Abstract
The effect of ultraviolet radiation (UVR) on photosynthetic efficiency and the resulting mechanisms against UV exposure employed by phytoplankton are not completely understood. To address this knowledge gap, we developed a novel close-coupled, wavelength-configurable platform designed to produce precise and repeatable in vitro irradiation of Corethron hystrix, a member of a genera found abundantly in the Southern Ocean where UV exposure is high. We aimed to determine its metabolic, protective, and repair mechanisms as a function of varying levels of specific electromagnetic energy. Our results show that the physiological responses to each energy level of UV have a negative linear decrease in the photosynthetic efficiency of photosystem II proportional to UV intensity, corresponding to a large increase in the turnover time of quinone reoxidation. Gene expression changes of photosystem II-related reaction center proteins D1, CP43, and CP47 showed coordinated downregulation whereas the central metabolic pathway demonstrated mixed expression of up and downregulated transcripts after UVR exposure. These results suggest that while UVR may damage photosynthetic machinery, oxidative damage may limit production of new photosynthetic and electron transport complexes as a result of UVR exposure.
This is a preview of subscription content, log in via an institution to check access.
References
Allen AE, Laroche J, Maheswari U, Lommer M, Schauer N, Lopez PJ, Finazzi G, Fernie AR, Bowler C (2008) Whole-cell response of the pennate diatom Phaeodactylum tricornutum to iron starvation. Proc Natl Acad Sci U S A 105:10438–10443. https://doi.org/10.1073/pnas.0711370105
Andrews S (2009) FastQC A Quality control tool for high throughput sequence data. https://www.bioinformatics.babraham.ac.uk/projects/fastqc/
Armbrust EV (2009) The life of diatoms in the world's oceans. Nature 459:185–192
Armbrust EV, Berges JA, Bowler C, Green BR, Martinez D, Putnam NH, Zhou S, Allen AE, Apt KE, Bechner M, Brzezinski MA, Chaal BK, Chiovitti A, Davis AK, Demarest MS, Detter JC, Glavina T, Goodstein D, Hadi MZ, Hellsten U, Hildebrand M, Jenkins BD, Jurka J, Kapitonov VV, Kröger N, Lau WWY, Lane TW, Larimer FW, Lippmeier JC, Lucas S, Medina M, Montsant A, Obornik M, Parker MS, Palenik B, Pazour GJ, Richardson PM, Rynearson TA, Saito MA, Schwartz DC, Thamatrakoln K, Valentin K, Vardi A, Wilkerson FP, Rokhsar DS (2004) The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306:79–86. https://doi.org/10.1126/science.1101156
Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G (2000) Gene ontology: tool for the unification of biology. Nat Genet 25:25–29. https://doi.org/10.1038/75556
Bender SJ, Durkin CA, Berthiaume CT, Morales RL, Armbrust EV (2014) Transcriptional responses of three model diatoms to nitrate limitation of growth. Front Mar Sci 1:1–15. https://doi.org/10.3389/fmars.2014.00003
Berardesca E, Bertona M, Altabas K, Altabas V, Emanuele E (2012) Reduced ultraviolet-induced DNA damage and apoptosis in human skin with topical application of a photolyase-containing DNA repair enzyme cream: clues to skin cancer prevention. Mol Med Rep 5:570–574. https://doi.org/10.3892/mmr.2011.673
Bilgin DD, Zavala JA, Zhu J, Clough SJ, Ort DR, DeLucia EH (2010) Biotic stress globally downregulates photosynthesis genes. Plant Cell Environ 33:1597–1613. https://doi.org/10.1111/j.1365-3040.2010.02167.x
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. https://doi.org/10.1093/bioinformatics/btu170
