Advertisement

Domestication of marine microalga Nannochloropsis oceanica to freshwater medium and the physiological responses

  • Li Guo
  • Sijie Liang
  • Zhongyi Zhang
  • Hang Liu
  • Songwen WangEmail author
  • Guanpin YangEmail author
Article

Abstract

Marine microalga Nannochl oropsis oceanica LAMB0001 were domesticated (~730 generations, ~two days each) to adapt freshwater BG11 medium. A number of freshwater medium adapted colonyderived strains were obtained. The strains were verifi ed phylogenetically to be N. oceanica LAMB0001 based on the 18S ribosomal RNA gene. Freshwater-medium adapted strain (FA1) grew faster in the BG11 medium prepared with freshwater than wild-type N. oceanica grew in f/2 medium prepared with seawater. We assumed that (1) the expression patterns of the genes that expressed diff erentially between FA1 and the wild-type N. oceanica exposing to the BG11 medium (WT-F) have been reprogrammed; (2) the physiological processes in which these genes involved have been modifi ed; and (3) a Gene Ontology (GO) term or a KEGG pathway enriched by DEGs between FA1 and WT-F has been up- or down-regulated if it was enriched simultaneously by up- or down-regulated DEGs between FA1 and WT-F, respectively. Under these assumptions, we found that FA1 reprogrammed the expression patterns of a set of genes that involved in cell adhesion, membrane and membrane integrity, material transportation, cell movement, and cellular signaling network. These changes in cellular functions and metabolic pathways indicate that the microalga modifi ed its gene expression pattern in a wide function range and at a high regulation rank in order to adapt to the freshwater medium. It is feasible to domesticate marine microalgae to a freshwater habitat, which may aid to modify their cultivation performances.

Key word

Nannochloropsis oceanica domestication acclimation adaptation genetic variation 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Supplementary material

343_2019_8202_MOESM1_ESM.pdf (238 kb)
Supplementary material, approximately 239 KB.

