Influence of substrate and pH on the diversity of the aeroterrestrial alga Klebsormidium (Klebsormidiales, Streptophyta): A potentially important factor for sympatric speciation

Phycologia

Volumn 55, Issue 4, 2016, Pages 347-358

  Ryšánek, David ^a   Holzinger, Andreas ^b   Škaloud, Pavel ^a  

^a CHARLES UNIVERSITY   (Czech Republic)

^b UNIVERSITY OF INNSBRUCK   (Austria)

Author keywords

Diversity; Klebsormidium; PH; Protist; Speciation

Indexed keywords

EID: 84975522473     PISSN: 00318884     EISSN: 23302968     Source Type: Journal    
DOI: 10.2216/15-110.1     Document Type: Article

References (92)

1. AGUILERA A., ZETTLER E., GOMEZ F., AMARAL-ZETTLER L., RODRIGUEZ N. & AMILS R. 2007. Distribution and seasonal variability in the benthic eukaryotic community of RioTinto (SW, Spain), an acidic, high metal extreme environment. Systematic and Applied Microbiology 30: 531-546.
2. ALLEN E.D. & SPENCE D.H.N. 1981. The differential ability of aquatic plants to utilize the inorganic carbon supply in fresh waters. New Phytologist 87: 269-283.
3. AMATO A., KOOISTRA W.H.C.F., GHIRON J.H.L., MANN D.G., PRÖSCHOLD T. & MONTRESOR M. 2007. Reproductive isolation among sympatric cryptic species in marine diatoms. Protist 158: 193-207.
4. BABA M. & SHIRAIWA Y. 2012. High-CO2 response mechanisms in microalgae. In: Advances in photosynthesis-fundamental aspects (Ed. by Mohammad Najafpour), pp. 299-320. InTech, Rijeka, Croatia.
5. BATES S.T., CLEMENTE J.C., FLORES G.E., WALTERS W.A., PARFREY L.W., KNIGHT R. & FIERER N. 2012. Global biogeography of highly diverse protistan communities in soil. The ISME Journal 7: 1-8.
6. BENTON M.J. & PEARSON P.N. 2001. Speciation in the fossil record. Trends in Ecology & Evolution 16: 405-411.
7. BIRKY JR. C.W., Adams J., Gemmel M. & Perry J. 2010. Using population genetic theory and DNA sequences for species detection and identification in asexual organisms. PLoS One 5(5): e10609. doi: 10.1371/journal.pone.0010609
8. BROCK T.D. 1973. Lower pH limit for existence of blue-green algae: evolutionary and ecological implications. Science 179: 480-483.
9. CARON D.A. 2009. Past president's address: protistan biogeography: why all the fuss? Journal of Eukaryotic Microbiology 56: 105-112.
10. CASTELEYN G., LELIAERT F., BACKELJAU T., DEBEER A.E., KOTAKI Y., RHODES L., LUNDHOLM N., SABBE K. & VYVERMAN W. 2010. Limits to gene flow in a cosmopolitan marine planktonic diatom. Proceedings of the National Academy of Sciences of the United States of America 107: 12952-12957.
11. DE MEESTER L., GOMEZ A., OKAMURA B. & SCHWENK K. 2002. The monopolization hypothesis and the dispersal-gene flow paradox in aquatic organisms. Acta Oecologica 23: 121-135.
12. DE VARGAS C., NORRIS R., ZANINETTI L., GIBB S.W. & PAWLOWSKI J. 1999. Molecular evidence of cryptic speciation in planktonic foraminifers and their relation to oceanic provinces. Proceedings of the National Academy of Sciences of the United States of America 96: 2864-2868.
13. DESROSIERS C., LEFLAIVE J., EULIN A. & TEN-HAGE L. 2013. Bioindicators in marine waters: benthic diatoms as a tool to assess water quality from eutrophic to oligotrophic coastal ecosystems. Ecological Indicators 32: 25-34.
