Skip to main content
SpringerLink
Log in

Effects of nitrogen source and irradiance on Porphyridium cruentum

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

Abstract

We determined the effects of two nitrogen sources (ammonium and nitrate) and two irradiance levels (50 and 200 μmol photons m−2 s−1) on the growth rate, cell size, proximate composition, pigment content, and photosynthesis of the unicellular red alga, Porphyridium cruentum. Irradiance significantly affects growth rate, as well as carbohydrate, protein, and phycoerythrin content. Nitrogen form significantly affects cell size, total dry weight, organic dry weight, ash content, carotene content, phycocyanin content, allophycocyanin content, maximum relative electron transport rate (rETRm), and photosynthetic efficiency (α). However, the irradiance and nitrogen source had significantly interaction with the content of lipids and chlorophyll a content, relative electron transport rate (rETR), and irradiance of saturation (Ik). These findings demonstrate that irradiance and nitrogen source influence the metabolism of P. cruentum and that the combination of these two variables induces the production of chemical products for biotechnological, aquaculture, and nutraceutical industry.

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.

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

Similar content being viewed by others

References

  • Adda M, Merchu JC, Arad SM (1986) Effect of nitrate on growth and production of cell-wall polysaccharide by the unicellular red alga Porphyridium. Biomass 10:131–140

    Article  CAS  Google Scholar 

  • Ahern TJ, Katoh S, Sada E (1983) Arachidonic acid production by the red algae Porphyridium cruentum. Biotechnol Bioeng 25:1057–1070

    Article  CAS  PubMed  Google Scholar 

  • Ahlström LH, Eskilsson CS, Björklund E (2005) Determination of banned azo dyes in consumer goods. Trends Anal Chem 24:49–56

    Article  Google Scholar 

  • Antia NJ, Desai ID, Romilly MJ (1970) The tocopherol, vitamin K and related isoprenoid quinone composition of an unicellular red algae (Porphyridium cruentum). J Phycol 6:305–312

    CAS  Google Scholar 

  • APHA (American Public Health Association (APHA) (1971) Standard methods for the examination of water and wastewater, 13th edn. APHA, Washington, D.C, p 110

    Google Scholar 

  • Arad A, Yaron A (1992) Natural pigments from red microalgae for use in foods and cosmetics. Trends Food Sci Technol 3:92–97

    Article  CAS  Google Scholar 

  • Becker EW (2007) Micro-algae as a source of protein. Biotechnol Adv 25:207–210

    Article  CAS  PubMed  Google Scholar 

  • Bennet A, Bogorad L (1973) Complimentary chromatic adaptation in a filamentous blue-green alga. J Cell Biol 58:419–435

    Article  Google Scholar 

  • Bermejo-Román R, Alvárez-Pez JM, Acién-Fernández FG, Molina-Grima E (2002) Recovery of pure B-phycoerythrin from the microalgae Porphyridium cruentum. J Biotechnol 93(1):73–85

    Article  PubMed  Google Scholar 

  • Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917

    Article  CAS  PubMed  Google Scholar 

  • Brown MR (2002) Nutritional value of microalgae for aquaculture. In: Cruz-Suárez LE, Ricque-Marie D, Tapia-Salazar M, Gaxiola-Cortez MG, Simoes N (eds) Avances en Nutrición Acuícola VI Simposium Internacional de Nutrición Acuícola. 3–6 de septiembre, Cancún, Quintana Roo, pp 281–292

  • Chiaverini J (1972) Techniques d’extraction et d’analyse des lipids. Université de Paris et Marie Curie, Paris. Station Zoologique Villefranche-Sur-Mer. Notes de Travail 12, p 12

  • Cuellar-Bermúdez SP, Aguilar-Hernández I, Cárdenas-Chávez DL, Ornelas-Soto N, Romero-Ogawa MA, Parra-Saldívar R (2014) Extraction and purification of high-value metabolites from microalgae: essential lipids, astaxanthin and phycobiliproteins. Microbioal Biotechnol 8:190–209

