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A chemosystematic investigation of selected Stichococcus-like organisms (Trebouxiophyta)

  • Van, Anh Tu (Department of Applied Ecology and Phycology, Institute of Biological Sciences, University of Rostock) ;
  • Karsten, Ulf (Department of Applied Ecology and Phycology, Institute of Biological Sciences, University of Rostock) ;
  • Glaser, Karin (Department of Applied Ecology and Phycology, Institute of Biological Sciences, University of Rostock)
  • Received : 2021.01.21
  • Accepted : 2021.06.05
  • Published : 2021.06.15

Abstract

The taxonomy of green microalgae relies traditionally on morphological traits but has been rapidly changing since the advent of molecular methods. Stichococcus Nägeli is a cosmopolitan terrestrial algal genus of the class Trebouxiophyceae that has recently been split into seven lineages, which, along with Pseudostichococcus, comprise the Stichococcuslike group; there is a need to further characterize these genera, since they are morphologically enigmatic. Here we used organic osmolytes as chemotaxonomic marker to verify the phylogenetic position of Stichococcus-like strains and were also able to exclude a strain hitherto identified as Gloeotila contorta from this group. Stichococcus-like organisms, including those recently revised, were characterized by the production of the polyol sorbitol and the disaccharide sucrose in high amounts, as is typical of Prasiola-clade algae. The results demonstrate that organic osmolyte chemotaxonomy can support green algal taxonomic designations as fundamental research.

Keywords

Acknowledgement

This cooperation would not have been possible without the generous materials support from Dr. Anna Temraleeva (Algal Collection of Soil Science Institute, Puschchino, Russia), Dr. Pavel Skaloud (Charles University, Prague, Czech Republic), Dr. Lira Gaysina (Resource Centre Culture Collection of Microorganisms, St. Petersburg, Russia), Dr. Tatiana Mikhailyuk (M.K. Kholodny Institute of Botany, Kiev, Ukraine) and Dr. Andreas Holzinger (University of Innsbruck, Innsbruck, Austria). Many thanks in particular to Dr. Rhena Schumann and Dr. Dirk Michalik at the University of Rostock for guidance in HPLC and NMR methodology. Within the framework of the German Research Foundation Special Priority Project: 1991 Taxon-Omics (CrustAlgaeTax-GL909/1-1), we were able to offer additional and critical data on the taxonomic revision of this genus using a chemotaxonomic approach.

