Terrestrial adaptation of green algae Klebsormidium and Zygnema (Charophyta) involves diversity in photosynthetic traits but not in CO2 acquisition

. 2017 Nov ; 246 (5) : 971-986. [epub] 20170718

Jazyk angličtina Země Německo Médium print-electronic

Typ dokumentu srovnávací studie, časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid28721563

Grantová podpora
15-34645 L Grantová Agentura České Republiky
I 1951-B16 Austrian Science Fund
P 24242-B16 Austrian Science Fund
I 1951 Austrian Science Fund FWF - Austria
1544214 Grantová Agentura, Univerzita Karlova
P 24242 Austrian Science Fund FWF - Austria

Odkazy

PubMed 28721563
PubMed Central PMC5633629
DOI 10.1007/s00425-017-2741-5
PII: 10.1007/s00425-017-2741-5
Knihovny.cz E-zdroje

The basal streptophyte Klebsormidium and the advanced Zygnema show adaptation to terrestrialization. Differences are found in photoprotection and resistance to short-term light changes, but not in CO 2 acquisition. Streptophyte green algae colonized land about 450-500 million years ago giving origin to terrestrial plants. We aim to understand how their physiological adaptations are linked to the ecological conditions (light, water and CO2) characterizing modern terrestrial habitats. A new Klebsormidium isolate from a strongly acidic environment of a former copper mine (Schwarzwand, Austria) is investigated, in comparison to Klebsormidium cf. flaccidum and Zygnema sp. We show that these genera possess different photosynthetic traits and water requirements. Particularly, the Klebsormidium species displayed a higher photoprotection capacity, concluded from non-photochemical quenching (NPQ) and higher tolerance to high light intensity than Zygnema. However, Klebsormidium suffered from photoinhibition when the light intensity in the environment increased rapidly, indicating that NPQ is involved in photoprotection against strong and stable irradiance. Klebsormidium was also highly resistant to cellular water loss (dehydration) under low light. On the other hand, exposure to relatively high light intensity during dehydration caused a harmful over-reduction of the electron transport chain, leading to PSII damages and impairing the ability to recover after rehydration. Thus, we suggest that dehydration is a selective force shaping the adaptation of this species towards low light. Contrary to the photosynthetic characteristics, the inorganic carbon (C i ) acquisition was equivalent between Klebsormidium and Zygnema. Despite their different habitats and restriction to hydro-terrestrial environment, the three organisms showed similar use of CO2 and HCO3- as source of Ci for photosynthesis, pointing out a similar adaptation of their CO2-concentrating mechanisms to terrestrial life.

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Adlassnig W, Sassmann S, Lendl T, Wernitznig S, Hofhansl F, Lang I, Lichtscheidl IK. Metal contamination and retention of the former mining site Schwarzwand (Salzburg, Austria) Appl Geochem. 2013;35:196–206. doi: 10.1016/j.apgeochem.2013.04.012. DOI

Alboresi A, Caffarri S, Nogue F, Bassi R, Morosinotto T. In silico and biochemical analysis of Physcomitrella patens photosynthetic antenna: identification of subunits which evolved upon land adaptation. PLoS One. 2008;3:e2033. doi: 10.1371/journal.pone.0002033. PubMed DOI PMC

Alboresi A, Gerotto C, Giacometti GM, Bassi R, Morosinotto T. Physcomitrella patens mutants affected on heat dissipation clarify the evolution of photoprotection mechanisms upon land colonization. Proc Natl Acad Sci USA. 2010;107:11128–11133. doi: 10.1073/pnas.1002873107. PubMed DOI PMC

Bar-Eyal L, Eisenberg I, Faust A, Raanan H, Nevo R, Rappaport F, Krieger-Liszkay A, Sétif P, Thurotte A, Reich Z, Kaplan A, Ohad I, Paltiel Y, Keren N. An easily reversible structural change underlies mechanisms enabling desert crust cyanobacteria to survive desiccation. Biochim Biophys Acta. 2015;1847:1267–1273. doi: 10.1016/j.bbabio.2015.07.008. PubMed DOI

Becker B. Snow ball earth and the split of Streptophyta and Chlorophyta. Trends Plant Sci. 2013;18:180–183. doi: 10.1016/j.tplants.2012.09.010. PubMed DOI