Bornman JF, Vogelmann TC (1991) Effect of UV-B radiation on leaf optical properties measured with fibre optics. J Exp Bot 42:547–554
Bouchard JN, Roy S, Campbell DA (2006) UVB effects on the photosystem II-D1 protein of phytoplankton and natural phytoplankton communities. Photochem Photobiol 82:936–951. https://doi.org/10.1562/2005-08-31-IR-666
Casati P, Walbot V (2003) Gene expression profiling in response to ultraviolet radiation in maize genotypes with varying flavonoid content. Plant Physiol 132:1739–1754. https://doi.org/10.1104/pp.103.022871
Choi BY, Roh KS (2003) UV-B radiation affects chlorophyll and activation of rubisco by rubisco activase in Canavalia ensiformis L. leaves. J Plant Biol 46:117–121. https://doi.org/10.1007/BF03030440
Coesel S, Mangogna M, Ishikawa T, Heijde M, Rogato A, Finazzi G, Todo T, Bowler C, Falciatore A (2009) Diatom PtCPF1 is a new cryptochrome/photolyase family member with DNA repair and transcription regulation activity. EMBO Rep 10:655–661. https://doi.org/10.1038/embor.2009.59
Critchley C (2000) Photoinhibition. In: Raghavendra AS (ed) Photosynthesis A Comprehensive Treatise. Cambridge University Press, Cambridge, UK, pp 264–272
Cullen JJ, Lesser MP (1991) Inhibition of photosynthesis by ultraviolet radiation as a function of dose and dosage rate: results for a marine diatom. Mar Biol 111:183–190. https://doi.org/10.1007/BF01319699
De Mora S, Demers S, Vernet M (2000) The effects of UV radiation in the marine environment. Cambridge University Press, Cambridge, UK
Domingues N, Matos AR, Marques da Silva J, Cartaxana P (2012) Response of the diatom Phaeodactylum tricornutum to photooxidative stress resulting from high light exposure. PLoS One 7:e38162–e38166. https://doi.org/10.1371/journal.pone.0038162
Dyhrman ST, Jenkins BD, Rynearson TA, Saito MA, Mercier ML, Alexander H, Whitney LP, Drzewianowski A, Bulygin VV, Bertrand EM, Wu Z, Benitez-Nelson C, Heithoff A (2012) The transcriptome and proteome of the diatom Thalassiosira pseudonana reveal a diverse phosphorus stress response. PLoS One 7:e33768. https://doi.org/10.1371/journal.pone.0033768
Emanuele E, Altabas V, Altabas K, Berardesca E (2013) Topical application of preparations containing DNA repair enzymes prevents ultraviolet-induced telomere shortening and c-FOS proto-oncogene hyperexpression in human skin: an experimental pilot study. J Drugs Dermatol 12:1017–1021
Falkowski PG, Raven JA (2007) Aquatic photosynthesis, 2nd edn. Princeton University Press, Princeton, NJ
Fricke A, Molis M, Wiencke C, Valdivia N, Chapman AS (2011) Effects of UV radiation on the structure of Arctic macrobenthic communities. Polar Biol 34:995–1009. https://doi.org/10.1007/s00300-011-0959-4
Fritz JJ, Neale PJ, Davis RF, Peloquin JA (2008) Response of Antarctic phytoplankton to solar UVR exposure: inhibition and recovery of photosynthesis in coastal and pelagic assemblages. Mar Ecol Prog Ser 365:1–16. https://doi.org/10.3354/meps07610
Frohnmeyer H, Staiger D (2003) Ultraviolet-B radiation-mediated responses in plants. Balancing damage and protection. Plant Physiol 133:1420–1428. https://doi.org/10.1104/pp.103.030049
Geider RJ, Greene RM, Kolber Z, MacIntyre HL, Falkowski PG (1993) Fluorescence assessment of the maximum quantum efficiency of photosynthesis in the western North Atlantic. Deep-Sea Res Pt I 40:1205–1224. https://doi.org/10.1016/0967-0637(93)90134-o
Gilstad M, Sakshaug E (1990) Growth rates of ten diatom species from the Barents Sea at different irradiances and day lengths. Mar Ecol Prog Ser 64:169–173. https://doi.org/10.3354/meps064169
