Fe limitation decreases transcriptional regulation over the diel cycle in the model diatom Thalassiosira pseudonana

English version

Autoři: Johanna A. L. Goldman ^aff001; Megan J. Schatz ^aff001; Chris T. Berthiaume ^aff001; Sacha N. Coesel ^aff001; Mónica V. Orellana ^aff002; E. Virginia Armbrust ^aff001
Působiště autorů: School of Oceanography, University of Washington, Seattle, Washington, United States of America ^aff001; Polar Science Center, Applied Physics Laboratory, University of Washington, Seattle, Washington, United States of America ^aff002; Institute for Systems Biology, Seattle, Washington, United States of America ^aff003
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0222325

Souhrn

Iron (Fe) is an important growth factor for diatoms and its availability is further restricted by changes in the carbonate chemistry of seawater. We investigated the physiological attributes and transcriptional profiles of the diatom Thalassiosira pseudonana grown on a day: night cycle under different CO₂/pH and iron concentrations, that in combination generated available iron (Fe’) concentrations of 1160, 233, 58 and 12 pM. We found the light-dark conditions to be the main driver of transcriptional patterns, followed by Fe’ concentration and CO₂ availability, respectively. At the highest Fe’ (1160 pM), 55% of the transcribed genes were differentially expressed between day and night, whereas at the lowest Fe’ (12 pM), only 28% of the transcribed genes displayed comparable patterns. While Fe limitation disrupts the diel expression patterns for genes in most central metabolism pathways, the diel expression of light- signaling molecules and glycolytic genes was relatively robust in response to reduced Fe’. Moreover, we identified a non-canonical splicing of transcripts encoding triose-phosphate isomerase, a key-enzyme of glycolysis, generating transcript isoforms that would encode proteins with and without an active site. Transcripts that encoded an active enzyme maintained a diel expression at low Fe’, while transcripts that encoded the non-active enzyme lost the diel expression. This work illustrates the interplay between nutrient limitation and transcriptional regulation over the diel cycle. Considering that future ocean conditions will reduce the availability of Fe in many parts of the oceans, our work identifies some of the regulatory mechanisms that may shape future ecological communities.

Klíčová slova:

Biology and life sciences – Genetics – Gene expression – Biochemistry – Organisms – Eukaryota – Plants – Physical sciences – Chemistry – Animals – Invertebrates – Gene regulation – Chemical compounds – Phosphates – Metabolism – Physics – Earth sciences – Ecology and environmental sciences – DNA transcription – Algae – Phytoplankton – Diatoms – Plankton – Metabolic processes – Glycolysis – Atmospheric science – Atmospheric chemistry – Greenhouse gases – Carbon dioxide – Environmental chemistry – Electromagnetic radiation – Light

Zdroje

1. Armbrust EV. The life of diatoms in the world's oceans. Nature. 2009;459(7244):185. doi: 10.1038/nature08057 19444204

2. Falkowski PG, Katz ME, Knoll AH, Quigg A, Raven JA, Schofield O, et al. The evolution of modern eukaryotic phytoplankton. Science. 2004;305(5682):354–60. doi: 10.1126/science.1095964 15256663

3. Nelson DM, Tréguer P, Brzezinski MA, Leynaert A, Quéguiner B. Production and dissolution of biogenic silica in the ocean: revised global estimates, comparison with regional data and relationship to biogenic sedimentation. Global Biogeochemical Cycles. 1995;9(3):359–72.

4. Huysman MJ, Fortunato AE, Matthijs M, Costa BS, Vanderhaeghen R, Van den Daele H, et al. AUREOCHROME1a-mediated induction of the diatom-specific cyclin dsCYC2 controls the onset of cell division in diatoms (Phaeodactylum tricornutum). The Plant Cell. 2013;25(1):215–28. doi: 10.1105/tpc.112.106377 23292736

5. Olson R, Chisholm S. Effects of photocycles and periodic ammonium supply on three marine phytoplankton species. I: Cell division patterns. Journal of Phycology. 1983;19(4):522–8.

