Skip to main content

Advertisement

SpringerLink
Log in

The metabolic survival strategy of marine macroalga Ulva prolifera under temperature stress

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

Ulva prolifera is a marine macroalga with medicinal and edible potential, but Ulva is also the causative genus behind undesirable green tides which cause serious adverse effects on coastal ecology and the environment. A strong relationship exists between U. prolifera blooms and ambient temperature; however, the metabolic mechanism involved is still largely unclear. To assess the metabolic changes in U. prolifera in response to temperature stress, the metabolic profile of U. prolifera was analyzed by gas chromatography-mass spectrometry (GC-MS), and a total of 67 compounds were identified. The metabolic profiles of U. prolifera cultured under high- and low-temperature treatments were significantly different from each other, as revealed by principal component analysis (PCA) and orthogonal partial least squares discriminant analysis (OPLS-DA). Twenty-four metabolites, including sugars and amino acids, accumulated under high-temperature stress (HTS) compared with those in the control group, while the levels of 9 and 6 metabolites significantly increased and decreased, respectively, under low-temperature stress (LTS). The galactose, starch/sucrose, and alanine/aspartate/glutamate metabolic pathways were changed under HTS, while the tricarboxylic acid cycle and starch/sucrose, tyrosine, and arginine/proline metabolism were involved in the LTS response. In addition, the metabolic network involved in temperature stress was further constructed. To the best of our knowledge, this is the first study to reveal metabolic shifts in U. prolifera in response to temperature stress and its results provide important insights into the mechanisms involved in the tolerance of U. prolifera to temperature stress and a basis for further research on green tide blooms.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Arbona V, Manzi M, Cd O, Gómezcadenas A (2013) Metabolomics as a tool to investigate abiotic stress tolerance in plants. Int J Mol Sci 14:4885–4991

    Article  CAS  Google Scholar 

  • Bascomb NF, Schmidt RR (1987) Purification and partial kinetic and physical characterization of two chloroplast-localized NADP-specific glutamate dehydrogenase isozymes and their preferential accumulation in Chlorella sorokiniana cells cultured at low or high ammonium levels. Plant Physiol 83:75–84

    Article  CAS  Google Scholar 

  • Bita CE, Gerats T (2013) Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Front Plant Sci 4:1–18

    Article  Google Scholar 

  • Chao Z (2014) Purification and composition analysis of polysaccharide from edible seaweed Enteromorpha prolifera and polysaccharides depolymerized enzymes from microorganisms. Res J Biotechnol 9:30–36

    CAS  Google Scholar 

  • Chen W, Li P (2002) Membrane stabilization by abscisic acid under cold aids proline in alleviating chilling injury in maize (Zea mays L.) cultured cells. Plant Cell Environ 25:955–962

    Article  CAS  Google Scholar 

  • Cui J, Zhang J, Huo Y (2015a) Adaptability of free-floating green tide algae in the Yellow Sea to variable temperature and light intensity. Mar Pollut Bull 101:660–666

    Article  CAS  Google Scholar 

  • Cui W, Fang Q, Zhang Y, Cao H, Zhang J, Wang R, Shen W (2015b) Methane-rich water induces cucumber adventitious rooting through heme oxygenase1/carbon monoxide and Ca2+ pathways. Plant Cell Rep 34:435–445

    Article  CAS  Google Scholar 

  • Diamant S, Eliahu N, Rosenthal D, Goloubinoff P (2001) Chemical chaperones regulate molecular chaperones in vitro and in cells under combined salt and heat stresses. J Biol Chem 276:39586–39591

    Article  CAS  Google Scholar 

  • Dittami SM, Gravot A, Goulitquer S, Rousvoal S, Peters AF, Bouchereau A (2012) Towards deciphering dynamic changes and evolutionary mechanisms involved in the adaptation to low salinities in Ectocarpus (brown algae). Plant J Cell Mol Biol 71:366–377

    CAS  Google Scholar 

  • Edwards DM, Reed RH, Chudek JA, Foster R, Stewart WDP (1987) Organic solute accumulation in osmotically-stressed Enteromorpha intestinalis. Mar Biotechnol 95:583–592

    CAS  Google Scholar 

  • Eggert A (2012) Seaweed responses to temperature. In: Wiencke C, Bischof K (eds) Seaweed biology: novel insights into ecophysiology, ecology and utilization. Springer, Berlin, pp 47–66

    Chapter  Google Scholar 

  • Fan X, Xu D, Wang Y, Zhang X, Cao S, Mou S, Ye N (2014) The effect of nutrient concentrations, nutrient ratios and temperature on photosynthesis and nutrient uptake by Ulva prolifera: implications for the explosion in green tides. J Appl Phycol 26:537–544

    Article  CAS  Google Scholar 

  • Fiehn O (2002) Metabolomics—the link between genotypes and phenotypes. Plant Mol Biol 48:155–171

