Light and Dehydration but Not Temperature Drive Photosynthetic Adaptations of Basal Streptophytes (Hormidiella, Streptosarcina and Streptofilum) Living in Terrestrial Habitats

Pierangelini, Mattia; Glaser, K.; Mikhailyuk, T.; Karsten, U.; Holzinger, A.

doi:10.1007/s00248-018-1225-x

Article (Scientific journals)

Light and Dehydration but Not Temperature Drive Photosynthetic Adaptations of Basal Streptophytes (Hormidiella, Streptosarcina and Streptofilum) Living in Terrestrial Habitats

Pierangelini, Mattia; Glaser, K.; Mikhailyuk, T. et al.

2019 • In Microbial Ecology, 77 (2), p. 380-393

Peer Reviewed verified by ORBi

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https://hdl.handle.net/2268/265925

DOI
10.1007/s00248-018-1225-x

PubMed
29974184

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Keywords :

Acclimation; Desiccation; Green algae; Photoprotection; Streptophyta; Temperature; Adaptation, Physiological; Ecosystem; Photosynthesis; Ultraviolet Rays; Water

Abstract :

[en] Streptophyte algae are the ancestors of land plants, and several classes contain taxa that are adapted to an aero-terrestrial lifestyle. In this study, four basal terrestrial streptophytes from the class Klebsormidiophyceae, including Hormidiella parvula; two species of the newly described genus Streptosarcina (S. costaricana and S. arenaria); and the newly described Streptofilum capillatum were investigated for their responses to radiation, desiccation and temperature stress conditions. All the strains showed low-light adaptation (I k < 70 μmol photons m −2 s −1 ) but differed in photoprotective capacities (such as non-photochemical quenching). Acclimation to enhanced photon fluence rates (160 μmol photons m −2 s −1 ) increased photosynthetic performance in H. parvula and S. costaricana but not in S. arenaria, showing that low-light adaptation is a constitutive trait for S. arenaria. This lower-light adaptation of S. arenaria was coupled with a higher desiccation tolerance, providing further evidence that dehydration is a selective force shaping species occurrence in low light. For protection against ultraviolet radiation, all species synthesised and accumulated different amounts of mycosporine-like amino acids (MAAs). Biochemically, MAAs synthesised by Hormidiella and Streptosarcina were similar to MAAs from closely related Klebsormidium spp. but differed in retention time and spectral characteristics in S. capillatum. Unlike the different radiation and dehydration tolerances, Hormidiella, Streptosarcina and Streptofilum displayed preferences for similar thermal conditions. These species showed a temperature dependence of photosynthesis similar to respiration, contrasting with Klebsormidium spp. and highlighting an interspecific diversity in thermal requirements, which could regulate species distributions under temperature changes. © 2018, The Author(s).

Disciplines :

Biochemistry, biophysics & molecular biology

Author, co-author :

Pierangelini, Mattia ; Université de Liège - ULg

Glaser, K.; Applied Ecology and Phycology, Institute of Biological Sciences, University of Rostock, Albert-Einstein-Strasse 3, Rostock, 18059, Germany

Mikhailyuk, T.; M.G. Kholodny Institute of Botany, National Academy of Sciences of Ukraine, Tereschenkivska Str. 2, Kyiv, 01004, Ukraine

Karsten, U.; Applied Ecology and Phycology, Institute of Biological Sciences, University of Rostock, Albert-Einstein-Strasse 3, Rostock, 18059, Germany

Holzinger, A.; Department of Botany, Functional Plant Biology, University of Innsbruck, Innsbruck, 6020, Austria

Language :

English

Title :

Light and Dehydration but Not Temperature Drive Photosynthetic Adaptations of Basal Streptophytes (Hormidiella, Streptosarcina and Streptofilum) Living in Terrestrial Habitats

Publication date :

2019

Journal title :

Microbial Ecology

ISSN :

0095-3628

eISSN :

1432-184X

Publisher :

Springer, Germany

Volume :

Issue :

Pages :

380-393

Peer reviewed :

Peer Reviewed verified by ORBi

Funders :

AvH - Alexander von Humboldt-Stiftung [DE]
DFG - Deutsche Forschungsgemeinschaft [DE]
FWF - Austrian Science Fund [AT]

