muggia, L.; Chiva, S.; Molins, A.; Bordenave, C.; García-Breijo, F. & Moya, P. (2022): Trebouxia lynnae sp. nov. (former Trebouxia sp. TR9): biology and biogeography of an epitome lichen symbiotic microalga. - Biology 11: 1196. Go to original source...
    4. Beck, A. (1999): Photobiont inventory of a lichen community growing on heavy-metal-rich rock. - The Lichenologist 31: 501-510. Go to original source...
    5. Beck, A. (2002): Selektivität der Symbionten schwermetalltoleranter Flechten [PhD. thesis]. - 162 pp., Ludwig-Maximilians-Universität München, Munich, Germany.
    6. Bhattacharya, D.; Friedl, T. & Damberger, S. (1996): Nuclear-encoded rDNA group I introns: origin and phylogenetic relationships of insertion site lineages in the green algae. - Molecular Biology and Evolution 13: 978-989. Go to original source...
    7. Bischoff, H. W.; Bold, H. C. (1963): Physiological studies: IV. - In: Some soil algae from enchanted rock and related algal species. - 6318 pp., University of Texas, Austin, TX, USA.
    8. Blonder, B.; Lamanna, C.; Violle, C. & Enquist, B. J. (2014): The n-dimensional hypervolume. - Global Ecology and Biogeography 23: 595-609. Go to original source...
    9. Bold, H. C. (1949): The morphology of Chlamydomonas chlamydogama, sp. nov. -Bulletin of the Torrey Botanical Club 76: 101-108. Go to original source...
    10. Boluda, C. G.; Rico, V. J.; Naciri, Y.; Hawksworth, D. L. & Scheidegger, C. (2021): Phylogeographic reconstructions can be biased by ancestral shared alleles: The case of the polymorphic lichen Bryoria fuscescens in Europe and North Africa. - Molecular Ecology 30: 4845-4865. Go to original source...
    11. Bordenave, C. D.; Muggia, L.; Chiva, S.; Leavitt, S. D.; Carrasco, P. & Barreno, E. (2022): Chloroplast morphology and pyrenoid ultrastructural analyses reappraise the diversity of the lichen phycobiont genus Trebouxia (Chlorophyta). - Algal Research 61: 102561. Go to original source...
    12. Casano, L. M.; del Campo, E. M.; García-Breijo, F. J.; Reig-Armiñana, J.; Gasulla, F.; Del Hoyo, A.; Guéra, A. & Barreno, E. (2011): Two Trebouxia algae with different physiological performances are ever-present in lichen thalli of Ramalina farinacea. Coexistence versus competition? - Environmental Microbiology 13: 806-818. Go to original source...
    13. Chiva, S.; Dumitru, C.; Bordenave, C. D. & Barreno, E. (2021): Watanabea green microalgae (Trebouxiophyceae) inhabiting lichen holobiomes: Watanabea lichenicola sp. nova. - Phycological Research 69: 226-236. Go to original source...
    14. De Carolis, R.; Cometto, A.; Moya, P.; Barreno, E.; Grube, M.; Tretiach, M.; Leavitt, S. D. & Muggia, L. (2022): Photobiont diversity in lichen symbioses from extreme environments. - Frontiers in Microbiology 13: 809804. Go to original source...
    15. Del Campo, E. M.; Casano, L. M.; Gasulla, F. & Barreno, E. (2010): Suitability of chloroplast LSU rDNA and its diverse group I introns for species recognition and phylogenetic analyses of lichen-forming Trebouxia algae. - Molecular Phylogenetics and Evolution 54: 437- 444. Go to original source...
    16. Domaschke, S.; Vivas, M.; Sancho, L. G. & Printzen, C. (2013): Ecophysiology and genetic structure of polar versus temperate populations of the lichen Cetraria aculeata. - Oecologia 173: 699-709. Go to original source...
    17. Ettl, H. & Gärtner, G. (2014): Syllabus der Boden-, Luft- und Flechtenalgen. - 773 pp., Springer, Berlin/ Heidelberg, Germany. Go to original source...