14. ELSTER J., DEGMA P., KOVÁČÍK L., VALENTOVÁ L., ŠRAMKOVÁ K. & PEREIRA A.B. 2008. Freezing and desiccation injury resistance in the filamentous green alga Klebsormidium from the Antarctic, Arctic and Slovakia. Biologia 63: 843-851.
15. EVANS K.M., CHEPURNOV V.A., SLUIMAN H.J., THOMAS S.J., SPEARS B.M. & MANN D.G. 2009. Highly differentiated populations of the fresh water diatom Sellaphora capitata suggest limited dispersal and opportunities for allopatric speciation. Protist 160: 386-396.
16. FALKOWSKI P.G. & RAVEN J.A. 2007. Aquatic photosynthesis. Princeton University Press, Princeton, New Jersey. 488 pp.
17. FENCHEL T. & FINLAY B.J. 2003. Is microbial diversity fundamentally different from biodiversity of larger animals and plants? European Journal of Protistology 39: 486-490.
18. FENCHEL T. & FINLAY B.J. 2004. The ubiquity of small species: patterns of local and global diversity. Bioscience 54: 777-784.
19. FINLAY B.J. 2002. Global dispersal of free-living microbial eukaryote species. Science 296: 1061-1063.
20. FINLAY B.J. & FENCHEL T. 1999. Divergent perspective on protist species richness. Protist 150: 229-233.
21. FINLAY B.J., MONAGHAN E.B. & MABERLY S.C. 2002. Hypothesis: the rate and scale of dispersal of fresh water diatom species is a fiction of their global abundance. Protist 153: 261-273.
22. FOISSNER W. 2006. Biogeography and dispersal of micro-organisms: a review emphasizing protists. Acta Protozoologica 45: 111-136.
23. FOISSNER W., CHAO A. & KATZ L.A. 2008. Diversity and geographic distribution of ciliates (Protista: Ciliophora). Biodiversity and Conservation 17: 235-242.
24. FONTANETO D., HERNIOU E.A., BOSCHETTI C., CAPRIOLI M., MELONE G., RICCI C. & BARRACLOUGH T.G. 2007. Independently evolving species in asexual bdelloid rotifers. PLoS Biology 5: e87. doi: 10. 1371/journal.pbio.0050087
25. GÄCHTER E. & WEISSE T. 2006. Local adaptation among geographically distant clones of the cosmopolitan freshwater ciliate Meseres corlissi. I. Temperature response. Aquatic Microbial Ecology 45: 291-300.
26. GAYSINA L.A., PURINA E.S., SAFIULLINA L.M. & BAKIEVA G.R. 2009. Resistance of Klebsormidium flaccidum (Streptophyta) to heavy metals. Plant Sciences 3: 39-41.
27. GROSS W. 2000. Ecophysiology of algae living in highly acidic environments. Hydrobiologia 433: 31-37.
28. HALLMANN C., STANNEK L., FRITZLAR D., HAUSE-REITNER D., FRIEDL T. & HOPPERT M. 2013. Molecular diversity of phototrophic biofilms on building stone. FEMS Microbiology Ecology 84: 355-372.
29. HAMMER O., HARPER D.A.T. & RYAN P.D. 2001. PAST: Paleontological Statistics software package for education and data analysis. Palaeontologia Electronica 4(1): 9
30. HEPPERLE D. 2004. SeqAssem© A sequence analysis tool, contig assembler and trace data visualisation tool for molecular sequences, version 09/2004. http://www.sequentix.de.
31. HERBURGER K. & HOLZINGER A. 2015. Localization and quantification of callose in the streptophyte green algae Zygnema and Klebsormidium: Correlation with desiccation tolerance. Plant and Cell Physiology 56: 2259-2270.