Becker B, Marin B. Streptophyte algae and the origin of embryophytes. Ann Bot. 2009;103:999–1004. doi: 10.1093/aob/mcp044. PubMed DOI PMC

Birmingham BC, Colman B. Measurement of carbon dioxide compensation points of freshwater algae. Plant Physiol. 1979;64:892–895. doi: 10.1104/pp.64.5.892. PubMed DOI PMC

Brading P, Warner ME, Smith DJ, Suggett DJ. Contrasting modes of inorganic carbon acquisition amongst Symbiodinium (Dinophyceae) phylotypes. New Phytol. 2013;200:432–442. doi: 10.1111/nph.12379. PubMed DOI

Christa G, Cruz S, Jahns P, de Vries J, Cartaxana P, Esteves AC, Serôdio J, Gould SB. Photoprotection in a monophyletic branch of chlorophyte algae is independent of energy-dependent quenching (qE) New Phytol. 2017;214:1132–1144. doi: 10.1111/nph.14435. PubMed DOI

Collins S, Bell G. Phenotypic consequences of 1000 generations of selection at elevated CO2 in a green alga. Nature. 2004;431:566–569. doi: 10.1038/nature02945. PubMed DOI

Cruz de Carvalho R, Bernardes da Silva A, Soares R, Almeida AM, Coelho AV, Marques da Silva J, Branquinho C. Differential proteomics of dehydration and rehydration in bryophytes: evidence towards a common desiccation tolerance mechanism. Plant Cell Environ. 2014;37:1499–1515. doi: 10.1111/pce.12266. PubMed DOI

de Vries J, Stanton A, Archibald JM, Gould SB. Streptophyte terrestrialization in light of plastid evolution. Trends Plant Sci. 2016;21:467–476. doi: 10.1016/j.tplants.2016.01.021. PubMed DOI

de Vries J, de Vries S, Slamovits CH, Rose LE, Archibald JM. How embryophytic is the biosynthesis of phenylpropanoids and their derivatives in streptophyte algae? Plant Cell Physiol. 2017;58:934–945. doi: 10.1093/pcp/pcx037. PubMed DOI

Elbert W, Weber B, Burrows S, Steinkamp J, Büdel B, Andreae MO, Pöschl U. Contribution of cryptogamic covers to the global cycles of carbon and nitrogen. Nat Geosci. 2012;5:459–462. doi: 10.1038/ngeo1486. DOI

Gao S, Shen S, Wang G, Niu J, Lin A, Pan G. PSI-driven cyclic electron flow allows intertidal macro-algae Ulva sp. (Chlorophyta) to survive in desiccated conditions. Plant Cell Physiol. 2011;52:885–893. doi: 10.1093/pcp/pcr038. PubMed DOI

Gerloff-Elias A, Spijkerman E, Pröschold T. Effect of external pH on the growth, photosynthesis and photosynthetic electron transport of Chlamydomonas acidophila Negoro, isolated from an extremely acidic lake (pH 2.6) Plant Cell Environ. 2005;28:1218–1229. doi: 10.1111/j.1365-3040.2005.01357.x. DOI

Gerotto C, Morosinotto T. Evolution of photoprotection mechanisms upon land colonization: evidence of PSBS-dependent NPQ in late Streptophyte algae. Physiol Plant. 2013;149:583–598. doi: 10.1111/ppl.12070. PubMed DOI

Gerotto C, Alboresi A, Giacometti GM, Bassi R, Morosinotto T. Role of PSBS and LHCSR in Physcomitrella patens acclimation to high light and low temperature. Plant Cell Environ. 2011;34:922–932. doi: 10.1111/j.1365-3040.2011.02294.x. PubMed DOI

Giordano M, Beardall J, Raven JA. CO2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. Annu Rev Plant Biol. 2005;56:99–131. doi: 10.1146/annurev.arplant.56.032604.144052. PubMed DOI

Golding AJ, Johnson GN. Down-regulation of linear and activation of cyclic electron transport during drought. Planta. 2003;218:107–114. doi: 10.1007/s00425-003-1077-5. PubMed DOI

Goss R, Lepetit B. Biodiversity of NPQ. J Plant Physiol. 2015;172:13–32. doi: 10.1016/j.jplph.2014.03.004. PubMed DOI