    Article  CAS  Google Scholar 

  • Gupta V, Thakur RS, Baghel RS, Reddy CRK, Jha B (2014) Seaweed metabolomics: new facet of functional genomics. Adv Bot Res 71:31–52

    Article  Google Scholar 

  • Guy C, Kaplan F, Kopka J, Selbig J, Hincha DK (2008) Metabolomics of temperature stress. Physiol Plant 132:220–235

    CAS  PubMed  Google Scholar 

  • Haxen PG, Lewis OAM (1981) Nitrate assimilation in the marine kelp Macrocystis anguatifolia (Phaeophyceae). Bot Mar 24:631–635

    CAS  Google Scholar 

  • Hiraoka M (2003) Different life histories of Enteromorpha prolifera (Ulvales, Chlorophyta) from four rivers on Shikoku Island, Japan. Phycologia 42:275–284

    Article  Google Scholar 

  • Hong J, Yang L, Zhang D, Shi J (2016) Plant metabolomics: an indispensable system biology tool for plant science. Int J Mol Sci 17:1–16

    Google Scholar 

  • Inokuchi R, Itagaki T, Wiskich JT, Nakayama K, Okada M (1997) An NADP-glutamate dehydrogenase from the green alga Bryopsis maxima: purification and properties. Plant Cell Physiol 38:327–335

    Article  CAS  Google Scholar 

  • Kakinuma M, Coury DA, Kuno Y, Itoh S, Kozawa Y, Inagaki E, Yoshiura Y, Amano H (2006) Physiological and biochemical responses to thermal and salinity stresses in a sterile mutant of Ulva pertusa (Ulvales, Chlorophyta). Mar Biol 149:97–106

    Article  CAS  Google Scholar 

  • Kumar M, Kuzhiumparambil U, Pernice M, Jiang Z, Ralph PJ (2016) Metabolomics: an emerging frontier of systems biology in marine macrophytes. Algal Res 16:76–92

    Article  Google Scholar 

  • Kumar M, Kuzhiumparambil U, Ralph P, Contreras-Porcia L (2017) Polyamines: stress metabolite in marine macrophytes. In: Madamwar D, Pandey A (eds) Algal green chemistry, recent progress in biotechnology. Elsevier, Amsterdam, pp 243–255

    Chapter  Google Scholar 

  • Li X, Han Z, Liu X, Jin S, Liu Y (2016) A study of the relationship between the processes of Enteromorpha and Sargassum and sea surface temperature. Trans Oceanol Limnol 5:126–130

    Google Scholar 

  • Li YH, Wang D, Xu XT, Gao XX, Sun X, Xu NJ (2017) Physiological responses of a green algae (Ulva prolifera) exposed to simulated acid rain and decreased salinity. Phytosynthetica 55:623–629

    Article  CAS  Google Scholar 

  • Lin A, Shen S, Wang J, Yan B (2008) Reproduction diversity of Enteromorpha prolifera. J Integr Plant Biol 50:622–629

    Article  Google Scholar 

  • Linting M, Meulman JJ (2011) Statistical significance of the contribution of variables to the PCA solution: an alternative permutation strategy. Psychometrika 76:440–460

    Article  Google Scholar 

  • Lisec J, Schauer N, Kopka J, Willmitzer L, Fernie AR (2006) Gas chromatography mass spectrometry-based metabolite profiling in plants. Nat Protoc 1:387–395

    Article  CAS  Google Scholar 

  • Liu Y, Xu J, Li X, Yao D, Liu Z (2014) The effects of different proliferative ways for the green tide alga Ulva prolifera on their growth and photophysiological performances. J Fish China 38:691–696

    Google Scholar 

  • Liu Q, Yu RC, Yan T, Zhang QC, Zhou MJ (2015) Laboratory study on the life history of bloom-forming Ulva prolifera in the Yellow Sea. Estuar Coast Shelf Sci 163:82–88

    Article  CAS  Google Scholar 

  • Luo MB, Liu F, Xu ZL (2012) Growth and nutrient uptake capacity of two co-occurring species, Ulva prolifera and Ulva linza. Aquat Bot 100:18–24

    Article  CAS  Google Scholar 

  • Mishra D, Shekhar S, Agrawal L, Chakraborty S, Chakraborty N (2017) Cultivar-specific high temperature stress responses in bread wheat (Triticum aestivum (L.)) associated with physicochemical traits and defense pathways. Food Chem 221:1077–1087

    Article  CAS  Google Scholar 

  • Muñoz-Blanco J, Moyano E, Cárdenas J (1989) Glutamate dehydrogenase isozymes of Chlamydomonas reinhardtii. FEMS Microbiol Lett 61:315–318

    Article  Google Scholar 

  • Nylund GM, Weinberger F, Rempt M, Pohnert G (2011) Metabolomic assessment of induced and activated chemical defence in the invasive red alga Gracilaria vermiculophylla. PLoS One 6:e29359