32. HERBURGER K., KARSTEN U. & HOLZINGER A. 2016. Entransia and Hormidiella, sister lineages of Klebsormidium (Streptophyta), respond differently to light, temperature and desiccation stress. Protoplasma in press doi: 10.1007/s00709-015-0889-z.
33. HOFFMANN L. 1989. Algae of terrestrial habitats. The BotanicalReview 55: 77-105.
34. HOLZINGER A. & BECKER B. 2015. Desiccation tolerance in the streptophyte green alga Klebsormidium: the role of phytohormones. Communicative and Integrative Biology 8: 4 e1059978. doi: 10.1080/19420889.2015.1059978
35. HOLZINGER A., KAPLAN F., BLAAS K., ZECHMANN B., KOMSICBUCHMANN K. & BECKER B. 2014. Transcriptomics of desiccation tolerance in the streptophyte green alga Klebsormidium reveal a land plant-like defense. PLoS One 9(10):e110630. doi: 10.1371/ journal.pone.0110630
36. HORI K., MARUYAMA F., FUJISAWA T., TOGASHI T., YAMAMOTO N., SEO M., SATO S., YAMADA T., MORI H., TAJIMA N., MORIYAMA T., IKEUCHI M., WATANABE M., WADA H., KOBAYASHI K., SAITO M., MASUDA T., SASAKI-SEKIMOTO Y., MASHIGUCHI K., AWAI K., SHIMOJIMA M., MASUDA S., IWAI M., NOBUSAWA T., NARISE T., KONDO S., SAITO H., SATO R., MURAKAWA M., IHARA Y., OSHIMAYAMADA Y., OHTAKA K., SATOH M., SONOBE K., ISHII M., OHTANI R., KANAMORI-SATO M., HONOKI R., MIYAZAKI D., MOCHIZUKI H., UMETSU J., HIGASHI K., SHIBATA D., KAMIYA Y., SATO N., NAKAMURA Y., TABATA S., IDA S., KUROKAWA K., & OHTA H. 2014. Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation. Nature Communications 5: 3978.
37. HUELSENBECK J.P. & RONQUIST F. 2001. MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17: 754-755.
38. HUSS V.A.R., FRANK C., HARTMANN E.C., HIRMER M., KLOBOUCEK A., SEIDEL B.M., WENZELER P. & KESSLER E. 1999. Biochemical taxonomy and molecular phylogeny of the genus Chlorella sensu lato (Chlorophyta). Journal of Phycology 35: 587-598.
39. HUSS V.A.R., CINIGLIA C., CENNAMO P., COZZOLINO S., PINTO G., & POLLIO A. 2002. Phylogenetic relationships and taxonomic position of Chlorella-like isolates from low pH environments (pH, 3.0). BMC Evolutionary Biology 26: 2-13.
40. KAPLAN F., LEWIS L.A., WASTIAN J. & HOLZINGER A. 2012. Plasmolysis effects and osmotic potential of two phylogenetically distinct alpine strains of Klebsormidium (Streptophyta). Protoplasma 249: 789-804.
41. KARSTEN U. & HOLZINGER A. 2012. Light, temperature, and desiccation effects on photosynthetic activity, and droughtinduced ultrastructural changes in the green alga Klebsormidium dissectum (Streptophyta) from a high alpine soil crust. Microbial Ecology 63: 51-63.
42. KARSTEN U. & HOLZINGER A. 2014. Green algae in alpine biological soil crust communities: acclimation strategies against ultraviolet radiation and dehydration. Biodiversity and Conservation 23: 1845-1858.
43. KARSTEN U., LÜTZ C. & HOLZINGER A. 2010. Ecophysiological performance of the aeroterrestrial green alga Klebsormidium crenulatum (Charophyceae, Streptophyta) isolated from an alpine soil crust with an emphasis on desiccation stress. Journal of Phycology 46: 1187-1197.
44. KARSTEN U., PRÖSCHOLD T., MIKHAILYUK T. & HOLZINGER A. 2013. Photosynthetic performance of different genotypes of the green alga Klebsormidium sp. (Streptophyta) isolated from biological soil crusts of the Alps. Algological Studies 142: 45-62.