Gray DW, Lewis LA, Cardon ZG. Photosynthetic recovery following desiccation of desert green algae (Chlorophyta) and their aquatic relatives. Plant Cell Environ. 2007;30:1240–1255. doi: 10.1111/j.1365-3040.2007.01704.x. PubMed DOI

Groom QJ, Kramer DM, Crofts AR, Ort DR. The non-photochemical reduction of plastoquinone in leaves. Photosynth Res. 1993;36:205–215. doi: 10.1007/BF00033039. PubMed DOI

Hagemann M, Kern R, Maurino VG, Hanson DT, Weber AP, Sage RF, Bauwe H. Evolution of photorespiration from cyanobacteria to land plants, considering protein phylogenies and acquisition of carbon concentrating mechanisms. J Exp Bot. 2016;67:2963–2976. doi: 10.1093/jxb/erw063. PubMed DOI

Heber U. Photoprotection of green plants: a mechanism of ultra-fast thermal energy dissipation in desiccated lichens. Planta. 2008;228:641–650. doi: 10.1007/s00425-008-0766-5. PubMed DOI

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

Herburger K, Holzinger A. Localization and quantification of callose in the streptophyte green algae Zygnema and Klebsormidium: correlation with desiccation tolerance. Plant Cell Physiol. 2015;56:2259–2270. PubMed PMC

Herburger K, Lewis LA, Holzinger A. Photosynthetic efficiency, desiccation tolerance and ultrastructure in two phylogenetically distinct strains of alpine Zygnema sp. (Zygnematophyceae, Streptophyta): role of pre-akinete formation. Protoplasma. 2015;252:571–589. doi: 10.1007/s00709-014-0703-3. PubMed DOI PMC

Holland DP, Pantorno A, Orr PT, Stojkovic S, Beardall J. The impacts of a high CO2 environment on a bicarbonate user: the cyanobacterium Cylindrospermopsis raciborskii. Water Res. 2012;46:1430–1437. doi: 10.1016/j.watres.2011.11.015. PubMed DOI

Holzinger A, Karsten U. Desiccation stress and tolerance in green algae: consequences for ultrastructure, physiological and molecular mechanisms. Front Plant Sci. 2013;4:327. doi: 10.3389/fpls.2013.00327. PubMed DOI PMC

Holzinger A, Pichrtová M. Abiotic stress tolerance of charophyte green algae: new challenges for omics techniques. Front Plant Sci. 2016;7:678. doi: 10.3389/fpls.2016.00678. PubMed DOI PMC

Holzinger A, Roleda MY, Lütz C. The vegetative arctic freshwater green alga Zygnema is insensitive to experimental UV exposure. Micron. 2009;40:831–838. doi: 10.1016/j.micron.2009.06.008. PubMed DOI

Holzinger A, Lütz C, Karsten U. Desiccation stress causes structural and ultrastructural alterations in the aeroterrestrial green alga Klebsormidium crenulatum (Klebsormidiophyceae, Streptophyta) isolated from an alpine soil crust1. J Phycol. 2011;47:591–602. doi: 10.1111/j.1529-8817.2011.00980.x. PubMed DOI

Holzinger A, Kaplan F, Blaas K, Zechmann B, Komsic-Buchmann K, Becker B. Transcriptomics of desiccation tolerance in the streptophyte green alga Klebsormidium reveal a land plant-like defense reaction. PLoS One. 2014;9:e110630. doi: 10.1371/journal.pone.0110630. PubMed DOI PMC

Hori K, Maruyama F, Fujisawa T, et al. Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation. Nat Commun. 2014;5:3978. doi: 10.1038/ncomms4978. PubMed DOI PMC

Huelsenbeck JP, Ronquist F. MRBAYES: bayesian inference of phylogenetic trees. Bioinformatics. 2001;17:754–755. doi: 10.1093/bioinformatics/17.8.754. PubMed DOI

IPCC (2014) Climate change 2014: synthesis report. In: Core Writing Team, Pachauri RK, Meyer LA (eds) Contribution of Working Groups I, II and III to the Fifth assessment report of the intergovernmental panel on climate change. IPCC, Geneva, Switzerland