Gladman S, Seemann T (2012) VelvetOptimiser: automate your Velvet assemblies. https://github.com/tseemann/VelvetOptimiser
Gray JC (1992) Cytochrome f: Structure, function and biosynthesis. Photosynth Res 34:359–374. https://doi.org/10.1007/BF00029811
Greenberg B, Wilson M, Huang X-D, Duxbury C, Gerhardt K, Gensemer R (1997) The effects of ultraviolet-B radiation on higher plants. In: Wuncheng W (ed) Plants for Environmental Studies. CRC Press, Boca Raton, Florida, pp 1–35
Guillard RRL, Hargraves PE (1993) Stichochrysis immobilis is a diatom, not a chrysophyte. Phycologia 32:234–236
Gururani MA, Venkatesh J, Tran L-SP (2015) Regulation of photosynthesis during abiotic stress-induced photoinhibition. Mol Plant 8:1304–1320. https://doi.org/10.1016/j.molp.2015.05.005
Heitman J, Model P (1987) Site-specific methylases induce the SOS DNA repair response in Escherichia coli. J Bacteriol 169:3243–3250
Helbling EW, Chalker BE, Dunlap WC, Holm-Hansen O, Villafañe VE (1996) Photoacclimation of antarctic marine diatoms to solar ultraviolet radiation. J Exp Mar Biol Ecol 204:85–101. https://doi.org/10.1016/0022-0981(96)02591-9
Herbstová M, Bína D, Koník P, Gardian Z, Vácha F, Litvín R (2015) Molecular basis of chromatic adaptation in pennate diatom Phaeodactylum tricornutum. BBA-Bioenergetics 1847:534–543. https://doi.org/10.1016/j.bbabio.2015.02.016
Hou HJM, Najafpour MM, Moore GF, Allakhverdiev SI (eds) (2017) Photosynthesis: structures, mechanisms, and applications. Springer International Publishing, New York City, NY
Huang L, McCluskey MP, Ni H, LaRossa RA (2002) Global gene expression profiles of the cyanobacterium Synechocystis sp. strain PCC 6803 in response to irradiation with UV-B and white light. J Bacteriol 184:6845–6858. https://doi.org/10.1128/JB.184.24.6845-6858.2002
Ifuku K, Noguchi T (2016) Structural coupling of extrinsic proteins with the oxygen-evolving center in photosystem II. Front Plant Sci 7:84. https://doi.org/10.3389/fpls.2016.00084
Ifuku K, Ido K, Sato F (2011) Molecular functions of PsbP and PsbQ proteins in the photosystem II supercomplex. J Photochem Photobiol B Biol 104:158–164. https://doi.org/10.1016/j.jphotobiol.2011.02.006
Janion C, Sikora nee Wójcik A, Nowosielska A, Grzesiuk E (2002) Induction of the SOS response in starved Escherichia coli. Environ Mol Mutagen 40:129–133. https://doi.org/10.1002/em.10094
Jenkins GI (2009) Signal transduction in responses to UV-B radiation. Annu Rev Plant Biol 60:407–431. https://doi.org/10.1146/annurev.arplant.59.032607.092953
Kanehisa M, Goto S (2000) KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28:27–30
Kanehisa M, Goto S, Sato Y, Kawashima M, Furumichi M, Tanabe M (2013) Data, information, knowledge and principle: back to metabolism in KEGG. Nucleic Acids Res 42:D199–D205. https://doi.org/10.1093/nar/gkt1076
Karentz D, Cleaver JE, Mitchell DL (1991) Cell survival characteristics and molecular responses of Antarctic phytoplankton to ultraviolet-B radiation. J Phycol 27:326–341. https://doi.org/10.1111/j.0022-3646.1991.00326.x
Kolber Z, Falkowski PG (1993) Use of active fluorescence to estimate phytoplankton photosynthesis in situ. Limnol Oceanogr 38:1646–1665. https://doi.org/10.4319/lo.1993.38.8.1646
Kolber Z, Zehr J, Falkowski P (1988) Effects of growth irradiance and nitrogen limitation on photosynthetic energy conversion in photosystem II. Plant Physiol 88:923–929