    Article  Google Scholar 

  • Curtin ME (1985) Chemicals from the sea. Biotechnology 3:34–37

    Google Scholar 

  • Darley MW (1987) Biología de las Algas: Enfoque Fisiológico. In: México, DF (ed) Limusa SA de CV. p 236

  • Dubinsky Z, Stambler N (2009) Photoacclimation processes in phytoplankton mechanism, consequences, and applications. Aquat Microb Ecol 56:163–176

    Article  Google Scholar 

  • Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356

  • Fábregas J, García D, Morales E, Domínguez A, Otero A (1998) Renewal rate of semicontinuous cultures of the microalga Porphyridium cruentum modifies phycoerythrin, exopolysaccharides and fatty acid productivity. J Ferment Bioeng 86:477–481

  • Falkowski PG, Owens TG (1980) Light-shade adaptation: two strategies in marine phytoplankton. Plant Physiol 66:592–595

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Falkowski PG, Raven JA (2007) Aquatic photosynthesis. Princeton University Press, Princenton, p 484

    Google Scholar 

  • Figueroa FL, Conde-Álvarez R, Gómez I (2003) Relation between electron transport rates determined by pulse amplitude modulated chlorophyll fluorescence and oxygen evolution on macroalgae under different light conditions. Photosynth Res 75:259–275

    Article  CAS  PubMed  Google Scholar 

  • Figueroa FL, Jerez CG, Korbee N (2013) Use of in vivo chlorophyll fluorescence to estimate photosynthetic activity and biomass productivity in microalgae grown in different culture systems. Lat Am J Aquat Res 41(5):801–819

    Article  Google Scholar 

  • Flaak AR, Epifanio CE (1978) Dietary protein levels and growth of the oyster Crassostrea virginica. Mar Biol 45:157–163

    Article  CAS  Google Scholar 

  • Fogg GE, Thake BJ (1987) Algal cultures and phytoplankton ecology. University of Wisconsin Press, London, p 269

    Google Scholar 

  • Gantt E (1969) Properties and ultrastructure of phycoerythrin from Porphyridium cruentum. Plant Physiol 44:1629–1638

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gantt E (1981) Phycobilisomes. Annu Rev Plant Physiol 32:327–347

    Article  CAS  Google Scholar 

  • Geider RJ, Osborne BA (1992) Algal photosynthesis: the measurement of algal gas exchange. Chapman and Hall Press, New York, p 256

    Book  Google Scholar 

  • Gigova LG, Ivanova NJ (2015) Microalgae respond differently to nitrogen availability during culturing. J Biosci 40:365–374

    Article  CAS  PubMed  Google Scholar 

  • Grewe CB, Pulz O (2012) The biotechnology of cyanobacteria. In: Whitton BA (ed) Ecology of Cyanobacteria II. Springer, Netherlands, pp 707–739

  • Guedes AC, Amaro HM, Malcata FX (2011) Microalgae as sources of carotenoids. Mar Drugs 9:625–644

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guillard RLL, Ryther JH (1962) Studies on marine planktonic diatoms I. Cyclotella nana Hustedt and Detonula confervacea (Cleve) Gran. Can J Microbiol 8:229–239

    Article  CAS  PubMed  Google Scholar 

  • Hu Q (2005) Environmental effects on cell composition. In: Richmond A (ed) Handbook of microalgal culture. Biotechnology and Applied Phycology. Blackwell Publishing, Oxford, pp 83–93

    Google Scholar 

  • Kathiresan S, Sarada R, Bhattacharya S, Ravishankar GA (2007) Culture media optimization for growth and phycoerythrin production from Porphyridium purpureum. Biotechnol Bioeng 96:456–463

    Article  CAS  PubMed  Google Scholar 

  • Kavitha MD, Seema Shree MH, Vidyashankar S, Sarada R (2016) Acute and subchronic safety assessment of Porphyridium purpureum biomass in the rat model. J Appl Phycol 28:1071–1083