Joliot P, Johnson GN. Regulation of cyclic and linear electron flow in higher plants. Proc Natl Acad Sci USA. 2011;108:13317–13322. doi: 10.1073/pnas.1110189108. PubMed DOI PMC

Kaplan F, Lewis LA, Herburger K, Holzinger A. Osmotic stress in Arctic and Antarctic strains of the green alga Zygnema (Zygnematales, Streptophyta): effects on photosynthesis and ultrastructure. Micron. 2013;44:317–330. doi: 10.1016/j.micron.2012.08.004. PubMed DOI PMC

Karsten U, Holzinger A. Green algae in alpine biological soil crust communities: acclimation strategies against ultraviolet radiation and dehydration. Biodivers Conserv. 2014;23:1845–1858. doi: 10.1007/s10531-014-0653-2. PubMed DOI PMC

Karsten U, Lütz C, Holzinger A. 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. 2010;46:1187–1197. doi: 10.1111/j.1529-8817.2010.00921.x. PubMed DOI

Karsten U, Pröschold T, Mikhailyuk T, Holzinger A. Photosynthetic performance of different genotypes of the green alga Klebsormidium sp. (Streptophyta) isolated from biological soil crusts of the Alps. Algol Stud. 2013;142:45–62. doi: 10.1127/1864-1318/2013/0102. DOI

Karsten U, Herburger K, Holzinger A. Dehydration, temperature, and light tolerance in members of the aeroterrestrial green algal genus Interfilum (Streptophyta) from biogeographically different temperate soils. J Phycol. 2014;50:804–816. doi: 10.1111/jpy.12210. PubMed DOI PMC

Karsten U, Herburger K, Holzinger A. 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. 2016;194:2–12. doi: 10.1016/j.jplph.2015.09.002. PubMed DOI PMC

Kitzing C, Pröschold T, Karsten U. 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 Ecol. 2014;67:327–340. doi: 10.1007/s00248-013-0317-x. PubMed DOI

Kotabová E, Kaňa R, Jarešová J, Prášil O. Non-photochemical fluorescence quenching in Chromera velia is enabled by fast violaxanthin de-epoxidation. FEBS Lett. 2011;585:1941–1945. doi: 10.1016/j.febslet.2011.05.015. PubMed DOI

La Rocca N, Sciuto K, Meneghesso A, Moro I, Rascio N, Morosinotto T. Photosynthesis in extreme environments: responses to different light regimes in the Antarctic alga Koliella antarctica. Physiol Plant. 2015;153:654–667. doi: 10.1111/ppl.12273. PubMed DOI

Lachmann SC, Maberly SC, Spijkerman E. Ecophysiology matters: linking inorganic carbon acquisition to ecological preference in four species of microalgae (Chlorophyceae) J Phycol. 2016;52:1051–1063. doi: 10.1111/jpy.12462. PubMed DOI

Lajos K, Mayr S, Buchner O, Blaas K, Holzinger A. A new microscopic method to analyse desiccation-induced volume changes in aeroterrestrial green algae. J Microsc. 2016;263:192–199. doi: 10.1111/jmi.12409. PubMed DOI PMC

Leliaert F, Verbruggen H, Zechman FW. Into the deep: new discoveries at the base of the green plant phylogeny. Bioessays. 2011;33:683–692. doi: 10.1002/bies.201100035. PubMed DOI

Lokhorst GM, Star W. Ultrastructure of mitosis and cytokinesis in Klebsormidium mucosum nov. comb., formerly Ulothrix verrucosa (Chlorophyta) J Phycol. 1985;21:466–476. doi: 10.1111/j.0022-3646.1985.00466.x. DOI

Maberly SC, Spence DHN. Photosynthetic inorganic carbon use by freshwater plants. J Ecol. 1983;71:705–724. doi: 10.2307/2259587. DOI

Maberly SC, Ball LA, Raven JA, Sültemeyer D. Inorganic carbon acquisition by chrysophytes. J Phycol. 2009;45:1052–1061. doi: 10.1111/j.1529-8817.2009.00734.x. PubMed DOI

Meneghesso A, Simionato D, Gerotto C, La Rocca N, Finazzi G, Morosinotto T. Photoacclimation of photosynthesis in the Eustigmatophycean Nannochloropsis gaditana. Photosynth Res. 2016;129:291–305. doi: 10.1007/s11120-016-0297-z. PubMed DOI