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Bibliography

Leliaert F, Verbruggen H, Zechman FW (2011) Into the deep: new discoveries at the base of the green plant phylogeny. Bioessays 33:683–692. 10.1002/bies.201100035
Becker B (2013) Snow ball earth and the split of Streptophyta and Chlorophyta. Trends Plant Sci 18:180–183. 10.1016/j.tplants.2012.09.010
Leliaert F, Smith DR, Moreau H, Herron MD, Verbruggen H, Delwiche CF, De Clerck O (2012) Phylogeny and molecular evolution of the green algae. Crit Rev Plant Sci 31:1–46. 10.1080/07352689.2011.615705
de Vries J, Stanton A, Archibald JM, Gould SB (2016) Streptophyte terrestrialization in light of plastid evolution. Trends Plant Sci 21:467–476. 10.1016/j.tplants.2016.01.021
Lewis LA (2017) Hold the salt: freshwater origin of primary plastids. Proc Natl Acad Sci U S A 114:9759–9760. 10.1073/pnas.1712956114
Sánchez-Baracaldo P, Raven JA, Pisani D, Knoll AH (2017) Early photosynthetic eukaryotes inhabited low-salinity habitats. Proc Natl Acad Sci U S A 114:E7737–E7745. 10.1073/pnas.1620089114
Wodniok S, Brinkmann H, Glöckner G, Heidel AJ, Philippe H, Melkonian M, Becker B (2011) Origin of land plants: do conjugating green algae hold the key? BMC Evol Biol 11:104. 10.1186/1471-2148-11-104
Wickett NJ, Mirarab S, Nguyen N, Warnow T, Carpenter E, Matasci N, Ayyampalayam S, Barker MS, Burleigh JG, Gitzendanner MA, Ruhfel BR, Wafula E, der JP, Graham SW, Mathews S, Melkonian M, Soltis DE, Soltis PS, Miles NW, Rothfels CJ, Pokorny L, Shaw AJ, DeGironimo L, Stevenson DW, Surek B, Villarreal JC, Roure B, Philippe H, dePamphilis CW, Chen T, Deyholos MK, Baucom RS, Kutchan TM, Augustin MM, Wang J, Zhang Y, Tian Z, Yan Z, Wu X, Sun X, Wong GKS, Leebens-Mack J (2014) Phylotranscriptomic analysis of the origin and early diversification of land plants. Proc Natl Acad Sci U S A 111:E4859–E4868. 10.1073/pnas.1323926111
Mikhailyuk T, Lukešová A, Glaser K, Holzinger A, Obwegeser S, Nyporko S, Friedl T, Karsten U (2018) New taxa of streptophyte algae (Streptophyta) from terrestrial habitats revealed using an integrative approach. Protist 169:406–431. 10.1016/j.protis.2018.03.002
Becker B, Marin B (2009) Streptophyte algae and the origin of embryophytes. Ann Bot 103:999–1004. 10.1093/aob/mcp044
Delwiche CF, Cooper ED (2015) The evolutionary origin of a terrestrial flora. Curr Biol 25:R899–R910. 10.1016/j.cub.2015.08.029
de Vries J, Archibald JM (2018) Plant evolution: landmarks on the path to terrestrial life. New Phytol 217:1428–1434. 10.1111/nph.14975
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. 10.1007/s00248-011-9924-6
Donner A, Glaser K, Borchhardt N, Karsten U (2017) Ecophysiological response on dehydration and temperature in terrestrial Klebsormidium (Streptophyta) isolated from biological soil crusts in central European grasslands and forests. Microb Ecol 73:850–864. 10.1007/s00248-016-0917-3
Donner A, Ryšánek D, Mikhailyuk T, Karsten U (2017) 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. 10.1007/s10811-017-1158-7
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. 10.1016/j.jplph.2015.09.002
Edwards D, Cherns L, Raven JA (2015) Could land-based early photosynthesizing ecosystems have bioengineered the planet in mid-Palaeozoic times? Palaeontology 58:803–837. 10.1111/pala.12187
Maberly SC (2014) The fitness of the environments of air and water for photosynthesis, growth, reproduction and dispersal of photoautotrophs: an evolutionary and biogeochemical perspective. Aquat Bot 118:4–13. 10.1016/j.aquabot.2014.06.014
Holzinger A, Pichrtová M (2016) Abiotic stress tolerance of charophyte green algae: new challenges for omics techniques. Front Plant Sci 7:678. 10.3389/fpls.2016.00678
de Vries J, Curtis BA, Gould SB, Archibald JM (2018) Embryophyte stress signaling evolved in the algal progenitors of land plants. Proc Natl Acad Sci U S A 201719230:E3471–E3480. 10.1073/pnas.1719230115