    18. Friedl, T. (1989): Systematik und Biologie von Trebouxia (Microthamniales, Chlorophyta) als Phycobiont der Parmeliaceae (lichenisierte Ascomyceten) [PhD thesis]. - 218 pp., Fakultät für Biologie, Chemie und Geowissenschaften, Universität Bayreuth, Bayreuth, Germany.
    19. García-Rodríguez, A.; Granados-López, D.; García-Rodríguez, S.; Díez-Mediavilla, M. & Alonso-Tristán, C. (2021): Modelling Photosynthetic Active Radiation (PAR) through meteorological indices under all sky conditions. - Agricultural and Forest Meteorology 310: 108627. Go to original source...
    20. Garrido-Benavent, I.; Chiva, S.; Bordenave, C. D.; Molins, A. & Barreno, E. (2022): Trebouxia maresiae sp. nov. (Trebouxiophyceae, Chlorophyta), a new lichenized species of microalga found in coastal environments. - Cryptogamie, Algologie 43: 135-145. Go to original source...
    21. Garrido-Benavent, I.; Pérez-Ortega, S.; de los Ríos, A. & Fernández-Mendoza, F. (2020): Amphitropical variation of the algal partners of Pseudephebe (Parmeliaceae, lichenized fungi). - Symbiosis 82: 35-48. Go to original source...
    22. Gartner, G. (1985): Die Gattung Trebouxia Puymaly (Chlorellales, Chlorophyceae). - Algological Studies 71: 495-548.
    23. Gasulla, F.; Guéra, A. & Barreno, E. (2010): A simple and rapid method for isolating lichen photobionts. - Symbiosis 51: 175-179. Go to original source...
    24. Grube, M. (2024): Lichens. - In: Fungal Associations; Cham. - pp. 145-179, Springer International Publishing. Go to original source...
    25. Guiry, M. D.; Guiry, G. M. AlgaeBase, World-Wide Electronic Publication. - National University of Ireland: Galway, Ireland, 2019; Available at https://www.algaebase.org (accessed on 22 January 2024).
    26. Helms, G.; Friedl, T.; Rambold, G. & Mayrhofer, H. (2001): Identification of photobionts from the lichen family Physciaceae using algal-specific ITS rDNA sequencing. - The Lichenologist 33: 73-86. Go to original source...
    27. Honegger, R. (1986): Ultrastructural studies in lichens: II. Mycobiont and photobiont cell wall surface layers and adhering crystalline lichen products in four Parmeliaceae. - New Phytologist 103: 797-808. Go to original source...
    28. Hutchinson, G. E. (1957): Concluding remarks. - Cold Spring Harbor Symposia on Quantitative Biology 22: 415-427. Go to original source...
    29. Karger, D.N.; Conrad, O.; Böhner, J.; Kawohl, T.; Kreft, H.; Soria-Auza, R.W. & Kessler, M. (2017): Climatologies at high resolution for the earth's land surface areas. - Scientific Data 4: 1-20. Go to original source...
    30. Katoh, K. & Standley, D. M. (2013): MAFFT multiple sequence alignment software version 7: improvements in performance and usability. - Molecular Biology and Evolution 30: 772-780. Go to original source...
    31. Katoh, K.; Misawa, K.; Kuma, K. I. & Miyata, T. (2002): MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. - Nucleic Acids Research 30: 3059-3066. Go to original source...
    32. Kosecka, M.; Kukwa, M.; Jab³oñska, A.; Flakus, A.; Rodriguez-Flakus, P.; Ptach, £. & Guzow-Krzemiñska, B. (2022): Phylogeny and ecology of Trebouxia photobionts from Bolivian lichens. - Frontiers in Microbiology 13: 779-784. Go to original source...
    33. Kroken, S. & Taylor, J. W. (2000): Phylogenetic species, reproductive mode, and specificity of the green alga Trebouxia forming lichens with the fungal genus Letharia. -Bryologist 103: 645-660. Go to original source...
    34. Lanfear, R.; Calcott, B.; Ho, S. Y. & Guindon, S. (2012): PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. - Molecular Biology and Evolution 29: 1695-1701. Go to original source...
    35. Leavitt, S. D.; Kraichak, E.; Nelsen, M. P.; Altermann, S.; Divakar, P. K.; Alors, D.; Esslinger, T. L.; Crespo, A. & Lumbsch, T. (2015): Fungal specificity and selectivity for algae play a major role in determining lichen partnerships across diverse ecogeographic regions in the lichen-forming family Parmeliaceae (Ascomycota). - Molecular Ecology 24: 3779-3797. Go to original source...