Meyer M, Griffiths H. Origins and diversity of eukaryotic CO2-concentrating mechanisms: lessons for the future. J Exp Bot. 2013;64:769–786. doi: 10.1093/jxb/ers390. PubMed DOI

Meyer M, Seibt U, Griffiths H. To concentrate or ventilate? Carbon acquisition, isotope discrimination and physiological ecology of early land plant life forms. Philos Trans R Soc Lond B Biol Sci. 2008;363:2767–2778. doi: 10.1098/rstb.2008.0039. PubMed DOI PMC

Mikhailyuk T, Glaser K, Holzinger A, Karsten U. Biodiversity of Klebsormidium (Streptophyta) from alpine biological soil crusts (Alps, Tyrol, Austria, and Italy) J Phycol. 2015;51:750–767. doi: 10.1111/jpy.12316. PubMed DOI PMC

Millero FJ. The thermodynamics of the carbonate system in seawater. Geochim Cosmochim Acta. 1979;43:1651–1661. doi: 10.1016/0016-7037(79)90184-4. DOI

Miyake C, Horiguchi S, Makino A, Shinzaki Y, Yamamoto H, Tomizawa KI. Effects of light intensity on cyclic electron flow around PSI and its relationship to non-photochemical quenching of Chl fluorescence in tobacco leaves. Plant Cell Physiol. 2005;46:1819–1830. doi: 10.1093/pcp/pci197. PubMed DOI

Moroney JV, Ma Y, Frey WD, Fusilier KA, Pham TT, Simms TA, DiMario RJ, Yang J, Mukherjee B. The carbonic anhydrase isoforms of Chlamydomonas reinhardtii: intracellular location, expression, and physiological roles. Photosynth Res. 2011;109:133–149. doi: 10.1007/s11120-011-9635-3. PubMed DOI

Ng EL, Patti AF, Rose MT, Schefe CR, Wilkinson K, Smernik RJ, Cavagnaro TR. Does the chemical nature of soil carbon drive the structure and functioning of soil microbial communities? Soil Biol Biochem. 2014;70:54–61. doi: 10.1016/j.soilbio.2013.12.004. DOI

Ohad I, Raanan H, Keren N, Tchernov D, Kaplan A. Light-induced changes within photosystem II protects Microcoleus sp. in biological desert sand crusts against excess light. PLoS One. 2010;5:e11000. doi: 10.1371/journal.pone.0011000. PubMed DOI PMC

Ohad I, Berg A, Berkowicz SM, Kaplan A, Keren N. Photoinactivation of photosystem II: is there more than one way to skin a cat? Physiol Plant. 2011;142:79–86. doi: 10.1111/j.1399-3054.2011.01466.x. PubMed DOI

Pichrtová M, Remias D, Lewis LA, Holzinger A. Changes in phenolic compounds and cellular ultrastructure of Arctic and Antarctic strains of Zygnema (Zygnematophyceae, Streptophyta) after exposure to experimentally enhanced UV to PAR ratio. Microbial Ecol. 2013;65:68–83. doi: 10.1007/s00248-012-0096-9. PubMed DOI PMC

Pichrtová M, Kulichová J, Holzinger A. Nitrogen limitation and slow drying induce desiccation tolerance in conjugating green algae (Zygnematophyceae) from polar habitats. PLoS One. 2014;9:e113137. doi: 10.1371/journal.pone.0113137. PubMed DOI PMC

Pichrtová M, Arc E, Stöggl W, Kranner I, Hajek T, Hackl H, Holzinger A. Formation of lipid bodies and changes in fatty acid composition upon pre-akinete formation in arctic and Antarctic Zygnema (Zygnematophyceae, Streptophyta) strains. FEMS Microbiol Ecol. 2016;92:fiw096. doi: 10.1093/femsec/fiw096. PubMed DOI PMC

Pierangelini M, Stojkovic S, Orr PT, Beardall J. Elevated CO2 causes changes in the photosynthetic apparatus of a toxic cyanobacterium, Cylindrospermopsis raciborskii. J Plant Physiol. 2014;171:1091–1098. doi: 10.1016/j.jplph.2014.04.003. PubMed DOI