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. 10.1111/j.1529-8817.2010.00921.x
Pierangelini M, Ryšánek D, Lang I, Adlassnig W, Holzinger A (2017) Terrestrial adaptation of green algae Klebsormidium and Zygnema (Charophyta) involves diversity in photosynthetic traits but not in CO 2 acquisition. Planta 246:971–986. 10.1007/s00425-017-2741-5
Gerotto C, Morosinotto T (2013) Evolution of photoprotection mechanisms upon land colonization: evidence of PSBS-dependent NPQ in late Streptophyte algae. Physiol Plant 149:583–598. 10.1111/ppl.12070
Lunch CK, LaFountain AM, Thomas S, Frank HA, Lewis LA, Cardon ZG (2013) The xanthophyll cycle and NPQ in diverse desert and aquatic green algae. Photosynth Res 115:139–151. 10.1007/s11120-013-9846-x
Jahns P, Holzwarth AR (2012) The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. BBA-Bioenergetics 1817:182–193. 10.1016/j.bbabio.2011.04.012
Ruban AV (2016) Nonphotochemical chlorophyll fluorescence quenching: mechanism and effectiveness in protecting plants from photodamage. Plant Physiol 170:1903–1916. 10.1104/pp.15.01935
Derks A, Schaven K, Bruce D (2015) Diverse mechanisms for photoprotection in photosynthesis. Dynamic regulation of photosystem II excitation in response to rapid environmental change. BBA-Bioenergetics 1847:468–485. 10.1016/j.bbabio.2015.02.008
Goss R, Lepetit B (2015) Biodiversity of NPQ. J Plant Physiol 172:13–32. 10.1016/j.jplph.2014.03.004
Christa G, Cruz S, Jahns P, de Vries J, Cartaxana P, Esteves AC, Serôdio J, Gould SB (2017) Photoprotection in a monophyletic branch of chlorophyte algae is independent of energy-dependent quenching (qE). New Phytol 214:1132–1144. 10.1111/nph.14435
Giovagnetti V, Han G, Ware MA, Ungerer P, Qin X, Wang WD, Kuang T, Shen J-R, Ruban AV (2018) A siphonous morphology affects light-harvesting modulation in the intertidal green macroalga Bryopsis corticulans (Ulvophyceae). Planta 247:1293–1306. 10.1007/s00425-018-2854-5
Bonente G, Ballottari M, Truong TB, Morosinotto T, Ahn TK, Fleming GR, Niyogi KK, Bassi R (2011) Analysis of LhcSR3, a protein essential for feedback de-excitation in the green alga Chlamydomonas reinhardtii. PLoS Biol 9:e1000577. 10.1371/journal.pbio.1000577
Correa-Galvis V, Redekop P, Guan K, Griess A, Truong TB, Wakao S, Niyogi KK, Jahns P (2016) Photosystem II subunit PsbS is involved in the induction of LHCSR protein-dependent energy dissipation in Chlamydomonas reinhardtii. J Biol Chem 291:17478–17487. 10.1074/jbc.M116.737312
Tibiletti T, Auroy P, Peltier G, Caffarri S (2016) Chlamydomonas reinhardtii PsbS protein is functional and accumulates rapidly and transiently under high light. Plant Physiol 171:2717–2730. 10.1104/pp.16.00572
Vincent WF, Neale PJ (2000) Mechanisms of UV damage to aquatic organisms. In: de Mora S, Demers S, Vermet M (eds) The effects of UV radiation in the marine environment. Cambridge University Press, Cambridge, pp 149–176
Karsten U (2008) Defense strategies of algae and cyanobacteria against solar ultraviolet radiation. In: Amsler CD (ed) Algal chemical ecology. Springer, Berlin, pp 273–296
Beardall J, Stojkovic S, Larsen S (2009) Living in a high CO 2 world: impacts of global climate change on marine phytoplankton. Plant Ecol Divers 2:191–205. 10.1080/17550870903271363
Sharma S, Chatterjee S, Kataria S, Joshi J, Datta S, Vairale MG, Veer V (2017) A review on responses of plants to UV-B radiation related stress. In: Singh VP, Singh S, Prasad SM, Parihar P (eds) UV-B radiation: from environmental stressor to regulator of plant growth. Wiley, Hoboken, pp 75–97
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. Microb Ecol 67:327–340. 10.1007/s00248-013-0317-x
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. 10.1111/jpy.12619