References

  1. Arce, G. 1971. Stichococcus sequoieti sp. nov. In Parker, B. C. & Brown, R. M. (Eds.) Contributions in Phycology. Allen Press, Lawrence, KS, pp. 25-30.
  2. Brown, L. M. 1977. Osmoregulatory mechanisms of a euryhaline alga, Stichococcus bacillaris (Chlorophyceae). J. Phycol. 13:9.
  3. Brown, L. M. & Hellebust, J. A. 1978. Sorbitol and proline as intracellular osmotic solutes in the green alga Stichococcus bacillaris. Can. J. Bot. 56:676-679. https://doi.org/10.1139/b78-074
  4. Brown, L. M. & Hellebust, J. A. 1980. Some new taxonomic characteristics applied to Stichococcus bacillaris (Chlorophyceae). Can. J. Bot. 58:1405-1411. https://doi.org/10.1139/b80-171
  5. Darienko, T., Gustavs, L., Eggert, A., Wolf, W. & Proschold, T. 2015. Evaluating the species boundaries of green microalgae (Coccomyxa, Trebouxiophyceae, Chlorophyta) using integrative taxonomy and DNA barcoding with further implications for the species identification in environmental samples. PLoS ONE 10:e0127838. https://doi.org/10.1371/journal.pone.0127838
  6. Darienko, T., Gustavs, L., Mudimu, O., Menendez, C. R., Schumann, R., Karsten, U., Friedl, T. & Proschold, T. 2010. Chloroidium, a common terrestrial coccoid green alga previously assigned to Chlorella (Trebouxiophyceae, Chlorophyta). Eur. J. Phycol. 45:79-95. https://doi.org/10.1080/09670260903362820
  7. Edgar, R. C. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792-1797. https://doi.org/10.1093/nar/gkh340
  8. Eggert, A. & Karsten, U. 2010. Low molecular weight carbohydrates in red algae-an ecophysiological and biochemical perspective. In Red algae in the genomic age. Springer, Dordrecht, pp. 443-456.
  9. Everard, J. D. & Loescher, W. H. 2016. Primary products of photosynthesis, sucrose and other soluble carbohydrates. In Thomas, B., Murray, B. G. & Murphy, D. J. (Eds.) Encyclopedia of Applied Plant Sciences. Academic Press, Waltmam, MA, pp. 96-104.
  10. Ferrenberg, S., Tucker, C. L. & Reed, S. C. 2017. Biological soil crusts: diminutive communities of potential global importance. Front. Ecol. Environ. 15:160-167. https://doi.org/10.1002/fee.1469
  11. Fontaine, K. M., Stocker-Woergoetter, E., Booth, T. & PierceyNormore, M. D. 2013. Genetic diversity of the lichenforming alga, Diplosphaera chodatii, in North America and Europe. Lichenologist 45:799-813. https://doi.org/10.1017/S0024282913000510
  12. Glaser, K., Baumann, K., Leinweber, P., Mikhailyuk, T. & Karsten, U. 2018. Algal richness in BSCs in forests under different management intensity with some implications for P cycling. Biogeosciences 15:4181-4192. https://doi.org/10.5194/bg-15-4181-2018
  13. Guiry, M. 2012. How many species of algae are there? J. Phycol. 48:1057-1063. https://doi.org/10.1111/j.1529-8817.2012.01222.x
  14. Gustavs, L., Gors, M. & Karsten, U. 2011. Polyol patterns in biofilm-forming aeroterrestrial green algae (Trebouxiophyceae, Chlorophyta). J. Phycol. 47:533-537. https://doi.org/10.1111/j.1529-8817.2011.00979.x
  15. Hallmann, C., Stannek, L., Fritzlar, D., Hause-Reitner, D., Friedl, T. & Hoppert, M. 2013. Molecular diversity of phototrophic biofilms on building stone. FEMS Microbiol. Ecol. 84:355-372. https://doi.org/10.1111/1574-6941.12065
  16. Handa, S., Nakahara, M., Tsubota, H., Deguchi, H. & Nakano, T. 2003. A new aerial alga, Stichococcus ampulliformis sp. nov. (Trebouxiophyceae, Chlorophyta) from Japan. Phycol. Res. 51:203-210. https://doi.org/10.1111/j.1440-1835.2003.tb00188.x
  17. Hellebust, J. A. 1985. Mechanisms of response to salinity in halotolerant microalgae. In Pasternak, D. & San Pietro, A. (Eds.) Biosalinity in Action: Bioproduction with Saline Water. Springer, Dordrecht, pp. 69-81.
  18. Henley, W. J., Hironaka, J. L., Guillou, L., Buchheim, M. A., Buchheim, J. A., Fawley, M. W. & Fawley, K. P. 2004. Phylogenetic analysis of the 'Nannochloris-like' algae and diagnoses of Picochlorum oklahomensis gen. et sp. nov. (Trebouxiophyceae, Chlorophyta). Phycologia 43:641-652. https://doi.org/10.2216/i0031-8884-43-6-641.1
