Mallomonas thrive primarily in freshwaters and dominate plankton communities, especially in oligotrophic waters. The cells have a siliceous cell covering of regularly arranged scales. Despite their ecological importance, the intricate structure and evolutionary significance of their silica scales are still unexplored. We investigated the nanopatterns on the scales and hypothesized that they may play a role in UV shielding. UVA and UVB exposure experiments were performed with 20 Mallomonas species, categorized into four groups based on the nanopattern of the scales (plain-scaled, meshed, striated, and papilliferous group); a fifth group consisted of the species that have extremely thick, robust scales regardless of the nanopattern. We revealed that thick scales were associated with enhanced UVB resistance, suggesting a protective role. No significant differences in UVA response were observed among the groups, except for the meshed group, which showed lower resistance, likely due to the less regular pattern on the shield. In conclusion, the scale case, composed of sufficiently silicified scales, provides effective UV protection in freshwater environments, regardless of the particular nanopattern. In increased UVB radiation, the thickness of the scales plays role. Contrary to expectations, cell size and phylogeny do not strongly predict UV resistance. The study highlights the diverse UV responses of Mallomonas, but further studies are needed to understand the role of scales/nanopatterns in the ecological adaptations of the species.

Department of Botany Faculty of Science Charles University Prague Czech Republic

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Aguirre, L. E., Ouyang, L., Elfwing, A., Hedblom, M., Wulff, A., & Inganäs, O. (2018). Diatom frustules protect DNA from ultraviolet light. Scientific Reports, 8(1), 5138. https://doi.org/10.1038/s41598‐018‐21810‐2

Ahlmann‐Eltze, C., & Patil, I. (2021). Ggsignif: R package for displaying significance brackets for 'ggplot2.' PsyArxiv. https://doi.org/10.31234/osf.io/7awm6

Blomberg, S. P., Garland, T., & Ives, A. R. (2003). Testing for phylogenetic signal in comparative data: Behavioral traits are more labile. Evolution, 57, 717–745. https://doi.org/10.1111/j.0014‐3820.2003.tb00285.x

Boenigk, J., Pfandl, K., & Hansen, P. (2006). Exploring strategies for nanoflagellates living in a wet desert. Aquatic Microbial Ecology, 44, 71–83. https://doi.org/10.3354/ame044071

Bühlmann, B., Bossard, P., & Uehlinger, U. (1987). The influence of longwave ultraviolet radiation (u.v.‐A) on the photosynthetic aktivity (14C‐assimilation) of phytoplankton. Journal of Plankton Research, 9, 935–943. https://doi.org/10.1093/plankt/9.5.935

Cadet, J., Douki, T., Ravanat, J.‐L., & Di Mascio, P. (2009). Sensitized formation of oxidatively generated damage to cellular DNA by UVA radiation. Photochemical & Photobiological Sciences, 8, 903–911. https://doi.org/10.1039/b905343n

Čertnerová, D., Čertner, M., & Škaloud, P. (2019). Molecular phylogeny and evolution of phenotype in silica‐scaled chrysophyte genus Mallomonas. Journal of Phycology, 55(4), 912–923. https://doi.org/10.1111/jpy.12882

De Stefano, L., Rea, I., Rendina, I., De Stefano, M., & Moretti, L. (2007). Lensless light focusing with the centric marine diatom Coscinodiscus walesii. Optics Express, 15, 18082. https://doi.org/10.1364/OE.15.018082

De Tommasi, E. (2016). Light manipulation by single cells: The case of diatoms. Journal of Spectroscopy, 2016, 1–13. https://doi.org/10.1155/2016/2490128

De Tommasi, E., Congestri, R., Dardano, P., De Luca, A. C., Managò, S., Rea, I., & De Stefano, M. (2018). UV‐shielding and wavelength conversion by centric diatom nanopatterned frustules. Scientific Reports, 8, 16285. https://doi.org/10.1038/s41598‐018‐34651‐w

De Tommasi, E., Rea, I., Ferrara, M. A., De Stefano, L., De Stefano, M., Al‐Handal, A. Y., Stamenković, M., & Wulff, A. (2021). Underwater light manipulation by the benthic diatom Ctenophora pulchella: From PAR efficient collection to UVR screening. Nanomaterials, 11, 2855. https://doi.org/10.3390/nano11112855

De Tommasi, E., Rea, I., Mocella, V., Moretti, L., De Stefano, M., Rendina, I., & De Stefano, L. (2010). Multi‐wavelength study of light transmitted through a single marine centric diatom. Optics Express, 18, 12203. https://doi.org/10.1364/OE.18.012203

