New Molecular Insights on the Response of the Green Alga Tetraselmis Suecica to Nitrogen Starvation

Overview

Journal Sci Rep

Specialty Science

Date 2019 Mar 6

PMID 30833632

Citations 23

Authors

Chiara Lauritano

Daniele De Luca

Mariano Amoroso

Salvatore Benfatto

Simone Maestri

Claudia Racioppi

Francesco Esposito

Adrianna Ianora

Affiliations

Soon will be listed here.

Abstract

Microalgae are currently considered one of the most promising resources for biofuel production, aquaculture feedstock and new pharmaceuticals. Among them, green algae of the genus Tetraselmis are extensively studied for their lipid accumulation in nutrient-starvation conditions. In this paper, we present the full-transcriptome of Tetraselmis suecica and differential expression analysis between nitrogen-starved and -repleted conditions (at stationary phase) focusing not only on lipid metabolism but giving new insights on nutrient starvation responses. Transcripts involved in signal transduction pathways, stress and antioxidant responses and solute transport were strongly up-regulated when T. suecica was cultured under nitrogen starvation. On the contrary, transcripts involved in amino acid synthesis, degradation of sugars, secondary metabolite synthesis, as well as photosynthetic activity were down-regulated under the same conditions. Among differentially expressed transcripts, a polyketide synthase and three lipoxygenases (involved in the synthesis of secondary metabolites with antipredator, anticancer and anti-infective activities) were identified, suggesting the potential synthesis of bioactive compounds by this microalga. In addition, the transcript for a putative nitrilase, enzyme used in nitrile bioremediation, is here reported for the first time for T. suecica. These findings give new insights on T. suecica responses to nutrient starvation and on possible biotechnological applications for green algae.

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References

Grabherr M, Haas B, Yassour M, Levin J, Thompson D, Amit I . Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol. 2011; 29(7):644-52. PMC: 3571712. DOI: 10.1038/nbt.1883. View

Zhao L, Li K, Wang Q, Song X, Su H, Xie B . Nitrogen Starvation Impacts the Photosynthetic Performance of Porphyridium cruentum as Revealed by Chlorophyll a Fluorescence. Sci Rep. 2017; 7(1):8542. PMC: 5561210. DOI: 10.1038/s41598-017-08428-6. View

Pruneda-Paz J, Kay S . An expanding universe of circadian networks in higher plants. Trends Plant Sci. 2010; 15(5):259-65. PMC: 2866796. DOI: 10.1016/j.tplants.2010.03.003. View

Bartels S, Gonzalez Besteiro M, Lang D, Ulm R . Emerging functions for plant MAP kinase phosphatases. Trends Plant Sci. 2010; 15(6):322-9. DOI: 10.1016/j.tplants.2010.04.003. View

Kohut G, Adam A, Fazekas B, Hornok L . N-starvation stress induced FUM gene expression and fumonisin production is mediated via the HOG-type MAPK pathway in Fusarium proliferatum. Int J Food Microbiol. 2009; 130(1):65-9. DOI: 10.1016/j.ijfoodmicro.2009.01.002. View

Caplan J, Mamillapalli P, Burch-Smith T, Czymmek K, Dinesh-Kumar S . Chloroplastic protein NRIP1 mediates innate immune receptor recognition of a viral effector. Cell. 2008; 132(3):449-62. PMC: 2267721. DOI: 10.1016/j.cell.2007.12.031. View

Simionato D, Block M, La Rocca N, Jouhet J, Marechal E, Finazzi G . The response of Nannochloropsis gaditana to nitrogen starvation includes de novo biosynthesis of triacylglycerols, a decrease of chloroplast galactolipids, and reorganization of the photosynthetic apparatus. Eukaryot Cell. 2013; 12(5):665-76. PMC: 3647774. DOI: 10.1128/EC.00363-12. View

Kobayashi J . Amphidinolides and its related macrolides from marine dinoflagellates. J Antibiot (Tokyo). 2008; 61(5):271-84. DOI: 10.1038/ja.2008.39. View

Shelest E, Heimerl N, Fichtner M, Sasso S . Multimodular type I polyketide synthases in algae evolve by module duplications and displacement of AT domains in trans. BMC Genomics. 2015; 16:1015. PMC: 4661987. DOI: 10.1186/s12864-015-2222-9. View

10.

Gonzalez A, Ruiz A, Serrano R, Arino J, Casamayor A . Transcriptional profiling of the protein phosphatase 2C family in yeast provides insights into the unique functional roles of Ptc1. J Biol Chem. 2006; 281(46):35057-69. DOI: 10.1074/jbc.M607919200. View

11.

Zhang Y, Chen H, He C, Wang Q . Nitrogen starvation induced oxidative stress in an oil-producing green alga Chlorella sorokiniana C3. PLoS One. 2013; 8(7):e69225. PMC: 3712941. DOI: 10.1371/journal.pone.0069225. View

12.

Wase N, Black P, Stanley B, DiRusso C . Integrated quantitative analysis of nitrogen stress response in Chlamydomonas reinhardtii using metabolite and protein profiling. J Proteome Res. 2014; 13(3):1373-96. DOI: 10.1021/pr400952z. View

13.

Andersen C, Jensen J, Orntoft T . Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res. 2004; 64(15):5245-50. DOI: 10.1158/0008-5472.CAN-04-0496. View

14.

Pfaffl M, Horgan G, Dempfle L . Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 2002; 30(9):e36. PMC: 113859. DOI: 10.1093/nar/30.9.e36. View

15.

Cook J, Bardwell L, Thorner J . Inhibitory and activating functions for MAPK Kss1 in the S. cerevisiae filamentous-growth signalling pathway. Nature. 1997; 390(6655):85-8. DOI: 10.1038/36355. View

16.

LARKIN M, Blackshields G, Brown N, Chenna R, McGettigan P, McWilliam H . Clustal W and Clustal X version 2.0. Bioinformatics. 2007; 23(21):2947-8. DOI: 10.1093/bioinformatics/btm404. View

17.

Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A . Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002; 3(7):RESEARCH0034. PMC: 126239. DOI: 10.1186/gb-2002-3-7-research0034. View

18.

Sansone C, Galasso C, Orefice I, Nuzzo G, Luongo E, Cutignano A . The green microalga Tetraselmis suecica reduces oxidative stress and induces repairing mechanisms in human cells. Sci Rep. 2017; 7:41215. PMC: 5259714. DOI: 10.1038/srep41215. View

19.

Rodriguez P . Protein phosphatase 2C (PP2C) function in higher plants. Plant Mol Biol. 1998; 38(6):919-27. DOI: 10.1023/a:1006054607850. View

20.

Brandao P, Bull A . Nitrile hydrolysing activities of deep-sea and terrestrial mycolate actinomycetes. Antonie Van Leeuwenhoek. 2003; 84(2):89-98. DOI: 10.1023/a:1025409818275. View