Abstract
Biological soil crusts (BSCs) represent a micro-ecosystem consisting of various microorganisms including algae in drylands worldwide. The green algal genus Klebsormidium is a typical member of such communities, and because of its filamentous morphology and sticky cells, it plays an ecological key role in the stabilization of soil surfaces. In the present study, we investigated for the first time the phylogeny and ecophysiological performance of five BSC Klebsormidium strains from the semi-arid Colorado Plateau, USA. The molecular phylogeny of rbcL sequences showed that these strains belong to two subclades, which have been described before from mainly humid habitats. During controlled dehydration, the effective quantum yield of photosystem II decreased during 370–430 min of exposure. After controlled rehydration, all strains recovered between 32.9 and 97.6% of the control, but with significant differences depending on the genetic lineage. All five isolates grew between 18.1 and 27.9 °C, with isolate-specific optimal growth temperatures. Similarly, all strains were grown under increasing photon fluence rates from 4 to 110 μmol photons m−2 s−1 with optima under the higher tested light levels. Two strains showed inhibition at higher photon fluence rates and hence low light requirements for growth. Photosynthesis under increasing photon fluence rates up to 314 μmol photons m−2 s−1 indicated again low light requirements, but with no photoinhibition. All results underline a pronounced plasticity of the ecophysiological traits of the investigated Klebsormidium strains, which allow these terrestrial algae to exploit the environmental gradients within BSCs in arid regions.
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Abe K, Mihara H, Hirano M (1998) Characteristics of growth and carotenoid accumulation of the aerial microalga Trentepohlia aurea in liquid culture. J Mar Biotech 6:53–58
Aigner S, Remias D, Karsten U, Holzinger A (2013) Unusual phenolic compounds contribute to ecophysiological performance in the purple-colored green alga Zygogonium ericetorum (Zygnematophyceae, Streptophyta) from a high-alpine habitat. J Phycol 49:648–660
Belnap J (1994) Potential role of cryptobiotic soil crust in semiarid rangelands. In: Monsen SB, Kitchen SG (eds) Proceedings: symposium on ecology, management, and restoration of intermountain annual rangelands. U.S. Department of Agriculture, National Forest Service, Intermountain Research Station, Fort Collins, pp 179–185
Belnap J (2002) Nitrogen fixation in biological soil crusts from southeast Utah, USA. Biol Fertil Soils 35:128–135
Belnap J (2003) Comparative structure of physical and biological soil crust. In: Belnap J, Lange OL (eds) Biological soil crusts: structure, function, and management. Springer, Berlin, pp 177–191
Belnap, Weber B, Büdel B (2016) Biological soil crusts as an organizing principle in drylands. In: Weber B, Büdel B, Belnap J (eds) Biological soil crusts: an organizing principle in drylands. Springer International Publishing, Cham, pp 3–13
Bischof K, Hanelt D, Tüg H, Karsten U, PEM B, Wiencke C (1998) Acclimation of brown algal photosynthesis to ultraviolet radiation in Arctic coastal waters (Spitsbergen, Norway). Polar Biol 20:388–395
Büdel B, Dulic T, Darienko T, Rybalka N, Friedl T (2016) Cyanobacteria and algae of biological soil crusts. In: Weber B, Büdel B, Belnap J (eds) Biological soil crusts: an organizing principle in drylands. Springer International Publishing, Cham, pp 55–80
Donner A, Glaser K, Borchhardt N, Karsten U (2016) Ecophysiological response on dehydration and temperature in terrestrial Klebsormidium (Streptophyta) isolated from biological soil crusts in Central European grasslands and forests. Microb Ecol DOI: 10.1007/s00248-016-0917-3.
Elbert W, Weber B, Burrows S, Steinkamp J, Büdel B, Andreae MO, Pöschl U (2012) Contribution of cryptogamic covers to the global cycles of carbon and nitrogen. Nat Geosci 5:459–462
Elster J (1999) Algal versatility in various extreme environments. In: Seckbach J (ed) Enigmatic microorganisms and life in extreme environments. Springer, Dordrecht, pp 215–227
Garcia-Pichel F, Felde V, Drahorad S, Weber B (2016) Microstructure and weathering processes within biological soil crusts. In: Weber B, Büdel B, Belnap J (eds) Biological soil crusts: an organizing principle in drylands. Springer International Publishing, Cham, pp 237–255
Glaser K, Donner A, Albrecht M, Mikhailyuk T, Karsten U (2017) Habitat-specific composition of morphotypes with low genetic diversity in the green algal genus Klebsormidium (Streptophyta) isolated from biological soil crusts in Central European grasslands and forests. Eur J Phycol, DOI: 10.1080/09670262.2016.1235730
Gray DW, Lewis LA, Cardon ZG (2007) Photosynthetic recovery following desiccation of desert green algae (Chlorophyta) and their aquatic relatives. Plant Cell Environ 30:1240–1255
Gustavs L, Schumann R, Eggert A, Karsten U (2009) In vivo growth fluorometry: accuracy and limits of microalgal growth rate measurements in ecophysiological investigations. Aquat Microb Ecol 55:95–104
Henley WJ (1993) Measurement and interpretation of photosynthetic light-response curves in algae in the context of photoinhibition and diel changes. J Phycol 29:729–739
Hepperle D (2004) SeqAssem. Version: Sequentix. A sequence analysis tool, Contig assembler.