Diffey, B. L. (1991). Solar ultraviolet radiation effects on biological systems. Physics in Medicine and Biology, 36, 299–328. https://doi.org/10.1088/0031‐9155/36/3/001

Ellegaard, M., Lenau, T., Lundholm, N., Maibohm, C., Friis, S. M. M., Rottwitt, K., & Su, Y. (2016). The fascinating diatom frustule—Can it play a role for attenuation of UV radiation? Journal of Applied Phycology, 28, 3295–3306. https://doi.org/10.1007/s10811‐016‐0893‐5

Ferrara, M. A., Dardano, P., De Stefano, L., Rea, I., Coppola, G., Rendina, I., Congestri, R., Antonucci, A., De Stefano, M., & De Tommasi, E. (2014). Optical properties of diatom nanostructured biosilica in Arachnoidiscus sp: Micro‐optics from mother nature. PLoS ONE, 9, e103750. https://doi.org/10.1371/journal.pone.0103750

Fuhrmann, T., Landwehr, S., El Rharbi‐Kucki, M., & Sumper, M. (2004). Diatoms as living photonic crystals. Applied Physics B, 78(3–4), 257–260. https://doi.org/10.1007/s00340‐004‐1419‐4

Garcia‐Pichel, F. (1994). A model for internal self‐shading in planktonic organisms and its implications for the usefulness of ultraviolet sunscreens. Limnology and Oceanography, 39, 1704–1717. https://doi.org/10.4319/lo.1994.39.7.1704

Glassmeier, K.‐H., & Vogt, J. (2010). Magnetic polarity transitions and biospheric effects. In G. Hulot, A. Balogh, U. R. Christensen, C. Constable, M. Mandea, & N. Olsen (Eds.), Terrestrial magnetism (Vol. 36, pp. 387–410). Springer. https://doi.org/10.1007/978‐1‐4419‐7955‐1_14

Häder, D.‐P. (1997). Effects of UV radiation on phytoplankton. In J. G. Jones (Ed.), Advances in microbial ecology (Vol. 15, pp. 1–26). Springer. https://doi.org/10.1007/978‐1‐4757‐9074‐0_1

Häder, D.‐P., Williamson, C. E., Wängberg, S.‐Å., Rautio, M., Rose, K. C., Gao, K., Helbling, E. W., Sinha, R. P., & Worrest, R. (2015). Effects of UV radiation on aquatic ecosystems and interactions with other environmental factors. Photochemical & Photobiological Sciences, 14, 108–126. https://doi.org/10.1039/c4pp90035a

Hale, M., & Mitchell, J. (2001). Functional morphology of diatom frustule microstructures: Hydrodynamic control of Brownian particle diffusion and advection. Aquatic Microbial Ecology, 24, 287–295. https://doi.org/10.3354/ame024287

Hamm, C. E., Merkel, R., Springer, O., Jurkojc, P., Maier, C., Prechtel, K., & Smetacek, V. (2003). Architecture and material properties of diatom shells provide effective mechanical protection. Nature, 42, 841–843. https://doi.org/10.1038/nature01416

Hazzard, C., Lesser, M. P., & Kinzie, R. A. (1997). Effects of ultraviolet radiation on photosynthesis in the subtropical marine diatom, Chaetoceros gracilis (Bacillariophyceae). Journal of Phycology, 33, 960–968. https://doi.org/10.1111/j.0022‐3646.1997.00960.x

Hessen, D. O., & Van Donk, E. (1994). Effects of UV‐radiation of humic water on primary and secondary production. Water, Air, and Soil Pollution, 75, 325–338. https://doi.org/10.1007/BF00482944

Hörning, M., Schertel, A., Schneider, R., Lemloh, M.‐L., Schweikert, M. R., & Weiss, I. M. (2020). Mineralized scale patterns on the cell periphery of the chrysophyte Mallomonas determined by comparative 3D Cryo‐FIB SEM data processing. Journal of Structural Biology, 209, 107403. https://doi.org/10.1016/j.jsb.2019.10.005

Jo, B. Y., Shin, W., Kim, H. S., Siver, P. A., & Andersen, R. A. (2013). Phylogeny of the genus Mallomonas (Synurophyceae) and descriptions of five new species on the basis of morphological evidence. Phycologia, 52, 266–278. https://doi.org/10.2216/12‐107.1

Jokiel, P. L., & York, R. H. (1984). Importance of ultraviolet radiation in photoinhibition of microalgal growth. Limnology and Oceanography, 29, 192–198. https://doi.org/10.4319/lo.1984.29.1.0192