    36. Lindgren, H.; Velmala, S.; Högnabba, F.; Goward, T.; Holien, H. & Myllys, L. (2014): High fungal selectivity for algal symbionts in the genus Bryoria. - The Lichenologist 46: 681-695. Go to original source...
    37. Maddison, W. P. & Knowles, L. L. (2006): Inferring phylogeny despite incomplete lineage sorting. - Systematic Biology 55: 21-30. Go to original source...
    38. Mark, K.; Laanisto, L.; Bueno, C. G.; Niinemets, Ü.; Keller, C. & Scheidegger, C. (2020): Contrasting co-occurrence patterns of photobiont and cystobasidiomycete yeast associated with common epiphytic lichen species. - New Phytologist 227: 1362-1375. Go to original source...
    39. Mason-Gamer, R. J. & Kellogg, E. A. (1996): Testing for phylogenetic conflict among molecular data sets in the tribe Triticeae (Gramineae). - Systematic Biology 45: 524-545. Go to original source...
    40. Miadlikowska, J.; Richardson, D.; Magain, N.; Ball, B.; Anderson, F.; Cameron, R.; Lendemer, J.; Truong, C. & Lutzoni, F. (2014): Phylogenetic placement, species delimitation, and cyanobiont identity of endangered aquatic Peltigera species (lichen-forming Ascomycota, Lecanoromycetes). - American Journal of Botany 101: 1141-1156. Go to original source...
    41. Miller, M. A.; Pfeiffer, W. & Schwartz, T. (2010): Creating the CIPRES Science Gateway for inference of large phylogenetic trees. - In: Proceedings of the Gateway Computing Environments Workshop, New Orleans, LA, USA, 14 November 2010. - pp. 1-8, IEEE. Go to original source...
    42. Molins, A.; Moya, P.; Garcia-Breijo, F. J.; José, R. A. & Barreno, E. (2018): A multi-tool approach to assess microalgal diversity in lichens: isolation, Sanger sequencing, HTS and ultrastructural correlations. - The Lichenologist 50: 123-138. Go to original source...
    43. Moya, P.; Chiva, S.; Catalá, M.; Garmendia, A.; Casale, M.; Gomez, J.; Pazos, T.; Giordani, P.; Calatayud, V. & Barreno, E. (2023). Lichen biodiversity and near-infrared metabolomic fingerprint as diagnostic and prognostic complementary tools for biomonitoring: a case study in the eastern Iberian Peninsula. - Journal of Fungi 9: 1064. Go to original source...
    44. Moya, P.; Molins, A.; ©kaloud, P.; Divakar, P. K.; Chiva, S.; Dumitru, C.; Molina, M. C.; Crespo, A. & Barreno, E. (2021): Biodiversity patterns and ecological preferences of the photobionts associated with the lichen-forming genus Parmelia. - Frontiers in Microbiology 12: 765310. Go to original source...
    45. Muggia, L.; Leavitt, S. & Barreno, E. (2018): The hidden diversity of lichenized Trebouxiophyceae (Chlorophyta). - Phycologia 57: 503-524. Go to original source...
    46. Muggia, L.; Nelsen, M. P.; Kirika, P. M.; Barreno, E.; Beck, A.; Lindgren, H.; Lumbsch, H. T.; Leavitt, S. D. & Trebouxia Working Group. (2020): Formally described species woefully underrepresent phylogenetic diversity in the common lichen photobiont genus Trebouxia (Trebouxiophyceae, Chlorophyta): an impetus for developing an integrated taxonomy. - Molecular Phylogenetics and Evolution 149: 106821. Go to original source...
    47. Nelsen, M. P.; Leavitt, S. D.; Heller, K.; Muggia, L. & Lumbsch, H. T. (2021): Macroecological diversification and convergence in a clade of keystone symbionts. - FEMS Microbiology Ecology 97: fiab072. Go to original source...
    48. Nelsen, M. P.; Leavitt, S. D.; Heller, K.; Muggia, L. & Lumbsch, H. T. (2022): Contrasting patterns of climatic niche divergence in Trebouxia-a clade of lichen-forming algae. - Frontiers in Microbiology 13: 791546. Go to original source...