6. Vaulot D, Olson R, Merkel S, Chisholm S. Cell-cycle response to nutrient starvation in two phytoplankton species, Thalassiosira weissflogii and Hymenomonas carterae. Marine Biology. 1987;95(4):625–30.

7. Behrenfeld MJ, Milligan AJ. Photophysiological expressions of iron stress in phytoplankton. Annual Review of Marine Science. 2013;5:217–46. doi: 10.1146/annurev-marine-121211-172356 22881354

8. Moore C, Mills M, Arrigo K, Berman-Frank I, Bopp L, Boyd P, et al. Processes and patterns of oceanic nutrient limitation. Nature Geoscience. 2013;6(9):701.

9. Boyd PW, Jickells T, Law C, Blain S, Boyle E, Buesseler K, et al. Mesoscale iron enrichment experiments 1993–2005: synthesis and future directions. Science. 2007;315(5812):612–7. doi: 10.1126/science.1131669 17272712

10. Shi D, Xu Y, Hopkinson BM, Morel FM. Effect of ocean acidification on iron availability to marine phytoplankton. Science. 2010;327(5966):676–9. doi: 10.1126/science.1183517 20075213

11. McQuaid JB, Kustka AB, Oborník M, Horák A, McCrow JP, Karas BJ, et al. Carbonate-sensitive phytotransferrin controls high-affinity iron uptake in diatoms. Nature. 2018;555(7697):534. doi: 10.1038/nature25982 29539640

12. Marchetti A, Schruth DM, Durkin CA, Parker MS, Kodner RB, Berthiaume CT, et al. Comparative metatranscriptomics identifies molecular bases for the physiological responses of phytoplankton to varying iron availability. Proceedings of the National Academy of Sciences. 2012;109(6):E317–E25.

13. Lampe RH, Mann EL, Cohen NR, Till CP, Thamatrakoln K, Brzezinski MA, et al. Different iron storage strategies among bloom-forming diatoms. Proceedings of the National Academy of Sciences. 2018;115(52):E12275–E84.

14. Strzepek RF, Harrison PJ. Photosynthetic architecture differs in coastal and oceanic diatoms. Nature. 2004;431(7009):689. doi: 10.1038/nature02954 15470428

15. La Roche J, Boyd PW, McKay RML, Geider RJ. Flavodoxin as an in situ marker for iron stress in phytoplankton. Nature. 1996;382(6594):802.

16. Marchetti A, Cassar N. Diatom elemental and morphological changes in response to iron limitation: a brief review with potential paleoceanographic applications. Geobiology. 2009;7(4):419–31. doi: 10.1111/j.1472-4669.2009.00207.x 19659798

17. Owens T, Falkowski P, Whitledge T. Diel periodicity in cellular chlorophyll content in marine diatoms. Marine Biology. 1980;59(2):71–7.

18. Ragni M, d'Alcalà MR. Circadian variability in the photobiology of Phaeodactylum tricornutum: pigment content. Journal of Plankton Research. 2007;29(2):141–56.

19. Ashworth J, Coesel S, Lee A, Armbrust EV, Orellana MV, Baliga NS. Genome-wide diel growth state transitions in the diatom Thalassiosira pseudonana. Proceedings of the National Academy of Sciences. 2013;110(18):7518–23.

20. Smith SR, Gillard JT, Kustka AB, McCrow JP, Badger JH, Zheng H, et al. Transcriptional orchestration of the global cellular response of a model pennate diatom to diel light cycling under iron limitation. PLoS Genetics. 2016;12(12):e1006490. doi: 10.1371/journal.pgen.1006490 27973599

21. van Oijen T, van Leeuwe MA, Gieskes WW, de Baar HJ. Effects of iron limitation on photosynthesis and carbohydrate metabolism in the Antarctic diatom Chaetoceros brevis (Bacillariophyceae). European Journal of Phycology. 2004;39(2):161–71.

