Abstract
Diatoms are important contributors to global net primary productivity, and play a crucial role in the biogeochemical cycles of carbon, phosphorus, nitrogen, iron, and silicon. Currently in some regions in the ocean, there’s a trend that carbon content is high while oxygen concentration is low, and the underlying mechanisms of diatoms’ response to low oxygen environments are worth investigating. Phaeodactylum tricornutum is a model diatom whose genome has been sequenced; it provides a universal molecular toolbox and a stable transgenic expression system. Therefore, the study of the responses of P. tricornutum to low oxygen has not only fundamental research significance but also important ecological significance. In this study, growth rates were determined and proteomic analysis and metabolomic analysis were performed to examine P. tricornutum responses under different oxygen concentrations (2% oxygen concentration for hypoxic condition and 21% oxygen concentration for the normal condition (sterilized air)). Results show that the hypoxic environment inhibited the growth of P. tricornutum. In the hypoxic conditions, P. tricornutum could reset its metabolism pathways, including enhancement in lipid utilization, replenishment of tricarboxylic acid (TCA) cycle through the glyoxylic acid cycle, and down-regulation of photorespiration to reduce energy waste. Additionally, the stress resistance mechanism was activated to facilitate the adaptation to low oxygen conditions. This study helps to reveal the different metabolic changes to hypoxia of diatom from that of higher plants, which might be ascribed to their different habitats and needs further exploration in the future.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability Statement
The data that support the findings of this study are available from the corresponding author upon reasonable request.
References
Banti V, Giuntoli B, Gonzali S, Loreti E, Magneschi L, Novi G, Paparelli E, Parlanti S, Pucciariello C, Santaniello A, Perata P. 2013. Low oxygen response mechanisms in green organisms. International Journal of Molecular Sciences, 14(3): 4734–4761, https://doi.org/10.3390/ijms14034734.
Bowler C, Allen A E, Badger J H, Grimwood J, Jabbari K, Kuo A, Maheswari U, Martens C, Maumus F, Otillar R P, Rayko E, Salamov A, Vandepoele K, Beszteri B, Gruber A, Heijde M, Katinka M, Mock T, Valentin K, Verret F, Berges J A, Brownlee C, Cadoret J P, Chiovitti A, Choi C J, Coesel S, De Martino A, Detter J C, Durkin C, Falciatore A, Fournet J, Haruta M, Huysman M J J, Jenkins B D, Jiroutova K, Jorgensen R E, Joubert Y, Kaplan A, Kröger N, Kroth P G, La Roche J, Lindquist E, Lommer M, Martin-jézéquel V, Lopez P J, Lucas S, Mangogna M, Mcginnis K, Medlin L K, Montsant A, Secq M P O, Napoli C, Obornik M, Parker M S, Petit J L, Porcel B M, Poulsen N, Robison M, Rychlewski L, Rynearson T A, Schmutz J, Shapiro H, Siaut M, Stanley M, Sussman M R, Taylor A R, Vardi A, Von Dassow P, Vyverman W, Willis A, Wyrwicz L S, Rokhsar D S, Weissenbach J, Armbrust E V, Green B R, Van De Peer Y, Grigoriev I V. 2008. The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature, 456(7219): 239–244, https://doi.org/10.1038/nature07410.
Bradford M M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72(1–2): 248–254, https://doi.org/10.1016/0003-2697(76)90527-3.
Dambek M, Eilers U, Breitenbach J, Steiger S, Büchel C, Sandmann G. 2012. Biosynthesis of fucoxanthin and diadinoxanthin and function of initial pathway genes in Phaeodactylum tricornutum. Journal of Experimental Botany, 63(15): 5607–5612, https://doi.org/10.1093/jxb/ers211.
Eastmond P J, Germain V, Lange P R, Bryce J H, Smith S M, Graham I A. 2000. Postgerminative growth and lipid catabolism in oilseeds lacking the glyoxylate cycle. Proceedings of the National Academy of Sciences of the United States of America, 97(10): 5669–5674, https://doi.org/10.1073/pnas.97.10.5669.
Enriquez M M, LaFountain A M, Budarz J, Fuciman M, Gibson G N, Frank H A. 2010. Direct determination of the excited state energies of the xanthophylls diadinoxanthin and diatoxanthin from Phaeodactylum tricornutum. Chemical Physics Letters, 493(4–6): 353–357, https://doi.org/10.1016/j.cplett.2010.05.051.
Falkowski P G, Barber R T, Smetacek V. 1998. Biogeochemical controls and feedbacks on ocean primary production. Science, 281(5374): 200–206, https://doi.org/10.1126/science.281.5374.200.