45. KARSTEN U., HERBURGER K. & HOLZINGER A. 2014. Dehydration, temperature and light tolerance in members of the aeroterrestrial green algal genus Interfilum (Streptophyta) from biogeographically different temperate soils. Journal of Phycology 50: 804-816.
46. 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. Journal of Plant Physiology in press doi: 10.1016/j.jplph.2015.09.002.
47. KITZING C. & KARSTEN U. 2015. UV-induced effects on growth, photosynthetic performance and sunscreen contents in members of the genera Interfilum, Klebsormidium, Hormidiella and Entransia (Klebsormidiophyceae, Streptophyta). European Journal of Phycology 50: 279-287.
48. KITZING C., PRÖSCHOLD 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. Microbial Ecology 67: 327-340.
49. LANE A.E. & BURRIS J.E. 1981. Effects of environmental pH on the internal pH of Chlorella pyrenoidosa, Scenedesmus quadricauda and Euglena mutabilis. Plant Physiology 68: 439-442.
50. LOGARES R., RENGEFORS K., KREMP A., SHALCHIAN-TABRIZI K., BOLTOVSKOY A., TENGS T., SHURTLEFF A. & KLAVENESS D. 2007. Phenotypically different microalgal morphospecies with identical ribosomal DNA: a case of rapid adaptive evolution? Microbial Ecology 53: 549-561.
51. LOMIN S.N., KRIVOSHEEV D.M., STEKLOV M.Y., ARKHIPOV D.V., OSOLODKIN D.I., SCHMÜLLING T. & ROMANOV G.A. 2015. Plant membrane assays with cytokinin receptors underpin the unique role of free cytokinin bases as biologically active ligands. Journal of Experimental Botany 66: 1851-1863.
52. LOWE R.L., FUREY P.C., RESS J.A. & JOHANSEN J.R. 2007. Diatom biodiversity and distribution on wet walls in Great Smoky Mountains National Park. Southeastern Naturalist 6: 135-152.
53. LUKEŠOVÁ A. 2001. Soil algae in brown coal and lignite post-mining areas in central Europe (Czech Republic and Germany). Restoration Ecology 9: 341-350.
54. LUKEŠOVÁ A. & HOFFMANN L. 1995. Soil algae from acid rain impacted forest areas of Krušnéhory mountains (Czech Republic). 2. Effects of pH on growth. Algological Studies 78: 39-51.
55. MACHOVÁ-ČERNÁ K. & NEUSTUPA J. 2009. Spatial distribution of algal assemblages in a temperate lowland peat bog. International Review of Hydrobiology 94: 40-56.
56. MIKHAILYUK T., HOLZINGER A., MASSALSKI A. & KARSTEN U. 2014. Morphology and ultrastructure of Interfilum and Klebsormidium (Klebsormidiales, Streptophyta) with special reference to cell division and thallus formation. European Journal of Phycology 49: 395-412.
57. MIKHAILYUK T., GLASER K., HOLZINGER A. & KARSTEN U. 2015. Biodiversity of Klebsormidium (Streptophyta) from alpine biological soil crusts (Alps, Tyrol, Austria and Italy). Journal of Phycology 51: 750-767.
58. MONIZ M.B., RINDI F., NOVIS P.M., BROADY P.A. & GUIRY M.D. 2012. Molecular phylogeny of antarctic Prasiola (Prasiolales, Trebouxiophyceae) reveals extensive cryptic diversity. Journal of Phycology 48: 940-955.
59. NAGAO M., MATSUI K. & UEMURA M. 2008. Klebsormidium flaccidum, a charophycean green alga, exhibits cold acclimation that is closely associated with compatible solute accumulation and ultrastructural changes. Plant, Cell & Environment 31: 872-885.