Kolber ZS, Prášil O, Falkowski PG (1998) Measurements of variable chlorophyll fluorescence using fast repetition rate techniques: defining methodology and experimental protocols. BBA 1367:88–106. https://doi.org/10.1016/s0005-2728(98)00135-2
Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359. https://doi.org/10.1038/nmeth.1923
Lao K, Glazer AN (1996) Ultraviolet-B photodestruction of a light-harvesting complex. Proc Natl Acad Sci U S A 93:5258–5263
Ligowski R, Jordan RW, Assmy P (2012) Morphological adaptation of a planktonic diatom to growth in Antarctic sea ice. Mar Biol 159:817–827. https://doi.org/10.1007/s00227-011-1857-6
Logemann E, Tavernaro A, Schulz W, Somssich IE, Hahlbrock K (2000) UV light selectively coinduces supply pathways from primary metabolism and flavonoid secondary product formation in parsley. Proc Natl Acad Sci U S A 97:1903–1907
Lohman KE (1960) The ubiquitous diatom–a brief survey of the present state of knowledge. Am J Sci A 258:180–191
Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15:550. https://doi.org/10.1186/s13059-014-0550-8
Mackerness S, Jordan BR, Thomas B (1999) Reactive oxygen species in the regulation of photosynthetic genes by ultraviolet-B radiation (UV-B: 280–320 nm) in green and etiolated buds of pea (Pisum sativum L.). J Photochem Photobiol B Biol 48:180–188. https://doi.org/10.1016/s1011-1344(99)00024-x
Marchetti A, Schruth DM, Durkin CA, Parker MS, Kodner RB, Berthiaume CT, Morales R, Allen AE, Armbrust EV (2012) Comparative metatranscriptomics identifies molecular bases for the physiological responses of phytoplankton to varying iron availability. Proc Natl Acad Sci U S A 109:E317–E325. https://doi.org/10.1073/pnas.1118408109
Mauzerall D (1986) The optical cross section and absolute size of a photosynthetic unit. Photosynth Res 10:163–170. https://doi.org/10.1007/BF00118279
Maxwell DP, Laudenbach DE, Huner N (1995) Redox regulation of light-harvesting complex II and cab mRNA abundance in Dunaliella salina. Plant Physiol 109:787–795
Melis A, Nemson JA, Harrison MA (1992) Damage to functional components and partial degradation of photosystem II reaction center proteins upon chloroplast exposure to ultraviolet-B radiation. BBA-Bioenergetics 1100:312–320. https://doi.org/10.1016/0167-4838(92)90487-x
Nawkar G, Maibam P, Park J, Sahi V, Lee S, Kang C (2013) UV-induced cell death in plants. Int J Mol Sci 14:1608–1628. https://doi.org/10.3390/ijms14011608
Neale PJ, Cullen JJ, Davis RF (1998) Inhibition of marine photosynthesis by ultraviolet radiation: variable sensitivity of phytoplankton in the Weddell-Scotia Confluence during the austral spring. Limnol Oceanogr 43:433–448. https://doi.org/10.4319/lo.1998.43.3.0433
Nelson DL, Cox MM (2005) Lehninger principles of biochemistry, 4th edn. W. H. Freeman and Company, New York City, NY
Olinares PDB, Kim J, van Wijk KJ (2011) The Clp protease system; a central component of the chloroplast protease network. BBA-Bioenergetics 1807:999–1011. https://doi.org/10.1016/j.bbabio.2010.12.003
Oxborough K, Moore CM, Suggett DJ, Lawson T, Chan HG, Geider RJ (2012) Direct estimation of functional PSII reaction center concentration and PSII electron flux on a volume basis: a new approach to the analysis of Fast Repetition Rate fluorometry (FRRf) data. Limnol Oceanogr Methods 10:142–154. https://doi.org/10.4319/lom.2012.10.142
Pierre Y, Breyton C, Kramer D, Popot JL (1995) Purification and characterization of the cytochrome b6 f complex from Chlamydomonas reinhardtii. J Biol Chem 270:29342–29349