Karentz, D., Cleaver, J. E., & Mitchell, D. L. (1991). Cell survival characteristics and molecular responses of antarctic phytoplankton to ultraviolet‐b radiation. Journal of Phycology, 27, 326–341. https://doi.org/10.1111/j.0022‐3646.1991.00326.x

Katoh, K., & Standley, D. M. (2013). Mafft multiple sequence alignment software version 7: Improvements in performance and usability. Molecular Biology and Evolution, 30, 772–780. https://doi.org/10.1093/molbev/mst010

Kiefer, J. (1990). Biological radiation effects. Springer. https://doi.org/10.1007/978‐3‐642‐83769‐2

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). European Journal of Phycology, 50, 279–287. https://doi.org/10.1080/09670262.2015.1031190

Knotek, P., & Škaloud, P. (2023). The effect of patterned structures on the mechanical resistance of microscopic silica scales. Fottea, 23, 190–200. https://doi.org/10.5507/fot.2023.007

Kristiansen, J. (2002). The genus Mallomonas (Synurophyceae): A taxonomic survey based on the ultrastructure of silica scales and bristles. Opera Botanica, 139, 1–218.

Laurion, I., & Vincent, W. F. (1998). Cell size versus taxonomic composition as determinants of UV‐sensitivity in natural phytoplankton communities. Limnology and Oceanography, 43, 1774–1779. https://doi.org/10.4319/lo.1998.43.8.1774

Lavau, S., Saunders, G. W., & Wetherbee, R. (1997). A phylogenetic analysis of the Synurophyceae using molecular data and scale case morphology. Journal of Phycology, 33, 135–151. https://doi.org/10.1111/j.0022‐3646.1997.00135.x

Lavau, S., & Wetherbee, R. (1994). Structure and development of the scale case of Mallomonas adamas (Synurophyceae). Protoplasma, 181(1–4), 259–268. https://doi.org/10.1007/BF01666400

Lengyel, E., Barreto, S., Padisák, J., Stenger‐Kovács, C., Lázár, D., & Buczkó, K. (2023). Contribution of silica‐scaled chrysophytes to ecosystems services: A review. Hydrobiologia, 850, 2735–2756. https://doi.org/10.1007/s10750‐022‐05075‐5

Li, H., & Durbin, R. (2009). Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics, 25, 1754–1760. https://doi.org/10.1093/bioinformatics/btp324

Likhoshway, Y. V., Masyukova, Y. A., Sherbakova, T. A., Petrova, D. P., & Grachev, M. A. (2006). Detection of the gene responsible for silicic acid transport in chrysophycean algae. Doklady Biological Sciences, 408, 256–260. https://doi.org/10.1134/S001249660603015X

Lyons, T. W., Reinhard, C. T., & Planavsky, N. J. (2014). The rise of oxygen in Earth's early ocean and atmosphere. Nature, 506, 307–315. https://doi.org/10.1038/nature13068

Marron, A. O., Ratcliffe, S., Wheeler, G. L., Goldstein, R. E., King, N., Not, F., De Vargas, C., & Richter, D. J. (2016). The evolution of silicon transport in eukaryotes. Molecular Biology and Evolution, 33, 3226–3248. https://doi.org/10.1093/molbev/msw209

Miklasz, K. A., & Denny, M. W. (2010). Diatom sinkings speeds: Improved predictions and insight from a modified Stokes' law. Limnology and Oceanography, 55, 2513–2525. https://doi.org/10.4319/lo.2010.55.6.2513

Milligan, A. J., & Morel, F. M. M. (2002). A proton buffering role for silica in diatoms. Science, 297, 1848–1850. https://doi.org/10.1126/science.1074958

Milot‐Roy, V., & Vincent, W. F. (1994). UV radiation effects on photosynthesis: the importance of near‐surface thermoclines in a subarctic lake. Archiv für Hydrobiologie, 43, 171–184.