Porra RJ, Thompson WA, Kriedemann PE. Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. BBA Bioenerg. 1989;975:384–394. doi: 10.1016/S0005-2728(89)80347-0. DOI

Raanan H, Felde VJ, Peth S, Drahorad S, Ionescu D, Eshkol G, Treves H, Felix-Henningsen P, Berkowicz SM, Keren N, Horn R, Hagemann M, Kaplan A. Three-dimensional structure and cyanobacterial activity within a desert biological soil crust. Environ Microbiol. 2016;18:372–383. doi: 10.1111/1462-2920.12859. PubMed DOI

Raanan H, Oren N, Treves H, Berkowicz SM, Hagemann M, Pade N, Keren N, Kaplan A. Simulated soil crust conditions in a chamber system provide new insights on cyanobacterial acclimation to desiccation. Environ Microbiol. 2016;18:414–426. doi: 10.1111/1462-2920.12998. PubMed DOI

Ratti S, Giordano M, Morse D. CO2-concentrating mechanisms of the potentially toxic dinoflagellate Protoceratium reticulatum (Dinophyceae, Gonyaulacales) J Phycol. 2007;43:693–701. doi: 10.1111/j.1529-8817.2007.00368.x. DOI

Raven JA, Colmer TD. Life at the boundary: photosynthesis at the soil-fluid interface. A synthesis focusing on mosses. J Exp Bot. 2016;67:1613–1623. doi: 10.1093/jxb/erw012. PubMed DOI

Raven JA, Giordano M, Beardall J, Maberly SC. Algal evolution in relation to atmospheric CO2: carboxylases, carbon-concentrating mechanisms and carbon oxidation cycles. Philos Trans R Soc B. 2012;367:493–507. doi: 10.1098/rstb.2011.0212. PubMed DOI PMC

Raven JA, Beardall J, Sánchez-Baracaldo P. The possible evolution, and future, of CO2-concentrating mechanisms. J Exp Bot. 2017 PubMed

Reinfelder JR. Carbon concentrating mechanisms in eukaryotic marine phytoplankton. Annu Rev Mar Sci. 2011;3:291–315. doi: 10.1146/annurev-marine-120709-142720. PubMed DOI

Rindi F, Mikhailyuk TI, Sluiman HJ, Friedl T, López-Bautista JM. Phylogenetic relationships in Interfilum and Klebsormidium (Klebsormidiophyceae, Streptophyta) Mol Phylogenet Evol. 2011;58:218–231. doi: 10.1016/j.ympev.2010.11.030. PubMed DOI

Roach T, Krieger-Liszkay A. Regulation of photosynthetic electron transport and photoinhibition. Curr Protein Pept Sci. 2014;15:351–362. doi: 10.2174/1389203715666140327105143. PubMed DOI PMC

Rumeau D, Peltier G, Cournac L. Chlororespiration and cyclic electron flow around PSI during photosynthesis and plant stress response. Plant Cell Environ. 2007;30:1041–1051. doi: 10.1111/j.1365-3040.2007.01675.x. PubMed DOI

Ryšánek D, Hrčková K, Škaloud P. Global ubiquity and local endemism of free-living terrestrial protists: phylogeographic assessment of the streptophyte alga Klebsormidium. Environ Microbiol. 2015;17:689–698. doi: 10.1111/1462-2920.12501. PubMed DOI

Ryšánek D, Holzinger A, Škaloud P. Influence of substrate and pH on diversity of the aeroterrestrial alga Klebsormidium: a potentially important factor for sympatric speciation? Phycologia. 2016;55:347–358. doi: 10.2216/15-110.1. PubMed DOI PMC

Shimakawa G, Matsuda Y, Nakajima K, Tamoi M, Shigeoka S, Miyake C. Diverse strategies of O2 usage for preventing photo-oxidative damage under CO2 limitation during algal photosynthesis. Sci Rep. 2017;7:41022. doi: 10.1038/srep41022. PubMed DOI PMC

Škaloud P, Rindi F. Ecological differentiation of cryptic species within an asexual protist morphospecies: a case study of filamentous green alga Klebsormidium (Streptophyta) J Eukaryot Microbiol. 2013;60:350–362. doi: 10.1111/jeu.12040. PubMed DOI