Shang JL, Zhang ZC, Yin XY, Chen M, Hao FH, Wang K, Feng JL, Xu HF, Yin YC, Tang HR, Qiu BS (2018) UV-B induced biosynthesis of a novel sunscreen compound in solar radiation and desiccation tolerant cyanobacteria. Environ Microbiol 20:200–213. 10.1111/1462-2920.13972
Bandaranayake WM (1998) Mycosporines: are they nature’s sunscreens? Nat Prod Rep 15:159–172. 10.1039/A815159Y
Ohad I, Raanan H, Keren N, Tchernov D, Kaplan A (2010) Light induced changes within photosystem II protects Microcoleus sp. in biological desert sand crusts against excess light. PLoS One 5:e11000. 10.1371/journal.pone.0011000
Raanan H, Oren N, Treves H, Keren N, Ohad I, Berkowicz SM, Hagemann M, Koch M, Shotland Y, Kaplan A (2016) Towards clarifying what distinguishes cyanobacteria able to resurrect after desiccation from those that cannot: the photosynthetic aspect. BBA-Bioenergetics 1857:715–722. 10.1016/j.bbabio.2016.02.007
Holzinger A, Kaplan F, Blaas K, Zechmann B, Komsic-Buchmann K, Becker B (2014) Transcriptomics of desiccation tolerance in the streptophyte green alga Klebsormidium reveal a land plant-like defense reaction. PLoS One 9:e110630. 10.1371/journal.pone.0110630
Holzinger A, Herburger K, Blaas K, Lewis LA, Karsten U (2017) The terrestrial green macroalga Prasiola calophylla (Trebouxiophyceae, Chlorophyta): ecophysiological performance under water-limiting conditions. Protoplasma 254:1755–1767. 10.1007/s00709-016-1068-6
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. 10.1111/j.1365-3040.2007.01704.x
Raanan H, Oren N, Treves H, Berkowicz SM, Hagemann M, Pade N, Keren N, Kaplan A (2016) Simulated soil crust conditions in a chamber system provide new insights on cyanobacterial acclimation to desiccation. Environ Microbiol 18:414–426. 10.1111/1462-2920.12998
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. 10.1111/jpy.12210
Herburger K, Karsten U, Holzinger A (2016) Entransia and Hormidiella, sister lineages of Klebsormidium (Streptophyta), respond differently to light, temperature, and desiccation stress. Protoplasma 253:1309–1323. 10.1007/s00709-015-0889-z
Herburger K, Lewis LA, Holzinger A (2015) Photosynthetic efficiency, desiccation tolerance and ultrastructure in two phylogenetically distinct strains of alpine Zygnema sp. (Zygnematophyceae, Streptophyta): role of pre-akinete formation. Protoplasma 252:571–589. 10.1007/s00709-014-0703-3
Padfield D, Yvon-Durocher G, Buckling A, Jennings S, Yvon-Durocher G (2016) Rapid evolution of metabolic traits explains thermal adaptation in phytoplankton. Ecol Lett 9:133–142. 10.1111/ele.12545
Aigner S, Holzinger A, Karsten U, Kranner I (2017) The freshwater red alga Batrachospermum turfosum (Florideophyceae) can acclimate to a wide range of light and temperature conditions. Eur J Phycol 52:238–249. 10.1080/09670262.2016.1274430
Padfield D, Lowe C, Buckling A, French-Constant R, Jennings S, Shelley F, Ólafsson JS, Yvon-Durocher G (2017) Metabolic compensation constrains the temperature dependence of gross primary production. Ecol Lett 20:1250–1260. 10.1111/ele.12820
Schaum CE, Buckling A, Smirnoff N, Studholme DJ, Yvon-Durocher G (2018) Environmental fluctuations accelerate molecular evolution of thermal tolerance in a marine diatom. Nat Commun 9:1719. 10.1038/s41467-018-03906-5
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. 10.1111/j.0022-3646.1993.00001.x
Ihnken S, Eggert A, Beardall J (2010) Exposure times in rapid light curves affect photosynthetic parameters in algae. Aquat Bot 93:185–194. 10.1016/j.aquabot.2010.07.002
Roach T, Na CS (2017) LHCSR3 affects de-coupling and re-coupling of LHCII to PSII during state transitions in Chlamydomonas reinhardtii. Sci Rep 7:43145. 10.1038/srep43145