Münkemüller, T., Lavergne, S., Bzeznik, B., Dray, S., Jombart, T., Schiffers, K., & Thuiller, W. (2012). How to measure and test phylogenetic signal. Methods in Ecology and Evolution, 3, 743–756. https://doi.org/10.1111/j.2041‐210X.2012.00196.x

Nemcova, Y., Neustupa, J., Kvíderová, J., & Řezáčová‐Škaloudová, M. (2010). Morphological plasticity of silica scales of Synura echinulata (Synurophyceae) in crossed gradients of light and temperature – A geometric morphometric approach. Nova Hedwigia. Beihefte, 136, 21–32. https://doi.org/10.1127/1438‐9134/2010/0136‐0021

Nemcova, Y., & Pichrtová, M. (2012). Shape dynamics of silica scales (Chrysophyceae, Stramenopiles) associated with pH. Fottea, 12, 281–291. https://doi.org/10.5507/fot.2012.020

Neustupa, J., Řezáčová‐Škaloudová, M., & Nemcova, Y. (2010). Shape variation of the silica‐scales of Mallomonas kalinae (Mallomonadales, Synurophyceae) in relation to their position on the cell body. Nova Hedwigia. Beihefte, 136, 33–41. https://doi.org/10.1127/1438‐9134/2010/0136‐0033

Petrucciani, A., Chaerle, P., & Norici, A. (2022). Diatoms versus copepods: Could frustule traits have a role in avoiding predation? Frontiers in Marine Science, 8, 804960. https://doi.org/10.3389/fmars.2021.804960

Pichrtová, M., & Nemcova, Y. (2011). Effect of temperature on size and shape of silica scales in Synura petersenii and Mallomonas tonsurata (Stramenopiles). Hydrobiologia, 673, 1–11. https://doi.org/10.1007/s10750‐011‐0743‐z

R Core Team. (2021). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing.

Reid, G. C., Isaksen, I. S. A., Holzer, T. E., & Crutzen, P. J. (1976). Influence of ancient solar‐proton events on the evolution of life. Nature, 259, 177–179. https://doi.org/10.1038/259177a0

Revell, L. J. (2012). Phytools: An R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution, 3(2), 217–223. https://doi.org/10.1111/j.2041‐210X.2011.00169.x

Ronquist, F., Teslenko, M., Van Der Mark, P., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M. A., & Huelsenbeck, J. P. (2012). Mrbayes 3.2: Efficient bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 539–542. https://doi.org/10.1093/sysbio/sys029

Salonen, K., Järvinen, M., Aalto, T., Likolammi, M., Lindblom, V., Münster, U., & Sarvala, J. (2024). Dynamic adaptation of phytoplankton vertical migration to changing grazing and nutrient conditions. Hydrobiologia, 851, 3639–3663. https://doi.org/10.1007/s10750‐024‐05526‐1

Sandgren, C. D., Hall, S. A., & Barlow, S. B. (1996). Siliceous scale production in chrysophyte and synurophyte algae. I. Effects of silica‐limited growth on cell silica content, scale morphology, and the construction of the scale layer of Synura petersenii. Journal of Phycology, 32, 675–692. https://doi.org/10.1111/j.0022‐3646.1996.00675.x

Sandgren, C. D., & Walton, W. E. (1995). The influence of zooplankton herbivory on the biogeography of chrysophyte algae. In C. D. Sandgren, J. P. Smol, & J. Kristiansen (Eds.), Chrysophyte algae (1st ed., pp. 269–302). Cambridge University Press. https://doi.org/10.1017/CBO9780511752292.013

Schindelin, J., Arganda‐Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., Tinevez, J.‐Y., White, D. J., Hartenstein, V., Eliceiri, K., Tomancak, P., & Cardona, A. (2012). Fiji: An open‐source platform for biological‐image analysis. Nature Methods, 9, 676–682. https://doi.org/10.1038/nmeth.2019

Shaviv, N. J., & Veizer, J. (2003). Celestial driver of Phanerozoic climate? GSA Today, 13, 4. https://doi.org/10.1130/1052‐5173(2003)013<0004:CDOPC>2.0.CO;2

Siver, P. A. (1991). The biology of mallomonas. Springer. https://doi.org/10.1007/978‐94‐011‐3376‐0

Siver, P. A. (1995). The distribution of chrysophytes along environmental gradients: Their use as biological indicators. In C. D. Sandgren, J. P. Smol, & J. Kristiansen (Eds.), Chrysophyte algae (1st ed., pp. 232–268). Cambridge University Press. https://doi.org/10.1017/CBO9780511752292.012

Siver, P. A., & Glew, J. R. (1990). The arrangement of scales and bristles on Mallomonas (Chrysophyceae): A proposed mechanism for the formation of the cell covering. Canadian Journal of Botany, 68, 374–380. https://doi.org/10.1139/b90‐049

Siver, P. A., Jo, B. Y., Kim, J. I., Shin, W., Lott, A. M., & Wolfe, A. P. (2015). Assessing the evolutionary history of the class Synurophyceae (Heterokonta) using molecular, morphometric, and paleobiological approaches. American Journal of Botany, 102, 921–941. https://doi.org/10.3732/ajb.1500004