References

  1. Alverson A J. 2007. Strong purifying selection in the silicon transporters of marine and freshwater diatoms. Limnology and Oceanography, 52 (4): 1 420–1 429.CrossRefGoogle Scholar
  2. Anders S, Huber W. 2010. Differential expression analysis for sequence count data. Genome Biol ogy, 11: R106.Google Scholar
  3. Benjamini Y, Yekutieli D. 2001. The control of the false discovery rate in multiple testing under dependency. The Annals of Statistics, 29 (4): 1 165–1 188.CrossRefGoogle Scholar
  4. Chen K, Li E C, Li T Y, Xu C, Wang X D, Lin H Z, Qin J G, Chen L Q. 2015. Transcriptome and molecular pathway analysis of the hepatopancreas in the Pacific white shrimp Litopenaeus vannamei under chronic low–salinity stress. PLoS One, 10 (7): e0131503.CrossRefGoogle Scholar
  5. Crevillén P, Yang H C, Cui X, Greeff C, Trick M, Qiu Q, Cao X F, Dean C. 2014. Epigenetic reprogramming that prevents transgenerational inheritance of the vernalized state. Nature, 515 (7528): 587–590.CrossRefGoogle Scholar
  6. Fawley K P, Fawley M W. 2007. Observations on the diversity and ecology of freshwater Nannochloropsis (Eustigmatophyceae), with descriptions of new taxa. Protist, 158 (3): 325–336.CrossRefGoogle Scholar
  7. Galloway R E. 1990. Selective conditions and isolation of mutants in salt–tolerant, lipid–producing microalgae. Journal of Phycology, 26 (4): 752–260.CrossRefGoogle Scholar
  8. Gee C W, Niyogi K K. 2017. The carbonic anhydrase CAH1 is an essential component of the carbon–concentrating mechanism in Nannochloropsis oceanica. Proceedings of the National Academy of Sciences of the United States of America, 114 (17): 4 537–4 542.CrossRefGoogle Scholar
  9. Guillard R R L, Ryther J H. 1962. Studies of marine planktonic diatoms: I. Cyclotella nana Hustedt, and Detonula confervace a (Cleve) gran. Canadian Journal of Microbiology, 8 (2): 229–239.CrossRefGoogle Scholar
  10. 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. Plenum Press, New York. p.29–60.Google Scholar
  11. Huang W C, Hu H H. 2013. Study on the salinity tolerance and oil accumulation in Nannochloropsis. Acta Hydrobiologica Sinica, 37 (2): 383–387. (in Chinese)Google Scholar
  12. Ji H T, Pardo J M, Batelli G, Van Oosten M J, Bressan R A, Li X. 2013. The Salt Overly Sensitive (SOS) pathway: established and emerging roles. Mol ecular Plant, 6 (2): 275–286.CrossRefGoogle Scholar
  13. Kilian O, Benemann C S E, Niyogi K K, Vick B. 2011. Highefficiency homologous recombination in the oil–producing alga Nannochloropsis sp. Proceedings of the National Academy of Sciences of the United States of America, 108 (52): 21 265–21 269.CrossRefGoogle Scholar
  14. Kim D, Langmead B, Salzberg S L. 2015. HISAT: a fast spliced aligner with low memory requirements. Nature Methods, 12 (4): 357–360.CrossRefGoogle Scholar
  15. Kouzarides T. 2007. Chromatin modifications and their function. Cell, 128 (4): 693–705.CrossRefGoogle Scholar
  16. Larkin M A, Blackshields G, Brown N P, Chenna R, McGettigan P A, McWilliam H, Valentin F, Wallace I M, Wilm A, Lopez R, Thompson J D, Gibson T J, Higgins D G. 2007. Clustal W and Clustal X version 2.0. Bioinformatics, 23 (21): 2 947–2 948.CrossRefGoogle Scholar
  17. Liang C W, Cao S N, Zhang X W, Zhu B H, Su Z L, Xu D, Guang X Y, Ye N H. 2013. De novo sequencing and global transcriptome analysis of Nannochloropsis sp. (Eustigmatophyceae) following nitrogen starvation. BioEnergy Research, 6 (2): 494–505.CrossRefGoogle Scholar
  18. Liu S K, Wang X L, Sun F Y, Zhang J R, Feng J B, Liu H, Rajendran K V, Sun L Y, Zhang Y, Jiang Y L, Peatman E, Kaltenboeck L, Kucuktas H, Liu Z J. 2013. RNA–Seq reveals expression signatures of genes involved in oxygen transport, protein synthesis, folding, and degradation in response to heat stress in catfish. Physiol ogical Genomics, 45 (12): 462–476.CrossRefGoogle Scholar
  19. Lohbeck K T, Riebesell U, Reusch T B H. 2014. Gene expression changes in the coccolithophore Emiliania huxleyi after 500 generations of selection to ocean acidification. Proceedings of the Royal Society B: Biological Sciences, 281 (1786): 20140003.CrossRefGoogle Scholar
  20. Mao X Z, Cai T, Olyarchuk J G, Wei L P. 2005. Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary. Bioinformatics, 21 (19): 3 787–3 793.CrossRefGoogle Scholar