22. Sunda WG, Price NM, Morel FM. Trace metal ion buffers and their use in culture studies. In: Anderson RA, editor. Algal culturing techniques. New York, USA: Elsevier Academic Press; 2005. p. 35–63.

23. Morel FM, Hering JG. Principles and applications of aquatic chemistry: John Wiley & Sons; 1993.

24. Strickland JD, Parsons TR. A practical handbook of seawater analysis. 1972.

25. Dickson AG, Sabine CL, Christian JR. Guide to best practices for ocean CO2 measurements: North Pacific Marine Science Organization; 2007.

26. Lewis E, Wallace D, Allison LJ. Program developed for CO {sub 2} system calculations. Brookhaven National Lab., Dept. of Applied Science, Upton, NY (United States); Oak Ridge National Lab., Carbon Dioxide Information Analysis Center, TN (United States), 1998.

27. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30(15):2114–20. doi: 10.1093/bioinformatics/btu170 24695404

28. Kim D, Langmead B, Salzberg SL. HISAT: a fast spliced aligner with low memory requirements. Nature methods. 2015;12(4):357. doi: 10.1038/nmeth.3317 25751142

29. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26(1):139–40. doi: 10.1093/bioinformatics/btp616 19910308

30. Rayko E, Maumus F, Maheswari U, Jabbari K, Bowler C. Transcription factor families inferred from genome sequences of photosynthetic stramenopiles. New Phytologist. 2010;188(1):52–66. doi: 10.1111/j.1469-8137.2010.03371.x 20646219

31. Montsant A, Allen AE, Coesel S, Martino AD, Falciatore A, Mangogna M, et al. Identification and comparative genomic analysis of signaling and regulatory components in the diatom Thalassiosira pseudonana. Journal of Phycology. 2007;43(3):585–604.

32. Levering J, Broddrick J, Dupont CL, Peers G, Beeri K, Mayers J, et al. Genome-scale model reveals metabolic basis of biomass partitioning in a model diatom. PLoS One. 2016;11(5):e0155038. doi: 10.1371/journal.pone.0155038 27152931

33. Pertea M, Kim D, Pertea GM, Leek JT, Salzberg SL. Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown. Nature Protocols. 2016;11(9):1650. doi: 10.1038/nprot.2016.095 27560171

34. Bray NL, Pimentel H, Melsted P, Pachter L. Near-optimal probabilistic RNA-seq quantification. Nature Biotechnology. 2016;34(5):525. doi: 10.1038/nbt.3519 27043002

35. Smith SR, Abbriano RM, Hildebrand M. Comparative analysis of diatom genomes reveals substantial differences in the organization of carbon partitioning pathways. Algal Research. 2012;1(1):2–16.

36. Wang Z-Y, Kenigsbuch D, Sun L, Harel E, Ong MS, Tobin EM. A Myb-related transcription factor is involved in the phytochrome regulation of an Arabidopsis Lhcb gene. The Plant Cell Online. 1997;9(4):491–507.

37. Hennon GM, Quay P, Morales RL, Swanson LM, Virginia Armbrust E. Acclimation conditions modify physiological response of the diatom Thalassiosira pseudonana to elevated CO2 concentrations in a nitrate‐limited chemostat. Journal of Phycology. 2014;50(2):243–53. doi: 10.1111/jpy.12156 26988182

38. Halsey KH, Jones BM. Phytoplankton strategies for photosynthetic energy allocation. Annual Review of Marine Science. 2015;7:265–97. doi: 10.1146/annurev-marine-010814-015813 25149563

39. Fisher NL, Halsey KH. Mechanisms that increase the growth efficiency of diatoms in low light. Photosynthesis Research. 2016;129(2):183–97. doi: 10.1007/s11120-016-0282-6 27312336