Siver, P. A., Wolfe, A. P., Rohlf, F. J., Shin, W., & Jo, B. Y. (2013). Combining geometric morphometrics, molecular phylogeny, and micropaleontology to assess evolutionary patterns in Mallomonas (Synurophyceae: Heterokontophyta). Geobiology, 11, 127–138. https://doi.org/10.1111/gbi.12023

Škaloud, P., Jadrná, I., Dvořák, P., Škvorová, Z., Pusztai, M., Čertnerová, D., Bestová, H., & Rengefors, K. (2024). Rapid diversification of a free‐living protist is driven by adaptation to climate and habitat. Current Biology, 34(1), 92–105.e6. https://doi.org/10.1016/j.cub.2023.11.046

Smith, R. C., Prézelin, B. B., Baker, K. S., Bidigare, R. R., Boucher, N. P., Coley, T., Karentz, D., MacIntyre, S., Matlick, H. A., Menzies, D., Ondrusek, M., Wan, Z., & Waters, K. J. (1992). Ozone depletion: Ultraviolet radiation and phytoplankton biology in antarctic waters. Science, 255, 952–959. https://doi.org/10.1126/science.1546292

Sprouffske, K., & Wagner, A. (2016). Growthcurver: An R package for obtaining interpretable metrics from microbial growth curves. BMC Bioinformatics, 17, 172. https://doi.org/10.1186/s12859‐016‐1016‐7

Stamatakis, A. (2014). RAxML version 8: A tool for phylogenetic analysis and post‐analysis of large phylogenies. Bioinformatics, 30, 1312–1313. https://doi.org/10.1093/bioinformatics/btu033

Su, Y., Lenau, T. A., Gundersen, E., Kirkensgaard, J. J. K., Maibohm, C., Pinti, J., & Ellegaard, M. (2018). The UV filtering potential of drop‐casted layers of frustules of three diatom species. Scientific Reports, 8, 959. https://doi.org/10.1038/s41598‐018‐19596‐4

Todor, H., Dulmage, K., Gillum, N., Bain, J. R., Muehlbauer, M. J., & Schmid, A. K. (2014). A transcription factor links growth rate and metabolism in the hypersaline adapted archaeon Halobacterium salinarum. Molecular Microbiology, 93, 1172–1182. https://doi.org/10.1111/mmi.12726

Waring, J., Underwood, G. J. C., & Baker, N. R. (2006). Impact of elevated UV‐B radiation on photosynthetic electron transport, primary productivity and carbon allocation in estuarine epipelic diatoms. Plant, Cell & Environment, 29, 521–534. https://doi.org/10.1111/j.1365‐3040.2005.01429.x

Weatherill, K., Lambiris, I., Pickett‐Heaps, J. D., Deane, J. A., & Beech, P. L. (2007). Plastid division in Mallomonas (Synurophyceae, Heterokonta). Journal of Phycology, 43, 535–541. https://doi.org/10.1111/j.1529‐8817.2007.00356.x

Wickham, H. (2016). Ggplot2: Elegant graphics for data analysis. Springer‐Verlag. https://ggplot2.tidyverse.org

Xu, H., Shi, Z., Zhang, X., Pang, M., Pan, K., & Liu, H. (2021). Diatom frustules with different silica contents affect copepod grazing due to differences in the nanoscale mechanical properties. Limnology and Oceanography, 66, 3408–3420. https://doi.org/10.1002/lno.11887

Zhang, W., Yang, H., Xia, X., Xie, L., & Xie, G. (2016). Triassic chrysophyte cyst fossils discovered in the Ordos Basin, China. Geology, 44, 1031–1034. https://doi.org/10.1130/G38527.1

Zhang, Y., Shen, W., Li, L., Long, Z., Li, S., Li, T., Wang, Y., Inganäs, O., & Tang, J. (2022). Living diatoms integrate polysaccharide‐Eu3+ complex for UV downconversion. Journal of Materials Research and Technology, 19, 2774–2780. https://doi.org/10.1016/j.jmrt.2022.05.187

Zudaire, L., & Roy, S. (2001). Photoprotection and long‐term acclimation to UV radiation in the marine diatom Thalassiosira weissflogii. Journal of Photochemistry and Photobiology B: Biology, 62, 26–34. https://doi.org/10.1016/S1011‐1344(01)00150‐6

Expanding our knowledge of Synurales (Chrysophyceae) in Florida, United States: Proposing three novel Mallomonas taxa