  21. Marschner H. 1995. Mineral Nutrition of Higher Plants. Academic Preßs, London.Google Scholar
  22. Mastrobuoni G, Irgang S, Pietzke M, Aßmus H E, Wenzel M, Schulze W X, Kempa S. 2012. Proteome dynamics and early salt stress response of the photosynthetic organism Chlamydomonas reinhardtii. BMC Genomics, 13: 215.Google Scholar
  23. Pan K H, Qin J J, Li S, Dai W K, Zhu B H, Jin Y C, Yu W G, Yang G P, Li D F. 2011. Nuclear monoploidy and asexual propagation of Nannochloropsis oceanica (Eustigmatophyceae) as revealed by its genome sequence. Journal of Phycology, 47 (6): 1 425–1 432.CrossRefGoogle Scholar
  24. Pedersen S F, Hoffmann E K, Mills J W: 2001. The cytoskeleton and cell volume regulation. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 130 (3): 385–399.CrossRefGoogle Scholar
  25. Perrineau M M, Zelzion E, Gross J, Price D C, Boyd J, Bhattacharya D. 2014. Evolution of salt tolerance in a laboratory reared population of Chlamydomonas reinhardtii. Environmental Microbiology, 16 (6): 1 755–1 766.CrossRefGoogle Scholar
  26. Posada D. 2008. jModelTest: phylogenetic model averaging. Molecular Biology and Evolution, 25 (7): 1 253–1 256.CrossRefGoogle Scholar
  27. Ronquist F, Teslenko M, van der Mark P, Ayres D L, Darling A, Höhna S, Larget B, Liu L, Suchard M A, Huelsenbeck J P. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biol ogy, 61 (3): 539–542.CrossRefGoogle Scholar
  28. Rozema J, Schat H. 2013. Salt tolerance of halophytes, research questions reviewed in the perspective of saline agriculture. Environmental and Experimental Botany, 92: 83–95.CrossRefGoogle Scholar
  29. Sawan C, Herceg Z. 2010. Histone modifications and cancer. Advances in Genetics, 70: 57–85.CrossRefGoogle Scholar
  30. Stanier R Y, Kunisawa R, Mandel M, Cohen–Bazire G. 1971. Purification and properties of unicellular blue–green algae (order Chroococcales). Bacteriological Reviews, 35 (2): 171–205.Google Scholar
  31. Sudhir P, Murthy S D S. 2004. Effects of salt stress on basic processes of photosynthesis. Photosynthetica, 42 (4): 481–486.CrossRefGoogle Scholar
  32. Sunday J M, Calosi P, Dupont S, Munday P L, Stillman J H, Reusch T B H. 2014. Evolution in an acidifying ocean. Trends in Ecology & Evolution, 29 (2): 117–125.CrossRefGoogle Scholar
  33. Trievel R C, Beach B M, Dirk L M A, Houtz R L, Hurley J H. 2002. Structure and catalytic mechanism of a SET domain protein methyltransferase. Cell, 111 (1): 91–103.CrossRefGoogle Scholar
  34. Vieler A, Wu G X, Tsai C H, Bullard B, Cornish A J, Harvey C, Reca I B, Thornburg C, Achawanantakun R, Buehl C J, Campbell M S, Cavalier D, Childs K L, Clark T J, Deshpande R, Erickson E, Armenia Ferguson A, Handee W, Kong Q, Li XB, Liu B S, Lundback S, Peng C, Roston R L, Sanjaya, Simpson J P, TerBush A, Warakanont J, Zäuner S, Farre E M, Hegg E L, Jiang N, Kuo M H, Lu Y, Niyogi K K, Ohlrogge J, Osteryoung K W, Shachar–Hill Y, Sears B B, Sun YN, Takahashi H, Yandell M, Shiu S H, Benning C. 2012. Genome, functional gene annotation, and nuclear transformation of the heterokont oleaginous alga Nannochloropsis oceanica CCMP1779. PLoS Genet, 8 (11): e1003064.CrossRefGoogle Scholar
  35. Wagner G P, Kin K, Lynch V J. 2012. Measurement of mRNA abundance using RNA–seq data: RPKM measure is inconsistent among samples. Theory in Biosciences, 131 (4): 281–285.CrossRefGoogle Scholar
  36. Weeks D P. 2011. Homologous recombination in Nannochloropsis: a powerful tool in an industrially relevant alga. Proceedings of the National Academy of Sciences of the United States of America, 108 (52): 20 859–20 860.CrossRefGoogle Scholar
  37. Young M D, Wakefield M J, Smyth G K, Oshlack A. 2010. Gene ontology analysis for RNA–seq: Accounting for selection bias. Genome Biol ogy, 11 (2): R14.Google Scholar

Copyright information

© Chinese Society for Oceanology and Limnology, Science Press and Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.College of Marine Life SciencesOcean University of ChinaQingdaoChina
  2. 2.Key Laboratory of Marine Genetics and Breeding of Ministry of EducationOcean University of ChinaQingdaoChina
  3. 3.Institutes of Evolution and Marine BiodiversityOcean University of ChinaQingdaoChina
  4. 4.College of Agriculture and Resources and EnvironmentTianjin Agricultural UniversityTianjinChina

Personalised recommendations