Field C B, Behrenfeld M J, Randerson J T, Falkowski P. 1998. Primary production of the biosphere: integrating terrestrial and oceanic components. Science, 281(5374): 237–240, https://doi.org/10.1126/science.281.5374.237.
Gaffney D O, Jennings E Q, Anderson C C, Marentette J O, Shi T D, Oxvig A M S, Streeter M D, Johannsen M, Spiegel D A, Chapman E, Roede J R, Galligan J J. 2020. Non, enzymatic lysine lactoylation of glycolytic enzymes. Cell Chemical Biology, 27(2): 206–213.E6, https://doi.org/10.1016/j.chembiol.2019.11.005.
Geigenberger P. 2003. Response of plant metabolism to too little oxygen. Current Opinion in Plant Biology, 6(3): 247–256, https://doi.org/10.1016/s1369-5266(03)00038-4.
Grossman A R, Catalanotti C, Yang W Q, Dubini A, Magneschi L, Subramanian V, Posewitz M C, Seibert M. 2011. Multiple facets of anoxic metabolism and hydrogen production in the unicellular green alga Chlamydomonas reinhardtii. New Phytologist, 190(2): 279–288, https://doi.org/10.1111/j.1469-8137.2010.03534.x.
Guillard R R L. 1975. Culture of phytoplankton for feeding marine invertebrates. In: Smith W L, Chanley M H eds. Culture of Marine Invertebrate Animals. Springer, Boston. p.29–60, https://doi.org/10.1007/978-1-4615-8714-9_3.
Harrison P J, Waters R E, Taylor F J R. 1980. A broad spectrum artificial sea water medium for coastal and open ocean phytoplankton. Journal of Phycology, 16(1): 28–35, https://doi.org/10.1111/j.0022-3646.1980.00028.x.
Jiang Y L, Wang X P, Sun H, Han S J, Li W F, Cui N, Lin G M Zhang J Y, Cheng W, Cao D D, Zhang Z Y, Zhang C C, Chen Y X, Zhou C Z. 2018. Coordinating carbon and nitrogen metabolic signaling through the cyanobacterial global repressor NdhR. Proceedings of the National Academy of Sciences of the United States of America, 115(2): 403–408, https://doi.org/10.1073/pnas.1716062115.
Khangaonkar T, Nugraha A, Premathilake L, Keister J, Borde A. 2021. Projections of algae, eelgrass, and zooplankton ecological interactions in the inner Salish Sea-for future climate, and altered oceanic states. Ecological Modelling, 441: 109420, https://doi.org/10.1016/j.ecolmodel.2020.109420.
Kreuzwieser J, Hauberg J, Howell K A, Carroll A, Rennenberg H, Millar A H, Whelan J. 2009. Differential response of gray poplar leaves and roots underpins stress adaptation during hypoxia. Plant Physiology, 149(1): 461–473, https://doi.org/10.1104/pp.108.125989.
Kroth P. 2007. Molecular biology and the biotechnological potential of diatoms. In: León R, Galván A, Fernández E eds. Transgenic Microalgae as Green Cell Factories. Springer, New York. p.23–33, https://doi.org/10.1007/978-0-387-75532-8_3.
Liu J H, Wang W, Wu H, Gong X Q, Moriguchi T. 2015. Polyamines function in stress tolerance: from synthesis to regulation. Frontiers in Plant Science, 6: 827, https://doi.org/10.3389/fpls.2015.00827.
Moellering R E, Cravatt B F. 2013. Functional lysine modification by an intrinsically reactive primary glycolytic metabolite. Science, 341(6145): 549–553, https://doi.org/10.1126/science.1238327.
Mustroph A, Lee S C, Oosumi T, Zanetti M E, Yang H J, Ma K, Yaghoubi-Masihi A, Fukao T, Bailey-Serres J. 2010. Cross-kingdom comparison of transcriptomic adjustments to low-oxygen stress highlights conserved and plant, specific responses. Plant Physiology, 152(3): 1484–1500, https://doi.org/10.1104/pp.109.151845.
Owens T G, Wold E R. 1986. Light-harvesting function in the diatom Phaeodactylum tricornutum. I. Isolation and characterization of pigment-protein complexes. Plant Physiology, 80(3): 732–738, https://doi.org/10.1104/pp.80.3.732.
Papagiannakis E, Van Stokkum I H M, Fey H, Büchel C, Van Grondelle R. 2005. Spectroscopic characterization of the excitation energy transfer in the fucoxanthin-chlorophyll protein of diatoms. Photosynthesis Research, 86(1): 241–250, https://doi.org/10.1007/s11120-005-1003-8.