    Article  CAS  Google Scholar 

  • Kirk JTO (1994) Light and photosynthesis in aquatic ecosystems. Cambridge University Press, Cambridge, p 401

    Book  Google Scholar 

  • Kromkamp J, Peene J (1999) Estimation of phytoplankton photosynthesis and nutrient limitation in the Eastern Scheldt estuary using variable fluorescence. Aquat Ecol 33:101–104

    Article  CAS  Google Scholar 

  • Lee YK, Tan HM (1988) Effect of temperature, light intensity and dilution rate on the cellular composition of red alga in light-limited chemostat cultures. MIRCEN J Appl Microbiol Biotechnol 4:231–237

    Article  CAS  Google Scholar 

  • Lourenço SO, Barbarino E, Mancini-Filho J, Schinke KP, Aidar E (2002) Effects of different nitrogen sources on the growth and biochemical profile of 10 marine microalgae in batch culture: an evaluation for aquaculture. Phycologia 41:158–168

  • Lowry OH, Rosebrough HJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin-phenol reagent. J Biol Chem 193:265–275

    CAS  PubMed  Google Scholar 

  • Matos-Moura A, Bezerra-Neto E, Koening ML, Leca EE (2007) Chemical composition of three microalgae species for possible use in mariculture. Braz Arch Biol Technol 50(3):461–467

    Article  Google Scholar 

  • Mazzuca-Sobczuc T, Ibañez-González MJ, Molina-Grima E, Urrutia-Martínez T, Yusuf Ch (2015) Concentración de cultivos de microalgas por un proceso de eliminación osmótica del medio utilizandodisoluciones de glicerol. Spanish Patent 2 545 829

  • Miller SR, Castenholtz RW (2001) Ecological physiology of Synechococcus sp. strain SH-94-5, a naturally occurring cyanobacterium deficient in nitrate assimilation. Appl Environ Microbiol 67:3002–3009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Misra HP, Fridovich I (1977) Purification and properties of superoxide dismutase from a red alga, Porphyridium cruentum. J Biol Chem 252:6421–6423

    CAS  PubMed  Google Scholar 

  • Muller-Feuga A, Moaly J, Kaas R (2007) The microalgae of aquaculture. In: Støttrup JG, McEvoy LA (eds) Live feeds in marine aquaculture. Blackwell Science, Oxford, pp 207–252

    Google Scholar 

  • Nuutila AM, Aura AM, Kiesvaara M, Kauppinen V (1997) The effect of salinity, nitrate concentration, pH and temperature on eicosapentaenoic acid (EPA) production by the red unicellular alga Porphyridium purpureum. J Biotechnol 55:55–63

    Article  CAS  Google Scholar 

  • Oh SH, Han JG, Kim Y, Ha JH, Kim SS, Jeong MH, Jeong HS, Kim NY, Cho JS, Yoon WB, Lee SY, Kang DH, Lee SY (2009) Lipid production in Porphyridium cruentum grown under different culture conditions. J Biosci Bioeng 108:429–434

    Article  CAS  PubMed  Google Scholar 

  • Pande SV, Khan RP, Venkitasubramanian TA (1963) Microdetermination of lipids and serum total acids. Anal Biochem 6:415–423

    Article  CAS  PubMed  Google Scholar 

  • Pangestuti R, Kim S-K (2011) Biological activities and health benefit effects of natural pigments derived from marine algae. J Funct Foods 3:255–266

    Article  CAS  Google Scholar 

  • Paniagua-Michel J, Dujardin E, Sironval C (1993) Le tecuitlatl, concentré de spirulines source de protéines comestibles chez les Aztèques. Cah Agric 2(4):283–287

    Google Scholar 

  • Parsons TR, Maita Y, Lalli CM (1984) A manual of chemical and biological methods for seawater analysis. Pergamon Press, Oxford, p 173