Herburger K, Holzinger A (2015) Localization and quantification of callose in the Streptophyte green algae Zygnema and Klebsormidium: correlation with desiccation tolerance. Plant Cell Physiol 56:2259–2270
Holzinger A, Karsten U (2013) Desiccation stress and tolerance in green algae: consequences for ultrastructure, physiological and molecular mechanisms. Front Plant Sci 4:327
Hori K, Maruyama F, Fujisawa T, Togashi T, Yamamoto N, Seo M et al (2014) Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation. Nat Commun 5:1–9
Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinform 17:754–755
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. J Phycol 46:1187–1197
Karsten U, Rindi F (2010) Ecophysiological performance of an urban strain of the aeroterrestrial green alga Klebsormidium sp. (Klebsormidiales, Klebsormidiophyceae). Eur J Phycol 45:426–435
Karsten U, Holzinger A (2012) Light, temperature, and desiccation effects on photosynthetic activity, and drought-induced ultrastructural changes in the green alga Klebsormidium dissectum (Streptophyta) from a high alpine soil crust. Microb Ecol 63:51–63
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. J Phycol 50:804–816
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
Lokhorst GM (1996) Comparative taxonomic studies on the genus Klebsormidium (Charophyceae) in Europe. Cryptogamic studies 5. Gustav Fischer Verlag, Stuttgart, p 132
Mikhailyuk T, Holzinger A, Massalski A, Karsten U (2014) Morphological and ultrastructural aspects of phylogenetically closely related genera Interfilum and Klebsormidium (Klebsormidiales, Streptophyta). Eur J Phycol 49:395–412
Mikhailyuk T, Glaser K, Holzinger A, Karsten U (2015) Biodiversity of Klebsormidium (Streptophyta) from alpine biological soil crusts (Alps, Tyrol, Austria, and Italy). J Phycol 51:750–767
Nylander JA (2004) MrModeltest v2. Version. Evolutionary Biology Centre, Uppsala University, Sweden
Pichrtová M, Hájek T, Elster J (2014) Osmotic stress and recovery in field populations of Zygnema sp. (Zygnematophyceae, Streptophyta) on Svalbard (high Arctic) subjected to natural desiccation. FEMS Microb Ecol 89:270–280
R Development Core Team (2009) R. A language and environment for statistical computing. Version: R foundation for statistical computing (http://www.R-project.org).
Raanan H, Felde V, Peth S, Drahorad S, Ionescu D, Gil E et al (2016) Three-dimensional structure and cyanobacterial activity within a desert biological soil crust. Environ Microbiol 18:372–383
Raven JA (2011) The cost of photoinhibition. Physiol Plant 142:87–104
Rindi F, Mikhailyuk T, Sluiman HJ, Friedl T, Lopez-Bautista JM (2011) Phylogenetic relationships in Interfilum and Klebsormidium (Klebsormidiophyceae, Streptophyta). Mol Phylogenet Evol 58:218–231
Rosentreter R, Belnap J (2003) Biological soil crusts of North Amercia. In: Belnap J, Lange OL (eds) Biological soil crusts: structure, function, and management. Springer, Berlin, pp 31–50
Ryšánek D, Hrčková K, Škaloud P (2015) Global ubiquity and local endemism of free-living terrestrial protists: phylogeographic assessment of the streptophyte alga Klebsormidium. Environ Microbiol 17:689–698
Schreiber U, Bilger W (1993) Progress in chlorophyll fluorescence research: major developments during the past years in retrospect. In: Behnke HD, Lüttge U, Esser K, Kadereit JW, Runge M (eds) Progress in botany. Springer, Berlin, pp 151–173
Škaloud P, Lukesová A, Malavasi V, Ryšánek D, Hrcková K, Rindi F (2014) Molecular evidence for the polyphyletic origin of low pH adaptation in the genus Klebsormidium (Klebsormidiophyceae, Streptophyta). Plant Ecol Evol 147:333–345
Škaloud P, Rindi F (2013) Ecological differentiation of cryptic species within an asexual protist morphospecies: a case study of filamentous green alga Klebsormidium (Streptophyta). J Eukaryot Microb 60:350–362
Starr RC, Zeikus JA (1993) UTEX—the culture collection of algae at the University of Texas at Austin 1993 list of cultures. J Phycol 29:1–106
Swofford DL (2002) PAUP* phylogenetic analysis using parsimony (∗and other methods). Version 4. Version 4. Sinauer Associates, Sunderland
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729
Tan CK, Lee YK, Ho KK (1993) Effect of light intensity and ammonium-N on carotenogenesis of Trentepohlia odorata and Dunaliella bardawil. J Appl Phycol 5:547–549
Thompson JD, Higgins DG, Gibson TJ (1994) Clustal-W—improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Walsby AE (1997) Numerical integration of phytoplankton photosynthesis through time and depth in a water column. New Phytol 136:189–209
Williams L, Borchhardt N, Colesie C, Baum C, Komsic-Buchmann K, Rippin M et al (2017) Biological soil crusts of Arctic Svalbard and of Livingston Island, Antarctica. Polar Biol 40:399–411
Woelfel J, Schoknecht A, Schumann R, Karsten, U (2014) Growth and primary production characteristics of three benthic diatoms from the brackish Southern Baltic Sea in relation to varying environmental conditions. Phycologia 53:639–651
Zwickl DJ (2006) Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. The University of Texas at Austin, USA
Acknowledgments
We thank Dr. Karin Glaser (University of Rostock) for support with the statistical data analysis. DR was supported by Charles University Science Foundation [GAUK no. 1544214], TM thanks the Alexander von Humboldt Foundation for financial support in the frame of a Georg-Forster-Fellowship, and UK greatly appreciates funding by the German Research Council (DFG) (KA899/16).
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Donner, A., Ryšánek, D., Mikhailyuk, T. et al. Ecophysiological traits of various genotypes of a green key alga in biological soil crusts from the semi-arid Colorado Plateau, USA. J Appl Phycol 29, 2911–2923 (2017). https://doi.org/10.1007/s10811-017-1158-7
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DOI: https://doi.org/10.1007/s10811-017-1158-7