    Article  CAS  Google Scholar 

  • Oaks A (1994) Primary nitrogen assimilation in higher plants and its regulation. Can J Bot 72:739–750

    Article  CAS  Google Scholar 

  • Planchet E, Limami AM (2015) Amino acid synthesis under abiotic stress. In: D’Mello JPF (ed) Amino acids in higher plants. CBA, Wallingford, pp 262–276

    Google Scholar 

  • Robinson SA, Slade AP, Fox GG, Phillips R, Ratcliffe RG, Stewart GR (1991) The role of glutamate dehydrogenase in plant nitrogen metabolism. Plant Physiol 95:509–516

    Article  CAS  Google Scholar 

  • Ruan YL, Jin Y, Yang YJ, Li GJ, Boyer JS (2010) Sugar input, metabolism, and signaling mediated by invertase: roles in development, yield potential, and response to drought and heat. Mol Plant 3:942–955

    Article  CAS  Google Scholar 

  • Sato M, Sato Y, Tsuchiya Y (1984) Glutamate dehydrogenase of Porphyra yezoensis. Hydrobiologia 116/117:584–587

    Article  Google Scholar 

  • Sieciechowicz KA, Joy KW, Ireland RJ (1988) The metabolism of asparagine in plants. Phytochemistry 27:663–671

    Article  CAS  Google Scholar 

  • Sousa AI, Martins I, Lillebø AI, Flindt MR, Pardal MA (2007) Influence of salinity, nutrients and light on the germination and growth of Enteromorpha sp. spores. J Exp Mar Biol Ecol 341:142–150

    Article  CAS  Google Scholar 

  • Srivastava HS, Singh RP (1987) Role and regulation of L-glutamate dehydrogenase activity in higher plants. Phytochemistry 26:597–610

    Article  CAS  Google Scholar 

  • Szabados L, Savouré A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97

    Article  CAS  Google Scholar 

  • Thakur P, Kumar S, Malik JA, Berger JD, Nayyar H (2010) Cold stress effects on reproductive development in grain crops: an overview. Environ Exp Bot 67:429–443

    Article  CAS  Google Scholar 

  • Theocharis A, Clément C, Barka EA (2012) Physiological and molecular changes in plants grown at low temperatures. Planta 235:1091–1105

    Article  CAS  Google Scholar 

  • Wang J, Yan B, Lin A, Hu J, Shen S (2007) Ecological factor research on the growth and induction of spores release in Enteromorpha prolifera (Chlorophyta). Mar Sci Bull (Chin Ed) 26:60–65

    Google Scholar 

  • Wang Y, Miao J, Jiang Y, Liu F, Zheng Z, Li G (2016) Roles of proline and soluble sugar in the cold-adaptation of Antarctic ice microalgae. Biotechnol Bull 32:198–202

    CAS  Google Scholar 

  • Webb WL, Newton M, Starr D (1974) Carbon dioxide exchange of Alnus rubra: a mathematical model. Oecologia 17:281–291

    Article  Google Scholar 

  • Xia J, Sinelnikov IV, Han B, Wishart DS (2015) MetaboAnalyst 3.0—making metabolomics more meaningful. Nucleic Acids Res 43:W251–W257

    Article  CAS  Google Scholar 

  • Zhang J, Huo Y, Yu K, Chen Q, He Q, Han W, Chen L, Cao J, Shi D, He P (2013a) Growth characteristics and reproductive capability of green tide algae in Rudong coast, China. J Appl Phycol 25:795–803

    Article  Google Scholar 

  • Zhang Z, Wang X, Zhao M, Yu S, Qi H (2013b) The immunological and antioxidant activities of polysaccharides extracted from Enteromorpha linza. Int J Biol Macromol 57:45–49

    Article  CAS  Google Scholar 

Download references

Funding

This study was financially supported by the National Natural Science Foundation of China (41276122; 41606129). This research was also sponsored by the K.C.Wong Magna Fund in Ningbo University.

Author information

Authors and Affiliations

  1. Key Laboratory of Applied Marine Biotechnology of Department of Education, Ningbo University, Ningbo, Zhejiang, 315211, People’s Republic of China

    Yanli He, Chaoyang Hu, Dandan Cui, Xue Sun, Yahe Li & Nianjun Xu

  2. Zhejiang Pharmaceutical College, Ningbo, Zhejiang, 315100, People’s Republic of China

    Yanli He & Yanhui Wang

Authors
  1. Yanli He
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chaoyang Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yanhui Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dandan Cui
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xue Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yahe Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Nianjun Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nianjun Xu.

Electronic supplementary material

Table S1

The fitted parameters from the rapid light curves of U. prolifera at LTS, Control and HTS. (DOCX 14 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

He, Y., Hu, C., Wang, Y. et al. The metabolic survival strategy of marine macroalga Ulva prolifera under temperature stress. J Appl Phycol 30, 3611–3621 (2018). https://doi.org/10.1007/s10811-018-1493-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-018-1493-3

Keywords

Search

Navigation