Karsten U, Escoubeyrou K, Charles F (2009) The effect of redissolution solvents and HPLC columns on the analysis of mycosporine-like amino acids (MAAs) in the macroalgal species Prasiola crispa and Porphyra umbilicalis. Helgol Mar Res 63:231–238. 10.1007/s10152-009-0152-0
Raven JA, Beardall J (2016) Dark respiration and organic carbon loss. In: Borowitzka M, Beardall J, Raven JA (eds) The physiology of microalgae. Developments in applied phycology. Springer, Cham, pp 129–140. 10.1007/978-3-319-24945-2_6
Karsten U, Herburger K, Holzinger A (2017) Photosynthetic plasticity in the green algal species Klebsormidium flaccidum (Streptophyta) from a terrestrial and a freshwater habitat. Phycologia 56:213–220. 10.2216/16-85.1
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 (2016) Three-dimensional structure and cyanobacterial activity within a desert biological soil crust. Environ Microbiol 18:372–383. 10.1111/1462-2920.12859
Richardson K, Beardall J, Raven JA (1983) Adaptation of unicellular algae to irradiance: an analysis of strategies. New Phytol 93:157–191. 10.1111/j.1469-8137.1983.tb03422.x
Giordano M (2013) Homeostasis: an underestimated focal point of ecology and evolution. Plant Sci 211:92–101. 10.1016/j.plantsci.2013.07.008
Pierangelini M, Stojkovic S, Orr PT, Beardall J (2015) Photo-acclimation to low light–changes from growth to antenna size in the cyanobacterium Cylindrospermopsis raciborskii. Harmful Algae 46:11–17. 10.1016/j.hal.2015.04.004
MacIntyre HL, Kana TM, Anning T, Geider RJ (2002) Photoacclimation of photosynthesis irradiance response curves and photosynthetic pigments in microalgae and cyanobacteria. J Phycol 38:17–38. 10.1046/j.1529-8817.2002.00094.x
McKew BA, Lefebvre SC, Achterberg EP, Metodieva G, Raines CA, Metodiev MV, Geider RJ (2013) Plasticity in the proteome of Emiliania huxleyi CCMP 1516 to extremes of light is highly targeted. New Phytol 200:61–73. 10.1111/nph.12352
McKew BA, Davey P, Finch SJ, Hopkins J, Lefebvre SC, Metodiev MV, Oxborough K, Raines CA, Lawson T, Geider RJ (2013) The trade-off between the light-harvesting and photoprotective functions of fucoxanthin-chlorophyll proteins dominates light acclimation in Emiliania huxleyi (clone CCMP 1516). New Phytol 200:74–85. 10.1111/nph.12373
Meneghesso A, Simionato D, Gerotto C, La Rocca N, Finazzi G, Morosinotto T (2016) Photoacclimation of photosynthesis in the Eustigmatophycean Nannochloropsis gaditana. Photosynth Res 129:291–305. 10.1007/s11120-016-0297-z
Quaas T, Berteotti S, Ballottari M, Flieger K, Bassi R, Wilhelm C, Goss R (2015) Non-photochemical quenching and xanthophyll cycle activities in six green algal species suggest mechanistic differences in the process of excess energy dissipation. J Plant Physiol 172:92–103. 10.1016/j.jplph.2014.07.023
La Rocca N, Sciuto K, Meneghesso A, Moro I, Rascio N, Morosinotto T (2015) Photosynthesis in extreme environments: responses to different light regimes in the Antarctic alga Koliella antarctica. Physiol Plant 153:654–667. 10.1111/ppl.12273
Gerotto C, Alboresi A, Giacometti GM, Bassi R, Morosinotto T (2011) Role of PSBS and LHCSR in Physcomitrella patens acclimation to high light and low temperature. Plant Cell Environ 34:922–932. 10.1111/j.1365-3040.2011.02294.x
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, Oshima-Yamada 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. Nat Commun 5:3978. 10.1038/ncomms4978
Garibay-Hernández A, Barkla BJ, Vera-Estrella R, Martinez A, Pantoja O (2017) Membrane proteomic insights into the physiology and taxonomy of a green microalga. Plant Physiol 173:390–416. 10.1104/pp.16.01240
Allorent G, Tokutsu R, Roach T, Peers G, Cardol P, Girard-Bascou J, Seigneurin-Berny D, Petroutsos D, Kuntz M, Breyton C, Franck F, Wollman FA, Niyogi KK, Krieger-Liszkay A, Minagawa J, Finazzi G (2013) A dual strategy to cope with high light in Chlamydomonas reinhardtii. Plant Cell 25:545–557. 10.1105/tpc.112.108274