Post A, Lukins PB, Walker PJ, Larkum AW (1996) The effects of ultraviolet irradiation on P680+ reduction in PS II core complexes measured for individual S-states and during repetitive cycling of the oxygen-evolving complex. Photosynth Res 49:21–27. https://doi.org/10.1007/BF00029424
Ragni M, Airs RL, Leonardos N, Geider RJ (2008) Photoinhibition of PsII in Emiliania Huxleyi (Haptophyta) under high light stress: the roles of photoacclimation, photoprotection, and photorepair. J Phycol 44:670–683. https://doi.org/10.1111/j.1529-8817.2008.00524.x
Rajagopal S, Murthy SD, Mohanty P (2000) Effect of ultraviolet-B radiation on intact cells of the cyanobacterium Spirulina platensis: characterization of the alterations in the thylakoid membranes. J Photochem Photobiol B Biol 54:61–66. https://doi.org/10.1016/S1011-1344(99)00156-6
Rastogi RP, Richa KA, Tyagi MB, Sinha RP (2010) Molecular mechanisms of ultraviolet radiation-induced DNA damage and repair. J Nucleic Acids 2010:592980–592932. https://doi.org/10.4061/2010/592980
Raven JA (2009) Contributions of anoxygenic and oxygenic phototrophy and chemolithotrophy to carbon and oxygen fluxes in aquatic environments. Aquat Microb Ecol 56:177–192. https://doi.org/10.3354/ame01315
Raven JA (2013) Rubisco: still the most abundant protein of Earth? New Phytol 198:1–3. https://doi.org/10.1111/nph.12197
Remmert M, Biegert A, Hauser A, Söding J (2011) HHblits: lightning-fast iterative protein sequence searching by HMM-HMM alignment. Nat Methods 9:173–175. https://doi.org/10.1038/nmeth.1818
Rijstenbil JW (2002) Assessment of oxidative stress in the planktonic diatom Thalassiosira pseudonana in response to UVA and UVB radiation. J Plankton Res 24:1277–1288. https://doi.org/10.1093/plankt/24.12.1277
Roberts A, Pachter L (2012) Streaming fragment assignment for real-time analysis of sequencing experiments. Nat Methods 10:71–73. https://doi.org/10.1038/nmeth.2251
Schulz MH, Zerbino DR, Vingron M, Birney E (2012) Oases: robust de novo RNA-seq assembly across the dynamic range of expression levels. Bioinformatics 28:1086–1092. https://doi.org/10.1093/bioinformatics/bts094
Sharon Y, Dishon G, Beer S (2011) The effects of UV radiation on chloroplast clumping and photosynthesis in the seagrass Halophila stipulacea grown under high-PAR conditions. Mar Biol 2011:1–6. https://doi.org/10.1155/2011/483428
Shrestha RP, Tesson B, Norden-Krichmar T, Federowicz S, Hildebrand M, Allen AE (2012) Whole transcriptome analysis of the silicon response of the diatom Thalassiosira pseudonana. BMC Genomics 13:499. https://doi.org/10.1186/1471-2164-13-499
Sinha RP, Häder D-P (2002) UV-induced DNA damage and repair: a review. Photochem Photobiol Sci 1:225–236. https://doi.org/10.1039/b201230h
Smith KC, Wang TV, Sharma RC (1987) recA-dependent DNA repair in UV-irradiated Escherichia coli. J Photochem Photobiol B Biol 1:1–11
Soding J (2005) Protein homology detection by HMM-HMM comparison. Bioinformatics 21:951–960. https://doi.org/10.1093/bioinformatics/bti125
Strid Å, Chow WS, Anderson JM (1990) Effects of supplementary ultraviolet-B radiation on photosynthesis in Pisum sativum. BBA 1020:260–268. https://doi.org/10.1016/0005-2728(90)90156-x
Suggett DJ, Moore CM, Hickman AE, Geider RJ (2009) Interpretation of fast repetition rate (FRR) fluorescence: signatures of phytoplankton community structure versus physiological state. Mar Ecol Prog Ser 376:1–19. https://doi.org/10.3354/meps07830