  19. Hodac, L., Hallmann, C., Spitzer, K., Elster, J., Fasshauer, F., Brinkmann, N., Lepka, D., Diwan, V. & Friedl, T. 2016. Widespread green algae Chlorella and Stichococcus exhibit polar-temperate and tropical-temperate biogeography. FEMS Microbiol. Ecol. 92:fiw122. https://doi.org/10.1093/femsec/fiw122
  20. Holzinger, A. & Karsten, U. 2013. Desiccation stress and tolerance in green algae: consequences for ultrastructure, physiological and molecular mechanisms. Front. Plant Sci. 4:327. https://doi.org/10.3389/fpls.2013.00327
  21. Holzinger, A. & Pichrtova, M. 2016. Abiotic stress tolerance of charophyte green algae: new challenges for omics techniques. Front. Plant Sci. 7:678.
  22. Hotter, V., Glaser, K., Hartmann, A., Ganzera, M. & Karsten, U. 2018. Polyols and UV-sunscreens in the Prasiola-clade (Trebouxiophyceae, Chlorophyta) as metabolites for stress response and chemotaxonomy. J. Phycol. 54:264-274. https://doi.org/10.1111/jpy.12619
  23. Kamiya, M., West, J. A., Karsten, U. & Ganesan, E. K. 2016. Molecular and morphological delineation of Caloglossa beccarii and related species (Delesseriaceae, Rhodophyta). Phycologia 55:640-649. https://doi.org/10.2216/16-19.1
  24. Karsten, U., Friedl, T., Schumann, R., Hoyer, K. & Lembcke, S. 2005. Mycosporine-like amino acids and phylogenies in green algae: Prasiola and its relatives from the Trebouxiophyceae (Chlorophyta). J. Phycol. 41:557-566. https://doi.org/10.1111/j.1529-8817.2005.00081.x
  25. Karsten, U., Gors, S., Eggert, A. & West, J. A. 2007. Trehalose, digeneaside, and floridoside in the Florideophyceae (Rhodophyta): a reevaluation of its chemotaxonomic value. Phycologia 46:143-150. https://doi.org/10.2216/06-29.1
  26. Karsten, U., Herburger, K. & Holzinger, A. 2016. Living in biological soil crust communities of African deserts: physiological traits of green algal Klebsormidium species (Streptophyta) to cope with desiccation, light and temperature gradients. J. Plant Physiol. 194:2-12. https://doi.org/10.1016/j.jplph.2015.09.002
  27. Karsten, U., West, J. A., Zuccarello, G. C., Nixdorf, O., Barrow, K. D. & King, R. J. 1999. Low molecular weight carbohydrate patterns in the Bangiophyceae (Rhodophyta). J. Phycol. 35:967-976. https://doi.org/10.1046/j.1529-8817.1999.3550967.x
  28. Kitzing, C., Proschold, T. & Karsten, U. 2014. UV-induced effects on growth, photosynthetic performance and sunscreen contents in different populations of the green alga Klebsormidium fluitans (Streptophyta) from alpine soil crusts. Microb. Ecol. 67:327-340. https://doi.org/10.1007/s00248-013-0317-x
  29. Medwed, C., Holzinger, A., Hofer, S., Hartmann, A., Michalik, D., Glaser, K. & Karsten, U. 2021. Ecophysiological, morphological, and biochemical traits of free-living Diplosphaera chodatii (Trebouxiophyceae) reveal adaptation to harsh environmental conditions. Protoplasma Advanced online publication. https://doi.org/10.1007/s00709-021-01620-6.
  30. Moewus, L. 1951. Systematische Bestimmung einzelliger gruner Algen auf Grund von Kulturversuchen (Sphaerosorus composita, Oocystis marina und Pseudostichococcus monallantoides). Bot. Not. 4:287-318.
  31. Muller, K., Muller, J., Neinhuis, C. & Quandt, D. 2010. PhyDE: Phylogenetic data editor, version 0.9971. Available from: http://www.phyde.de. Accessed May 30, 2021.
  32. Mutaf, T., Oz, Y., Kose, A., Elibol, M. & Oncel, S. S. 2019. The effect of medium and light wavelength towards Stichococcus bacillaris fatty acid production and composition. Bioresour. Technol. 289:121732. https://doi.org/10.1016/j.biortech.2019.121732
  33. Neustupa, J., Elias, M. & Sejnohova, L. 2007. A taxonomic study of two Stichococcus species (Trebouxiophyceae, Chlorophyta) with a starch-enveloped pyrenoid. Nova Hedwigia 84:51-63. https://doi.org/10.1127/0029-5035/2007/0084-0051
  34. Neustupa, J. & Skaloud, P. 2008. Diversity of subaerial algae and cyanobacteria on tree bark in tropical mountain habitats. Biologia 63:806-812. https://doi.org/10.2478/s11756-008-0102-3
  35. Neustupa, J. & Skaloud, P. 2010. Diversity of subaerial algae and cyanobacteria growing on bark and wood in the lowland tropical forests of Singapore. Plant Ecol. Evol. 143:51-62. https://doi.org/10.5091/plecevo.2010.417