    49. Nelsen, M. P.; Lücking, R.; Mbatchou, J. S.; Andrew, C. J.; Spielmann, A. A. & Lumbsch, H. T. (2011): New insights into relationships of lichen-forming Dothideomycetes. - Fungal Diversity 51: 155-162. Go to original source...
    50. Onuț-Brännström, I.; Benjamin, M.; Scofield, D. G.; Heiðmarsson, S.; Andersson, M. G.; Lindström, E. S. & Johannesson, H. (2018): Sharing of photobionts in sympatric populations of Thamnolia and Cetraria lichens: evidence from high-throughput sequencing. - Scientific Reports 8: 4406. Go to original source...
    51. Opanowicz, M. & Grube, M. (2004): Photobiont genetic variation in Flavocetraria nivalis from Poland (Parmeliaceae, lichenized Ascomycota). - The Lichenologist 36: 125-131. Go to original source...
    52. Ossowska, E.; Guzow-Krzemiñska, B.; Kolanowska, M.; Szczepañska, K. & Kukwa, M. (2019): Morphology and secondary chemistry in species recognition of Parmelia omphalodes group-evidence from molecular data with notes on the ecological niche modelling and genetic variability of photobionts. - MycoKeys 61: 39. Go to original source...
    53. Pateiro-Lopez, B. & Rodriguez-Casal, A. (2016). Alphahull: generalization of the convex hull of a sample of points in the plane. - Available at: https:// cran.r-project.org/package=alphahull (Accessed 17 March, 2024).
    54. Peksa, O.; Gebouská, T.; ©kvorová, Z.; Vanèurová, L. & ©kaloud, P. (2022): The guilds in green algal lichens-An insight into the life of terrestrial symbiotic communities. - FEMS Microbiology Ecology 98: fiac008. Go to original source...
    55. Piercey-Normore, M. D. (2009): Vegetatively reproducing fungi in three genera of the Parmeliaceae share divergent algal partners. - The Bryologist 112: 773-785. Go to original source...
    56. Piercey-Normore, M. D. & DePriest, P. T. (2001): Algal switching among lichen symbioses. - American Journal of Botany 88: 1490-1498. Go to original source...
    57. Proutsos, N.; Alexandris, S.; Liakatas, A.; Nastos, P. & Tsiros, I. X. (2022): PAR and UVA composition of global solar radiation at a high altitude Mediterranean forest site. - Atmospheric Research 269: 106039. Go to original source...
    58. R Core Team. (2021): R: a language and environment for statistical computing. - Available online: https://www.R-project.org/ (accessed on 17 February 2024).
    59. Rachoski, M.; Gazquez, A.; Calzadilla, P.; Bezus, R.; Rodriguez, A.; Ruiz, O.; Bernardina, A. & Maiale, S. (2015): Chlorophyll fluorescence and lipid peroxidation changes in rice somaclonal lines subjected to salt stress. - Acta Physiologiae Plantarum 37: 1-12. Go to original source...
    60. Rambold, G.; Friedl, T. & Beck, A. (1998): Photobionts in lichens: possible indicators of phylogenetic relationships. - The Bryologist 101: 392-397. Go to original source...
    61. Rivas-Martínez, S.; Penas, Á.; del Río, S.; Díaz González, T. E. & Rivas-Sáenz, S. (2017): Bioclimatology of the Iberian Peninsula and the Balearic Islands. - In: Loidi, J. (ed.): The vegetation of the Iberian Peninsula. - pp. 29-80, Springer, Cham, Switzerland. Go to original source...
    62. Ronquist, F.; Teslenko, M.; Van Der Mark, P.; Ayres, D. L.; Darling, A.; Höhna, S.; Larget, B.; Liu, L.; Suchard, M. A. & Huelsenbeck, J. P. (2012): MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. - Systematic Biology 61: 539-542. Go to original source...
    63. RStudio Team. RStudio: Integrated Development Environment for R; RStudio, PBC: Boston, MA, USA, 2023. - Available online: https://www.algaebase.org (accessed on 17 January 2024).
