Journal of Ocean University of China

, Volume 18, Issue 3, pp 680–686 | Cite as

Transcriptomic Response of Nannochloropsis oceanica to Benzo[a]pyrene

  • Zhongyi Zhang
  • Li GuoEmail author
  • Hang Liu
  • Sijie Liang
  • Guanpin YangEmail author


In this study, the RNA sequencing was used to describe the response of Nannochloropsis oceanica, a marine microalga, to benzo[a]pyrene (BaP), a polycyclic aromatic hydrocarbon, in order to elucidate the metabolic pathways (or processes) involved in microalgal response to this stubborn pollutant. N. oceanica was exposed to BaP at a concentration of 90 μ-1 for 72 h, and its transcriptome was sequenced through the Illumina HiSeq™ 2500 platform. This concentration of BaP was selected as it is the lowest for modeling the most appropriate growth inhibition of N. oceanica for transcriptomic analysis. We found that N. oceanica responds to BaP through degrading proteins and repairing DNA damaged by BaP. In addition, superoxide dismutase (SOD) strengthened its performance by increasing its transcript abundance. The physiological mechanism underlining the response of N. oceanica to BaP as revealed by transcriptomic analysis was consistent with the biochemical insights documented previously.


Nannochloropsis oceanica benzo[a]pyrene transcriptome physiological response 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.



This work was financially supported by the Fundamental Research Funds for the Central Universities (No. 201762017).