Gao Q, Garcia-Pichel F (2011) Microbial ultraviolet sunscreens. Nat Rev Microbiol 9:791–802. 10.1038/nrmicro2649
La Barre S, Roullier C, Boustie J (2014) Mycosporine-like amino acids (MAAs) in biological photosystems. In: La Barre S, Kornprobst JM (eds) Outstanding marine molecules: chemistry, biology, analysis. Wiley-Blackwell, Weinheim, pp 333–360. 10.1002/9783527681501.ch15
Kitzing C, Karsten U (2015) Effects of UV radiation on optimum quantum yield and sunscreen contents in members of the genera Interfilum, Klebsormidium, Hormidiella and Entransia (Klebsormidiophyceae, Streptophyta). Eur J Phycol 50:279–287. 10.1080/09670262.2015.1031190
Tamaru Y, Takani Y, Yoshida T, Sakamoto T (2005) Crucial role of extracellular polysaccharides in desiccation and freezing tolerance in the terrestrial cyanobacterium Nostoc commune. Appl Environ Microbiol 71:7327–7333. 10.1128/AEM.71.11.7327-7333.2005
Graham LE, Arancibia-Avila P, Taylor WA, Strother PK, Cook ME (2012) Aeroterrestrial Coleochaete (Streptophyta, Coleochaetales) models early plant adaptation to land. Am J Bot 99:130–144. 10.3732/ajb.1100245
Berry J, Bjorkman O (1980) Photosynthetic response and adaptation to temperature in higher plants. Annu Rev Plant Physiol 31:491–543
Collier CJ, Ow YX, Langlois L, Uthicke S, Johanssonc CL, O'Brien KR, Hrebien V, Adams MP (2017) Optimum temperatures for net primary productivity of three tropical seagrass species. Front Plant Sci 8:1446. 10.3389/fpls.2017.01446
Salvucci ME, Osteryoung KW, Crafts-Brandner SJ, Vierling E (2001) Exceptional sensitivity of rubisco activase to thermal denaturation in vitro and in vivo. Plant Physiol 127:1053–1064. 10.1104/pp.010357
Atkin OK, Tjoelker MG (2003) Thermal acclimation and the dynamic response of plant respiration to temperature. Trends Plant Sci 8:343–351. 10.1016/S1360-1385(03)00136-5
Allakhverdiev SI, Kreslavski VD, Klimov VV, Los DA, Carpentier R, Mohanty P (2008) Heat stress: an overview of molecular responses in photosynthesis. Photosynth Res 98:541–550. 10.1007/s11120-008-9331-0
Kruse J, Rennenberg H, Adams MA (2011) Steps towards a mechanistic understanding of respiratory temperature responses. New Phytol 189:659–677. 10.1111/j.1469-8137.2010.03576.x
Sukenik A, Bennett J, Falkowski P (1987) Light-saturated photosynthesis−limitation by electron transport or carbon fixation? BBA-Bioenergetics 891:205–215. 10.1016/0005-2728(87)90216-7
Raven JA, Geider RJ (1988) Temperature and algal growth. New Phytol 110:441–461. 10.1111/j.1469-8137.1988.tb00282.x
Schaum CE, Barton S, Bestion E, Buckling A, Garcia-Carreras B, Lopez P, Lowe C, Pawar S, Smirnoff N, Trimmer M, Yvon-Durocher G (2017) Adaptation of phytoplankton to a decade of experimental warming linked to increased photosynthesis. Nat Ecol Evol 1:0094. 10.1038/s41559-017-0094
López-Urrutia Á, San Martin E, Harris RP, Irigoien X (2006) Scaling the metabolic balance of the oceans. Proc Natl Acad Sci U S A 103:8739–8744. 10.1073/pnas.0601137103
Yvon-Durocher G, Caffrey JM, Cescatti A, Dossena M, del Giorgio P, Gasol JM, Montoya JM, Pumpanen J, Staehr PA, Trimmer M, Woodward G (2012) Reconciling the temperature dependence of respiration across timescales and ecosystem types. Nature 487:472–476. 10.1038/nature11205
Fernandes V, de Lima M, Maria N, Roush D, Rudgers J, Collins SL, Garcia-Pichel F (2018) Exposure to predicted precipitation patterns decreases population size and alters community structure of cyanobacteria in biological soil crusts from the Chihuahuan Desert. Environ Microbiol 20:259–269. 10.1111/1462-2920.13983
Borchhardt N, Baum C, Mikhailyuk T, Karsten U (2017) Biological soil crusts of arctic Svalbard—water availability as potential controlling factor for microalgal biodiversity. Front Microbiol 8:1485. 10.3389/fmicb.2017.01485