Pucciariello C, Parlanti S, Banti V, Novi G, Perata P. 2012. Reactive oxygen species-driven transcription in Arabidopsis under oxygen deprivation. Plant Physiology, 159(1): 184–196, https://doi.org/10.1104/pp.111.191122.
Rivoal J, Ricard B, Pradet A. 1991. Lactate dehydrogenase in Oryza sativa l. Seedlings and roots: identification and partial characterization. Plant Physiology, 95(3): 682–686, https://doi.org/10.1104/pp.95.3.682.
Rushforth S R, Johansen J R, Sorensen D L. 1988. Occurrence of Phaedactylum tricornutum in the Great Salt Lake-Utah, USA. Great Basin Naturalist, 48(3): 324–326-
Slocum R D. 2005. Genes, enzymes and regulation of arginine biosynthesis in plants. Plant Physiology and Biochemistry, 43(8): 729–745, https://doi.org/10.1016/j.plaphy.2005.06.007.
Solaini G, Baracca A, Lenaz G, Sgarbi G. 2010. Hypoxia and mitochondrial oxidative metabolism. Biochimica et Biophysica Acta (BBA)-Bioenergetics, 1797(6–7): 1171–1177, https://doi.org/10.1016/j.bbabio.2010.02.011.
Sweetlove L J, Dunford R, Ratcliffe R G, Kruger N J. 2000. Lactate metabolism in potato tubers deficient in lactate dehydrogenase activity. Plant, Cell & Environment, 23(8): 873–881, https://doi.org/10.1046/j.1365-3040.2000.00605.x.
Thayer S S, Björkman O. 1990. Leaf xanthophyll content and composition in sun and shade determined by HPLC. Photosynthesis Research, 23(3): 331–343, https://doi.org/10.1007/bf00034864.
Winter G, Todd C D, Trovato M, Forlani G, Funck D. 2015. Physiological implications of arginine metabolism in plants. Frontiers in Plant Science, 6: 534, https://doi.org/10.3389/fpls.2015.00534.
Wiśniewski J R, Zougman A, Nagaraj N, Mann M. 2009. Universal sample preparation method for proteome analysis. Nature methods, 6(5): 359–362, https://doi.org/10.1038/nmeth.1322.
Yang L Q, Zhang Y Y. 2020. Effects of atrazine and its two major derivatives on the photosynthetic physiology and carbon sequestration potential of a marine diatom. Ecotoxicology and Environmental Safety, 205: 111359, https://doi.org/10.1016/j.ecoenv.2020.111359.
Zhang C C, Zhou C Z, Burnap R L, Peng L. 2018. Carbon/nitrogen metabolic balance: lessons from Cyanobacteria. Trends in Plant Science, 23(12): 1116–1130, https://doi.org/10.1016/j.tplants.2018.09.008.
Zhao P P, Gu W H, Huang A Y, Wu S C, Liu C H, Huan L, Gao S, Xie X J, Wang G C. 2018. Effect of iron on the growth of Phaeodactylum tricornutum via photosynthesis. Journal of Phycology, 54(1): 34–43, https://doi.org/10.1111/jpy.12607.
Zhao P P, Gu W H, Wu S C, Huang A Y, He L W, Xie X J, Gao S, Zhang B Y, Niu J F, Lin A P, Wang G C. 2014. Silicon enhances the growth of Phaeodactylum tricornutum Bohlin under green light and low temperature. Scientific Reports, 4: 3958, https://doi.org/10.1038/srep03958.
Author information
Authors and Affiliations
Corresponding author
Additional information
Supported by the National Natural Science Foundation of China (Nos. 41876158, 31770024), the Natural Science Foundation of Hainan Province (No. 420QN219), the Biology and Biochemistry ESI Cultivation Discipline Open Project of Qilu University of Technology (No. ESIBBC202004), the Innovation and Development Joint Fund of Natural Science Foundation from Shandong Province (No. ZR2021LSW022), the Young Taishan Scholarship to Xuekui XIA (No. tsqn202103100), and the Start-up Fund Project of Hainan University (No. KYQD(ZR)20060)
Electronic supplementary material
Rights and permissions
About this article
Cite this article
Zhao, P., Wu, Q., Xia, X. et al. Metabolomic and proteomic responses of Phaeodactylum tricornutum to hypoxia. J. Ocean. Limnol. 40, 1963–1973 (2022). https://doi.org/10.1007/s00343-021-1232-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00343-021-1232-5