40. Morrissey J, Bowler C. Iron utilization in marine cyanobacteria and eukaryotic algae. Frontiers in microbiology. 2012;3:43. doi: 10.3389/fmicb.2012.00043 22408637

41. Nunn BL, Faux JF, Hippmann AA, Maldonado MT, Harvey HR, Goodlett DR, et al. Diatom proteomics reveals unique acclimation strategies to mitigate Fe limitation. PLoS One. 2013;8(10):e75653. doi: 10.1371/journal.pone.0075653 24146769

42. Hopkinson BM, Meile C, Shen C. Quantification of extracellular carbonic anhydrase activity in two marine diatoms and investigation of its role. Plant Physiology. 2013;162(2):1142–52. doi: 10.1104/pp.113.217737 23656892

43. Goldman JA, Bender ML, Morel FM. The effects of pH and pCO 2 on photosynthesis and respiration in the diatom Thalassiosira weissflogii. Photosynthesis research. 2017;132(1):83–93. doi: 10.1007/s11120-016-0330-2 28062941

44. Depauw FA, Rogato A, Ribera d’Alcalá M, Falciatore A. Exploring the molecular basis of responses to light in marine diatoms. Journal of Experimental Botany. 2012;63(4):1575–91. doi: 10.1093/jxb/ers005 22328904

45. Coesel S, Mangogna M, Ishikawa T, Heijde M, Rogato A, Finazzi G, et al. Diatom PtCPF1 is a new cryptochrome/photolyase family member with DNA repair and transcription regulation activity. EMBO reports. 2009;10(6):655–61. doi: 10.1038/embor.2009.59 19424294

46. Fortunato AE, Jaubert M, Enomoto G, Bouly J-P, Raniello R, Thaler M, et al. Diatom phytochromes reveal the existence of far-red light based sensing in the ocean. The Plant Cell. 2016:tpc. 00928.2015.

47. Takahashi F, Yamagata D, Ishikawa M, Fukamatsu Y, Ogura Y, Kasahara M, et al. AUREOCHROME, a photoreceptor required for photomorphogenesis in stramenopiles. Proceedings of the National Academy of Sciences. 2007;104(49):19625–30.

48. Huysman MJ, Vyverman W, De Veylder L. Molecular regulation of the diatom cell cycle. Journal of Experimental Botany. 2013;65(10):2573–84. doi: 10.1093/jxb/ert387 24277280

49. Annunziata R, Ritter A, Fortunato AE, Cheminant-Navarro S, Agier N, Huysman MJ, et al. A bHLH-PAS protein regulates light-dependent diurnal rhythmic processes in the marine diatom Phaeodactylum tricornutum. bioRxiv. 2018:271445.

50. Matthijs M, Fabris M, Obata T, Foubert I, Franco‐Zorrilla JM, Solano R, et al. The transcription factor bZIP14 regulates the TCA cycle in the diatom Phaeodactylum tricornutum. The EMBO journal. 2017;36(11):1559–76. doi: 10.15252/embj.201696392 28420744

51. Kroth PG, Chiovitti A, Gruber A, Martin-Jezequel V, Mock T, Parker MS, et al. A model for carbohydrate metabolism in the diatom Phaeodactylum tricornutum deduced from comparative whole genome analysis: Bibliothek der Universität Konstanz; 2008.

52. Rastogi A, Maheswari U, Dorrell RG, Maumus F, Vieira FRJ, Kustka A, et al. Integrative analysis of large scale transcriptome data draws a comprehensive landscape of Phaeodactylum tricornutum functional genome and evolutionary origin of diatoms. bioRxiv. 2017:176024.

Fe limitation decreases transcriptional regulation over the diel cycle in the model diatom Thalassiosira pseudonana

Souhrn

Klíčová slova:

Zdroje

PLOS One

Aktuální možnosti diagnostiky a léčby litiáz