60. NOVIS P.M. 2006. Taxonomy of Klebsormidium (Klebsormidiales, Charophyceae) in New Zealand streams and the significance of low-pH habitats. Phycologia 45: 293-301.
61. NOVIS P.M. & HARDING J.S. 2007. Extreme acidophiles: freshwater algae associated with acid mine drainage. In: Extremophilic algae, cyanobacteria and non-photosynthetic protists: from prokaryotes to astrobiology (Ed. by J. Seckbach), pp. 445-463. Springer Verlag, Dordrecht, the Netherlands
62. NYLANDER J.A.A. 2004. MrModeltest, version 2. http://www.abc.se/ ñylander
63. PEKSA O. & ŠKALOUD P. 2011. Do photobionts influence the ecology of lichens? A case study of environmental preferences in symbiotic green alga Asterochloris (Trebouxiophyceae). Molecular Ecology 20: 3936-3948.
64. PIETRASIAK N., JOHANSEN J.R. & DRENOVSKY R.E. 2011. Geologic composition influences distribution of microbiotic crusts in the Mojave and Colorado Deserts at the regional scale. Soil Biology and Biochemistry 43: 967-974.
65. R Core Team. 2016. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, version R 2.15.1. http://www.R-project.org/.
66. REYNOLDS C.S. 1984. The ecology of freshwater phytoplankton. Cambridge University Press, Cambridge, UK. 384 pp.
67. RINDI F. & GUIRY M.D. 2002. Diversity, life history and ecology of Trentepohlia and Printzina (Trentepohliales, Chlorophyta) in urban habitats in western Ireland. Journal of Phycology 38: 39-54.
68. RINDI F. & GUIRY M.D. 2004. Composition and spatial variability of terrestrial algal assemblages occurring at the bases of urban walls in Europe. Phycologia 43: 225-235.
69. RINDI F., MCIVOR L., SHERWOOD A.R., FRIEDL T., GUIRY M.D. & SHEATH R.G. 2007. Molecular phylogeny of the green algal order Prasiolales (Trebouxiophyceae, Chlorophyta). Journal of Phycology 43: 811-822.
70. RINDI F., GUIRY M.D. & LÓPEZ-BAUTISTA J.M. 2008. Distribution, morphology, and phylogeny of Klebsormidium (Klebsormidiales, Charophyceae) in urban environment in Europe. Journal of Phycology 44: 1529-1540.
71. RINDI F., MIKHAILYUK T.I., SLUIMAN H.J., FRIEDL T. & LÓPEZBAUTISTA J.M. 2011. Phylogenetic relationships in Interfilum and Klebsormidium (Klebsormidiophyceae, Streptophyta). Molecular Phylogenetics and Evolution 58: 218-231.
72. RYŠÁNEK D., HRČKOVÁ K. & ŠKALOUD P. 2015. Global ubiquity and local endemism of free-living terrestrial protists: phylogeographic assessment of the streptophyte alga Klebsormidium. Environmental Microbiology 17: 689-698.
73. SHELP B.J. & CANVIN D.T. 1980. Utilization of exogenous inorganic carbon species in photosynthesis by Chlorella pyrenoidosa. Plant Physiology 65: 774-779.
74. SHIELDS L.M. & DURELL L.W. 1964. Algae in relation to soil fertility. The Botanical Review 30: 92-128.
75. SHIRAIWA Y., GOYAL A. & TOLBERT N.E. 1993. Alkalization of the medium by unicellular green algae during uptake dissolved inorganic carbon. Plant and Cell Physiology 34: 649-657.
76. SILVA P.C., MATTOX K.R. & BLACKWELL W.H. 1972. The generic name Hormidium as applied to green algae. Taxon 21: 639-645.
77. ŠKALOUD P. & PEKSA O. 2010. Evolutionary inferences based on ITS rDNA and actin sequences reveal extensive diversity of the common lichen alga Asterochloris (Trebouxiophyceae, Chlorophyta). Molecular Phylogenetics and Evolution 54: 36-46.