  36. Olivieri, G., Marzocchella, A., Andreozzi, R., Pinto, G. & Pollio, A. 2011. Biodiesel production from Stichococcus strains at laboratory scale. J. Chem. Technol. Biotechnol. 86:776-783. https://doi.org/10.1002/jctb.2586
  37. Oren, A. & Gunde-Cimerman, N. 2007. Mycosporines and mycosporine-like amino acids: UV protectants or multipurpose secondary metabolites? FEMS Microbiol. Lett. 269:1-10. https://doi.org/10.1111/j.1574-6968.2007.00650.x
  38. Orfanoudaki, M., Hartmann, A., Ngoc, H. N., Gelbrich, T., West, J., Karsten, U. & Ganzera, M. 2020. Mycosporinelike amino acids, brominated and sulphated phenols: suitable chemotaxonomic markers for the reassessment of classification of Bostrychia calliptera (Ceramiales, Rhodophyta). Phytochemistry 174:112344. https://doi.org/10.1016/j.phytochem.2020.112344
  39. Pollio, A., Aliotta, G., Pinto, G., Paterno, M. & Bevilacqua, A. 1997. Ecophysiological characters and biochemical composition of Stichococcus bacillaris Naegeli strains from low pH environments. Algol. Stud. 84:129-143. https://doi.org/10.1127/algol_stud/84/1997/129
  40. Posada, D. 2008. jModelTest: phylogenetic model averaging. Mol. Biol. Evol. 25:1253-1256. https://doi.org/10.1093/molbev/msn083
  41. Proschold, T. & Darienko, T. 2020. The green puzzle Stichococcus (Trebouxiophyceae, Chlorophyta): new generic and species concept among this widely distributed genus. Phytotaxa 441:113-142. https://doi.org/10.11646/phytotaxa.441.2.2
  42. Proschold, T., Darienko, T. & Guiry, M. D. 2020. Nomenclatural corrections in the green algal genus Deuterostichococcus Proschold & Darienko (Trebouxiophyceae). Notulae Algarum 137:1-2.
  43. Rambaut, A. 2008. Figtree version 1.2.2. Institute of Evolutionary Biology, University of Edinburgh. Available from: http://tree.bio.ed.ac.uk/software/figtree. Accessed May 30, 2021.
  44. Rindi, F. 2007. Diversity, distribution and ecology of green algae and cyanobacteria in urban habitats. In Seckbach, J. (Ed.) Algae and Cyanobacteria in Extreme Environments: Cellular Origina, Life in Extreme Habitats and Astrobiology. Springer, Dordrecht, pp. 619-638.
  45. Roberts, M. F. 2005. Organic compatible solutes of halotolerant and halophilic microorganisms. Saline Syst. 1:5. https://doi.org/10.1186/1746-1448-1-5
  46. Sommer, V., Karsten, U. & Glaser, K. 2020a. Halophilic algal communities in biological soil crusts isolated from potash tailings pile areas. Front. Ecol. Evol. 8:46. https://doi.org/10.3389/fevo.2020.00046
  47. Sommer, V., Mikhailyuk, T., Glaser, K. & Karsten, U. 2020b. Uncovering unique green algae and cyanobacteria isolated from biocrusts in highly haline potash tailing pile habitats using an integrative approach. Microorganisms 8:1667. https://doi.org/10.3390/microorganisms8111667
  48. Starr, R. C. & Zeikus, J. A. 1993. Utex: the culture collection of algae at The University of Texas at Austin 1993 list of cultures. J. Phycol. 29:1-106. https://doi.org/10.1111/j.0022-3646.1993.00001.x
  49. Tavare, S. 1986. Some probabilistic and statistical problems in the analysis of DNA sequences. In Miura, R. (Ed.) Some Mathematical Questions in Biology: DNA Sequence Analysis. Vol. 17. Lectures on Mathematics in the Life Sciences. American Mathematical Society, Providence, RI, pp. 57-86.
  50. Thus, H., Muggia, L., Perez-Ortega, S., Favero-Longo, S. E., Joneson, S., O'Brien, H., Nelsen, M. P., Duque-Thus, R., Grube, M., Friedl, T., Brodie, J., Andrew, C. J., Lucking, R., Lutzoni, F. & Gueidan, C. 2011. Revisiting photobiont diversity in the lichen family Verrucariaceae (Ascomycota). Eur. J. Phycol. 46:399-415. https://doi.org/10.1080/09670262.2011.629788
  51. Uher, B. 2008. Spatial distribution of cyanobacteria and algae from the tombstone in a historic cemetery in Bratislava, Slovakia. Fottea 9:81-92. https://doi.org/10.5507/fot.2009.007
  52. Vinatzer, G. 1975. Neue Bodenalgen aus den Dolomiten. Plant Syst. Evol. 123:213-235. https://doi.org/10.1007/BF00989405

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