Smith EC, Griffiths H. The occurrence of the chloroplast pyrenoid is correlated with the activity of a CO2-concentrating mechanism and carbon isotope discrimination in lichens and bryophytes. Planta. 1996;198:6–16. doi: 10.1007/BF00197580. DOI

Spijkerman E, Maberly SC, Coesel PF. Carbon acquisition mechanisms by planktonic desmids and their link to ecological distribution. Can J Bot. 2005;83:850–858. doi: 10.1139/b05-069. DOI

Stirbet A, Riznichenko GY, Rubin AB, Govindjee Modeling chlorophyll a fluorescence transient: relation to photosynthesis. Biochemistry (Moscow) 2014;79:291–323. doi: 10.1134/S0006297914040014. PubMed DOI

Stojkovic S, Beardall J, Matear R. CO2-concentrating mechanisms in three southern hemisphere strains of Emiliania huxleyi. J Phycol. 2013;49:670–679. doi: 10.1111/jpy.12074. PubMed DOI

Strasser RJ, Srivastava A, Tsimilli-Michael M. The fluorescence transient as a tool to characterize and screen photosynthetic samples. In: Yunuf M, Pathre M, Mohanty P, editors. Probing photosynthesis: mechanisms, regulation and adaptation. Boca Raton: CRC Press; 2000. pp. 445–483.

Suseela V, Conant RT, Wallenstein MD, Dukes JS. Effects of soil moisture on the temperature sensitivity of heterotrophic respiration vary seasonally in an old-field climate change experiment. Glob Change Biol. 2012;18:336–348. doi: 10.1111/j.1365-2486.2011.02516.x. DOI

Swofford DL. PAUP*: phylogenetic analysis using parsimony (*and other methods). Version 4. Sunderland: Sinauer Associates; 2002.

Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011;28:2731–2739. doi: 10.1093/molbev/msr121. PubMed DOI PMC

Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving sensitivity of progressive multiple sequence alignment through sequence weighting, position 86 specific gap penalties, and weight matrix choice. Nuc Acid Res. 1994;22:4673–4680. doi: 10.1093/nar/22.22.4673. PubMed DOI PMC

Timme RE, Bachvaroff TR, Delwiche CF. Broad phylogenomic sampling and the sister lineage of land plants. PLoS One. 2012;7:e29696. doi: 10.1371/journal.pone.0029696. PubMed DOI PMC

Tóth SZ, Schansker G, Strasser RJ. A non-invasive assay of the plastoquinone pool redox state based on the OJIP-transient. Photosynth Res. 2007;93:193–203. doi: 10.1007/s11120-007-9179-8. PubMed DOI

Treves H, Raanan H, Finkel OM, Berkowicz SM, Keren N, Shotland Y, Kaplan A. A newly isolated Chlorella sp. from desert sand crusts exhibits a unique resistance to excess light intensity. FEMS Microbiol Ecol. 2013;86:373–380. doi: 10.1111/1574-6941.12162. PubMed DOI

Treves H, Raanan H, Kedem I, Murik O, Keren N, Zer H, Berkowicz SM, Giordano M, Norici A, Shotland Y, Ohad I, Kaplan A. The mechanisms whereby the green alga Chlorella ohadii, isolated from desert soil crust, exhibits unparalleled photodamage resistance. New Phytol. 2016;210:1229–1243. doi: 10.1111/nph.13870. PubMed DOI

Villarreal JC, Renner SS. Hornwort pyrenoids, carbon-concentrating structures, evolved and were lost at least five times during the last 100 million years. Proc Natl Acad Sci. 2012;109:18873–18878. doi: 10.1073/pnas.1213498109. PubMed DOI PMC

Walsby AE. Numerical integration of phytoplankton photosynthesis through time and depth in a water column. New Phytol. 1997;136:189–209. doi: 10.1046/j.1469-8137.1997.00736.x. DOI

Yamakawa H, Fukushima Y, Itoh S, Heber U. Three different mechanisms of energy dissipation of a desiccation-tolerant moss serve one common purpose: to protect reaction centres against photo-oxidation. J Exp Bot. 2012;63:1–11. doi: 10.1093/jxb/ers062. PubMed DOI PMC

Zwickl DJ (2006) Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. Dissertation, University of Texas at Austin

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