78. ŠKALOUD P. & RINDI F. 2013. Ecological differentiation of cryptic species within an asexual protest morphospecies: a case study of filamentous green alga Klebsormidium (Streptophyta). Journal of Eukaryotic Microbiology 60: 350-362.
79. ŠKALOUD P., KYNČLOVÁA., BENADA O., KOFROŇOVÁO. & ŠKALOUDOVÁ M. 2012. Toward a revision of the genus Synura, section Petersenianae (Synurophyceae, Heterokontophyta): morphological characterization of six pseudo-cryptic species. Phycologia 51: 303-329.
80. ŠKALOUD P., LUKEŠOVÁ A., MALAVASI V., RYŠÁNEK D., HRČKOVÁ K. & RINDI F. 2014. Molecular evidence for the polyphyletic origin of low pH adaptation in the genus Klebsormidium (Klebsormidiophyceae, Streptophyta). Plant Ecology and Evolution 147: 333-345.
81. SLUIMAN H.J., GUIHAL C. & MUDIMU O. 2008. Assessing phylogenetic affinities and species deliminations in Klebsormidiales (Streptophyta): nuclear-encoded rDNA phylogenies and ITS secondary structure models in Klebsormidium, Hormidiella, and Entransia. Journal of Phycology 44: 183-195.
82. STARKS T.L., SHUBERT L.E. & TRAINOR F.R. 1981. Ecology of soil algae: a review. Phycologia 20: 65-80.
83. STARR R.C. & ZEIKUS J.A. 1993. UTEX -the Culture Collection of Algae at the University of Texas at Austin 1993 List of Cultures. Journal of Phycology 29: 1-106.
84. SVOBODA P., KULICHOVÁ J. & ŠŤASTNÝ J. 2014. Spatial and temporal community structure of desmids on a small spatial scale. Hydrobiologia 722: 291-303.
85. SWOFFORD D.L. 2002. PAUP∗. Phylogenetic Analysis Using Parsimony (∗and other methods). Version 4. Sinauer Associates, Sunderland, Massachusetts.
86. TAMURA K., PETERSON D., PETERSON N., STECHER G., NEI M. & KUMAR S. 2011. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28: 2731-2739.
87. THOMPSON J.D., HIGGINS D.G. & GIBSON T.J. 1994. CLUSTAL W: improving sensitivity of progressive multiple sequence alignment through sequence weighting, position 86 specific gap penalties, and weight matrix choice. Nucleic Acids Research 22: 4673-4680.
88. VANELSLANDER B., CREACH V., VANORMELINGEN P., ERNST A., CHEPURNOV V.A., SAHAN E. & SABBE K. 2009. Ecological differentiation between sympatric pseudocryptic species in the estuarine benthic diatom Navicula phyllepta (Bacillariophyceae). Journal of Phycology 45: 1278-1289.
89. VANORMELINGEN P., VYVERMAN W., DE BOCK D., VAN DER GUCHT K. & DE MEESTER L. 2009. Local genetic adaptation to grazing pressure of the green alga Desmodesmus armatus in a strongly connected pond system. Limnology and Oceanography 54: 503-511.
90. VON DER HEYDEN S., CHAO E. & CAVALIER-SMITH T. 2004. Genetic diversity of goniomonads: an ancient divergence between freshwater and marine species. European Journal of Phycology 39: 343-350.
91. WEISSE T. 2008. Distribution and diversity of aquatic protists: an evolutionary and ecological perspective. Biodiversity and Conservation 17: 243-259.
92. ZWICKL D.J. 2006. Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. Dissertation, The University of Texas at Austin, Texas. 115 pp. Available from Digital Repository, University of Texas Libraries. http://hdl.Handle. net/2152/2666.