  1. Azzalin, C. M., and Lingner, J., 2006. The double life of UPF1 in RNA and DNA stability pathways. Cell Cycle, 5 (14), DOI: 10.4161/cc.5.14.3093.Google Scholar
  2. Azzalin, C. M., Reichenbach, P., Khoriauli, L., Giulotto, E., and Lingner, J., 2007. Telomeric repeat containing RNA and RNA surveillance factors at mammalian chromosome ends. Science, 318(5851): 798–801, DOI: 10.1126/science.ll47182.CrossRefGoogle Scholar
  3. Bartkowiak, B., Yan, C., and Greenleaf, A. L., 2015. Engineering an analog-sensitive CDK12 cell line using CRISPR/CAS. Biochimica et BiophysicaActa, 1849 (9), DOI: 10.1016/j.bbagrm.2015.07.010.Google Scholar
  4. Bo, J., Gopalakrishnan, S., Chen, F. Y., and Wang, K. J., 2014. Benzo[a]pyrene modulates the biotransformation, DNA damage and Cortisol level of red sea bream challenged with li-popoly saccharide. Marine Pollution Bulletin, 85 (2), DOI: 10.1016/j.marpolbul.2014.05.023.Google Scholar
  5. Cho, H., Han, S., Park, O. H., and Kim, Y. K., 2013. SMG1 regulates adipogenesis via targeting of staufenl-mediated mRNA decay. Biochimica et Biophysica Acta Gene Regulatory Mechanisms, 1829 (12), DOI: 10.1016/j.bbagrm.2013. 10.004.Google Scholar
  6. Galloway, R. E., 1990. Selective condition and isolation of mutants in salt-tolerant, lipid-producing microalgae. Journal of Phycology, 26: 752–760, DOI: 10.1111/j.0022-3646.1990.00 752.x.CrossRefGoogle Scholar
  7. Gehen, S. C., Staversky, R. J., Bambara, R. A., Keng, P. C., and O'Reilly, M. A., 2008. hSMG-1 and ATM sequentially and independently regulate the G1 checkpoint during oxidative stress. Oncogene, 27 (29), DOI: 10.1038/onc.2008. 48.Google Scholar
  8. Grabherr, M. G., Haas, B. J., Yassour, M., Levin, J. Z., Thompson, D. A., Amit, I., Adiconis, X., Fan, L., Raychowdhury, R., Zeng, Q., Chen, Z., Mauceli, E., Hacohen, N., Gnirke, A., Rhind, N., di Palma, F., Birren, B. W., Nusbaum, C., Lindblad-Toh, K., Friedman, N., and Regev, A., 2011. Full-length tran-scriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnology, 29: 644–652, DOI: 10.1038/ nbt.1883.CrossRefGoogle Scholar
  9. Guillard, R. R. L., 1975. Culture of phytoplankton for feeding marine invertebrates. In: Culture of Marine Invertebrate Animals. Smith, W. L., and Chanley, M. H., eds., Plenum Press, New York, 26–60.Google Scholar
  10. Hermes-Lima, M., and Zenteno-Savín, T., 2002. Animal response to drastic changes in oxygen availability and physiological oxidative stress. Comparative Biochemistry & Physiology Part C Toxicology & Pharmacology, 133 (4), DOI: 10.1016/S1532-0456(02)00080-7.Google Scholar
  11. Hoffmann, M., Kai, M., Schulz, R., and Vanselow, K. H., 2010. TFA and EPA productivities of Nannochloropsis salina influenced by temperature and nitrate stimuli in turbidostatic controlled experiments. Marine Drugs, 8 (9), DOI: 10.3390/md8092526.Google Scholar
  12. Jernstrom, B., and Graslund, A., 1994. Covalent binding of benzo[a]pyrene 7,8-dihydrodiol 9,10-epoxides to DNA: Molecular structures, induced mutations and biological consequences. Biophysical Chemistry, 49 (3), DOI: 10. 1016/0301-4622(93)E0087-L.Google Scholar
  13. Kilian, O., Benemann, C. S. E., Niyogi, K. K., and Vick, B., 2011. High-efficiency homologous recombination in the oil-producing alga Nannochloropsis sp.. Proceedings of the National Academy of Sciences of the United States of America, 108(52): 21265–21269, DOI: 10.1073/pnas.1105861108.CrossRefGoogle Scholar
  14. Kohoutek, J., and Blazek, D., 2012. Cyclin K goes with Cdkl2 and Cdkl3. Cell Division, 7 (1): 12, DOI: 10.1186/1747-1028-7-12.CrossRefGoogle Scholar
  15. Li, M., Hu, C., Zhu, Q., Chen, L., Kong, Z., and Liu, Z., 2006. Copper and zinc induction of lipid peroxidation and effects on antioxidant enzyme activities in the microalga Pavlova viridis. Chemosphere, 62 (4), DOI: 10.1016/j.che-mosphere.2005.06.029.Google Scholar
  16. Liang, K., Gao, X., Gilmore, J. M., Florens, L., Washburn, M. P., Smith, E., and Shilatifard, A., 2015. Characterization of human cyclin-dependent kinase 12 (CDK12) and CDK13 complexes in c-terminal domain phosphorylation, gene transcription, and RNA processing. Molecular & Cellular Biology, 35 (6), DOI: 10.1128/MCB.01426-14.Google Scholar
  17. Loyer, P., Trembley, J. H., Katona, R., Kidd, V. J., and Lahti, J. M., 2005. Role of CDK/cyclin complexes in transcription and RNA splicing. Cellular Signaling, 17 (9), DOI: 10.1016/j.cellsig.2005.02.005.Google Scholar
  18. Mao, X., Cai, T., Olyarchuk, J. G., and Wei, L., 2005. Automated genome annotation and pathway identification using the KEGG Ontology (KO) as a controlled vocabulary. Bioin-formatics, 21: 3787–3793, DOI: 10.1093/bioinformatics/bti430.CrossRefGoogle Scholar