    64. Ruprecht, U.; Brunauer, G. & Türk, R. (2014): High photobiont diversity in the common European soil crust lichen Psora decipiens. - Biodiversity and conservation 23: 1771-1785. Go to original source...
    65. Sadowska-De¶, A. D.; Dal Grande, F.; Lumbsch, H. T.; Beck, A.; Otte, J.; Hur, J. S.; Kim, J. & Schmitt, I. (2014): Integrating coalescent and phylogenetic approaches to delimit species in the lichen photobiont Trebouxia. - Molecular Phylogenetics and Evolution 76: 202-210. Go to original source...
    66. Sahu, N.; Singh, S. N.; Singh, P.; Mishra, S.; Karakoti, N.; Bajpai, R.; Behera, S. K.; Nayaka, S. & Upreti, D. K. (2019): Microclimatic variations and their effects on photosynthetic efficiencies and lichen species distribution along elevational gradients in Garhwal Himalayas. - Biodiversity and Conservation 28: 1953-1976. Go to original source...
    67. Schindelin, J.; Arganda-Carreras, I.; Frise, E.; Kaynig, V.; Longair, M.; Pietzsch, T.; Preibisch, S.; Rueden, C.; Saalfeld, S.; Schmid, B.; Tinevez, J.; White, D. J.; Hartenstein, V.; Eliceiri, K, Tomancak, P & Cardona, A. (2012): Fiji: an open-source platform for biological-image analysis. - Nature Methods 9: 676-682. Go to original source...
    68. Singh, G.; Kukwa, M.; Dal Grande, F.; £ubek, A.; Otte, J. & Schmitt, I. (2019): A glimpse into genetic diversity and symbiont interaction patterns in lichen communities from areas with different disturbance histories in Bia³owie¿a forest, Poland. - Microorganisms 7: 335. Go to original source...
    69. ©kaloud, P.; Moya, P.; Molins, A.; Peksa, O.; Santos-Guerra, A. & Barreno, E. (2018): Untangling the hidden intrathalline microalgal diversity in Parmotrema pseudotinctorum: Trebouxia crespoana sp. nov. - The Lichenologist 50: 357-369. Go to original source...
    70. Stamatakis, A. (2006): RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. - Bioinformatics 22: 2688-2690. Go to original source...
    71. Stamatakis, A.; Hoover, P. & Rougemont, J. (2008): A rapid bootstrap algorithm for the RAxML web servers. - Systematic Biology 57: 758-771. Go to original source...
    72. Stirbet, A. & Govindjee (2011): On the relation between the kautsky effect (chorophyll a fluorescence induction and photosystem II: basic and applications of the OJIP fluorescent transient. - Journal of Photochemistry and Photobiology B: Biology 104: 236-257. Go to original source...
    73. Tschermak-Woess, E. (1978): Über die Phycobionten der Sektion Cystophora von Chaenotheca, insbesondere Dictyochloropsis splendida und Trebouxia simplex, spec. nova: the phycobionts in the section Cystophora of Chaenotheca, especially Dictyochloropsis splendida and Trebouxia simplex, spec. nova. - Plant Systematics and Evolution 129: 185-208. Go to original source...
    74. Vanèurová, L.; Malíèek, J.; Steinová, J. & ©kaloud, P. (2021): Choosing the right life partner: ecological drivers of lichen symbiosis. - Frontiers in Microbiology 12: 769304. Go to original source...
    75. Vanèurová, L.; Muggia, L.; Peksa, O.; Øídká, T. & ©kaloud, P. (2018): The complexity of symbiotic interactions influences the ecological amplitude of the host: a case study in Stereocaulon (lichenized Ascomycota). - Molecular Ecology 27: 3016-3033. Go to original source...
    76. Veselá, V.; Malavasi, V. & ©kaloud, P. (2024): A synopsis of green-algal lichen symbionts with an emphasis on their free-living lifestyle. - Phycologia 63: 317-338. Go to original source...
    77. Zhao, X.; Fernández-Brime, S.; Wedin, M.; Locke, M.; Leavitt, S.D. & Lumbsch, H.T. (2017): Using multi-locus sequence data for addressing species boundaries in commonly accepted lichen-forming fungal species. - Organisms, Diversity and Evolution 17: 351-363. Go to original source...

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