Surplus SL, Jordan BR, Murphy AM, Carr JP, Thomas B, Mackerness SAH (1998) Ultraviolet-B-induced responses in Arabidopsis thaliana: role of salicylic acid and reactive oxygen species in the regulation of transcripts encoding photosynthetic and acidic pathogenesis-related proteins. Plant Cell Environ 21:685–694. https://doi.org/10.1046/j.1365-3040.1998.00325.x
Szilárd A, Sass L, Deák Z, Vass I (2007) The sensitivity of photosystem II to damage by UV-B radiation depends on the oxidation state of the water-splitting complex. BBA 1767:876–882. https://doi.org/10.1016/j.bbabio.2006.11.020
Teramura AH, Ziska LH (1996) Ultraviolet-B radiation and photosynthesis. In: Baker NR (ed) Photosynthesis and the Environment. Springer Netherlands, Dordrecht, NL, pp 435–450
Tevini M, Teramura AH (1989) UV-B effects on terrestrial plants. Photochem Photobiol 50:479–487. https://doi.org/10.1111/j.1751-1097.1989.tb05552.x
The Gene Ontology Consortium (2017) Expansion of the gene ontology knowledgebase and resources. Nucleic Acids Res 45:D331–D338. https://doi.org/10.1093/nar/gkw1108
The UniProt Consortium (2017) UniProt: the universal protein knowledgebase. Nucleic Acids Res 45:D158–D169. https://doi.org/10.1093/nar/gkw1099
Vass I, Sass L, Spetea C, Bakou A, Ghanotakis DF, Petrouleas V (1996) UV-B-induced inhibition of photosystem II electron transport studied by EPR and chlorophyll fluorescence. Impairment of donor and acceptor side components. Biochemistry 35:8964–8973. https://doi.org/10.1021/bi9530595
Verde C, Prisco GD (2012) Adaptation and evolution in marine environments, Volume 2: The impacts of global change on biodiversity. Springer, Berlin/Heidelberg, DE
Vincent WF (1988) Microbial ecosystems of Antarctica. Cambridge University Press, Cambridge, UK
Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer New York, New York City, NY
Wu Y, Li Z, Du W, Gao K (2015) Physiological response of marine centric diatoms to ultraviolet radiation, with special reference to cell size. J Photochem Photobiol B Biol 153:1–6. https://doi.org/10.1016/j.jphotobiol.2015.08.035
Zerbino DR, Birney E (2008) Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18:821–829. https://doi.org/10.1101/gr.074492.107
Zhang Z-S, Jin L-Q, Li Y-T, Tikkanen M, Li Q-M, Ai X-Z, Gao H-Y (2016) Ultraviolet-B radiation (UV-B) relieves chilling-light-induced PSI photoinhibition and accelerates the recovery of CO2 assimilation in cucumber (Cucumis sativus L.) leaves. Sci Rep 6:34455. https://doi.org/10.1038/srep34455
Zulu NN, Zienkiewicz K, Vollheyde K, Feussner I (2018) Current trends to comprehend lipid metabolism in diatoms. Prog Lipid Res 70:1–16
Acknowledgements
We would like to thank Dr. Zbigniew Kolber for his expertise and guidance during the manuscript preparation.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
Authors Robert Read, David Vuono, and Iva Neveux declare that they have no conflict of interest. Authors Joseph Grzymski and Carl Staub have a conflict of interest as they are co-founders of the company, EMS Genomics, that developed the light engine.
Ethical approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(PDF 717 kb)
Rights and permissions
About this article
Cite this article
Read, R.W., Vuono, D.C., Neveux, I. et al. Coordinated downregulation of the photosynthetic apparatus as a protective mechanism against UV exposure in the diatom Corethron hystrix. Appl Microbiol Biotechnol 103, 1837–1850 (2019). https://doi.org/10.1007/s00253-018-9544-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-018-9544-x