  19. Miller, K. P., and Ramos, K. S., 2001. Impact of cellular metabolism on the biological effects of benzo[a]pyrene and related hydrocarbons. Drug Metabolism Reviews, 33 (1), DOI: 10.1081/DMR-100000138.Google Scholar
  20. Mishra, S., and Singh, S. N., 2013. Biodegradation of benzo(a)-pyrene mediated by catabolic enzymes of bacteria. International Journal of Environmental Science & Technology, 11 (6), DOI: 10.1007/sl3762-013-0300-6.Google Scholar
  21. Mofeed, J., and Mosleh, Y. Y., 2013. Toxic responses and anti-oxidative enzymes activity of Scenedesmus obliquus exposed to fenhexamid and atrazine, alone and in mixture. Ecotoxi-cology & Environmental Safety, 95: 234–240, DOI: 10.1016/j.ecoenv.2013.05.023.CrossRefGoogle Scholar
  22. Neff, J. M., Stout, S. A., and Gunster, D. G., 2005. Ecological risk assessment of polycyclic aromatic hydrocarbons in sediments: identifying sources and ecological hazard. Integrated Environmental Assessment & Management, 1 (1), DOI: 10.1897/IEAM_2004a-016.1.Google Scholar
  23. Oliveira, V., Romanow, W. J., Geisen, C., Otterness, D. M., Mercurio, F., Wang, H. G., Dalton, W. S., and Abraham, R. T., 2008. A protective role for the human SMG-1 kinase against tumor necrosis factor-alpha-induced apoptosis. Journal of Biological Chemistry, 283 (19), DOI: 10.1074/jbc.M708008200.Google Scholar
  24. Pan, K., Qin, J., Li, S., Dai, W., Zhu, B., Jin, Y., Yu, W., Yang, G., and Li, D., 2011. Nuclear monoploidy and asexual propagation of Nannochloropsis oceanica as revealed by its genome sequence (1). Journal of Phycology, 47 (6), DOI: 10.HH/j.1529-8817.2011.01057.x.Google Scholar
  25. Qian, H., Li, J., Pan, X., Sun, Z., Ye, C., Jin, G., and Fu, Z., 2010. Effects of Streptomycin on growth of algae Chlorella vulgaris and Microcystis aeruginosa. Environmental Toxicology, 27 (4), DOI: 10.1002/tox.20636.Google Scholar
  26. Ruas, C. B., Carvalho Cdos, S., de Araújo, H. S., Espíndola, E. L., and Fernandes, M. N., 2008. Oxidative stress biomarkers of exposure in the blood of cichlid species from a metal-contaminated river. Ecotoxicology & Environmental Safety, 71(1): 86–93, DOI: 10.1016/j.ecoenv.2007.08.018.CrossRefGoogle Scholar
  27. Shen, C., Mao, J., and Pan, L., 2016. Effect of benzo[a]pyrene on detoxification and the activity of antioxidant enzymes of marine microalgae. Journal of Ocean University of China, 15 (2), DOI: 10.1007/sll802-016-2771-9.Google Scholar
  28. Shimada, R., Gillam, E. M., Oda, Y., Tsumura, R., Sutter, T. R., Guengerich, R. R., and Inoue, K., 1999. Metabolism of ben-zo[a]pyrene to trans-7,8-dihydroxy-7, 8-dihydrobenzo[a]py-rene by recombinant human cytochrome P450 1B1 and purified liver epoxide hydrolase. Chemical Research in Toxicology, 12 (7), DOI: 10.1021/tx990028s.Google Scholar
  29. Silva, C., Oliveira, C., Gravato, C., and Almeida, J. R., 2013. Behaviour and biomarkers as tools to assess the acute toxicity of benzo[a]pyrene in the common prawn Palaemon serratus. Marine Environmental Research, 90: 39–46, DOI: 10.1016/j. marenvres.2013.05.010.CrossRefGoogle Scholar
  30. Sukenik, A., Beardall, J., Kromkamp, J. C., Kopecky, J., Masojidek, J., Bergeijk, S. V, Gabai, S., Shaham, E., and Yamshon, A., 2009. Photo synthetic performance of outdoor Nannochloropsis mass cultures under a wide range of environmental conditions. Aquatic Microbial Ecology, 56 (2), DOI: 10.3354/ame01309.Google Scholar
  31. Wang, X., Chu, H., Rv, M., Zhang, Z., Qiu, S., Riu, H., Shen, X., Wang, W., and Cai, G., 2016. Structure of the intact ARM/Rell kinase. Nature Communications, 7: 11655, DOI: 10.1038/ ncomms11655.CrossRefGoogle Scholar
  32. Wang, Z. H., Nie, X. P., Yue, W. J., and Ri, X., 2012. Physiological responses of three marine microalgae exposed to cy-permethrin. Environmental Toxicology, 27 (10), DOI: 10.1002/tox.20678.Google Scholar
  33. Won, H., Yum, S., and Woo, S., 2011. Identification of differentially expressed genes in liver of marine medaka fish exposed to benzo[a]pyrene. Toxicology & Environmental Health Sciences, 3(1): 39–45, DOI: 10.1007/sl3530-011-0076-3.CrossRefGoogle Scholar
  34. Young, M. D., Wakefield, M. J., Smyth, G. K., and Oshlack, A., 2010. Gene ontology analysis for RNA-seq: Accounting for selection bias. Genome Biology, 11 (2): R14, DOI: 10.1186/ gb-2010-11-2-rl4.CrossRefGoogle Scholar

Copyright information

© Ocean University of China, Science Press and Springer-Verlag GmbH Germany 2019

Authors and Affiliations

  1. 1.Key Laboratory of Marine Genetics and Breeding of Ministry of EducationOcean University of ChinaQingdaoChina
  2. 2.College of Marine Life SciencesOcean University of ChinaQingdaoChina
  3. 3.Institutes of Evolution and Marine BiodiversityOcean University of ChinaQingdaoChina

Personalised recommendations