    Google Scholar 

  • Pulz O, Gross W (2004) Valuable products from biotechnology of microalgae. Microbiol Biotechnol 65:635–648

    Article  CAS  Google Scholar 

  • Qi H, Wang J, Wang Z (2013) A comparative study of the sensitivity of Fv/Fm to phosphorus limitation on four marine microalgae. J Ocean Univ China 12:77–84

    Article  CAS  Google Scholar 

  • Raven JA, Geider RJ (2003) Adaptation, acclimation and regulation in algal photosynthesis. In: Larkum AWD, Douglas SE, Raven JA (eds) Advances in photosynthesis and respiration, Photosynthesis in algae, Kluwer, Dordrecht, pp 385–412

  • Raven JA, Giodano M (2016) Combined nitrogen. In: Borowitzka MA, Beardall J, Raven JA (eds) The physiology of microalgae. Springer, Dordrecht, pp 143–154

    Chapter  Google Scholar 

  • Razaghi A, Godhe A, Albers E (2014) Effects of nitrogen on growth and carbohydrate formation in Porphyridium cruentum. Cent Eur J Biol 9:156–162

  • Rebolloso-Fuentes MM, Acién-Fernández GG, Sánchez-Péz JA, Guil-Guerrero JL (2000) Biomass nutrient profiles of the microalga Porphyridium cruentum. Food Chem 70:345–353

    Article  CAS  Google Scholar 

  • Romay C, González R, Ledón N, Remirez D, Rimbao V (2003) C-Phycocyanin: a biliprotein with antioxidant, anti-inflamatory and neuroprotective effects. Curr Protein Pept Sci 4:207–216

    Article  CAS  PubMed  Google Scholar 

  • Ruiz-Ruiz F, Benavides J, Rito-Palomares M (2013) Scaling-up of a B-phycoerythrin production and purification bioprocess involving aqueous two phase systems: practical experiences. Process Biochem 48:738–745

    Article  CAS  Google Scholar 

  • Safi C, Ursu AV, Laroche C, Zebib B, Merah O, Pontalier P-Y, Vaca-García C (2014) Aqueous extraction of proteins from microalgae: effect of different cell disruption methods. Algal Res 3:61–65

    Article  Google Scholar 

  • Sánchez-Saavedra MP, Voltolina D (2005) The growth rate, biomass production and composition of Chaetoceros sp. grown with different light sources. Aquac Eng 35:161–165

    Article  Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry. The principles and practice of statistics in biological research, 3rd edn. WH Freeman & Co., New York, p 887

    Google Scholar 

  • Sorokin C (1973) Dry weight, packed cell volume and optical density. In: Stein JR (ed) Handbook of phycological methods and growth measured. Cambridge University Press, New York, pp 321–343

    Google Scholar 

  • South GR, Whittick A (1987) Introduction to phycology. Blackwell Scientific Publications, London, p 341

    Google Scholar 

  • Spolaore P, Joannis-Cassan C, Duran E, Isambert A (2006) Commercial applications of microalgae. J Biosci Bioeng 101:87–96

    Article  CAS  PubMed  Google Scholar 

  • Thepenier C, Gudin C (1985) Studies on optimal conditions for polysaccharide production by Porphyridium cruentum. World J Microbiol Biotech 1:257–268

    Article  CAS  Google Scholar 

  • Vadiveloo A, Moheimani NR, Cosgrove JJ, Parlevliet D, Bahri PA (2017) Effects of different light spectra on the growth, productivity and photosynthesis of two acclimated strains of Nannochloropsis sp. J Appl Phycol 29:1765–1774

  • Villafañe VE, Gao K, Helbling EW (2005) Short- and long-term effects of solar ultraviolet radiation on the red algae Porphyridium cruentum (S.F. Gray) Nägeli. Photochem Photobiol 4:376–382

  • Vonshak A (1988) Porphyridium. In: Borowitzka MA, Borowitzka LJ (eds) Micro-algal biotechnology. Cambridge University Press, Cambridge, pp 122–134

    Google Scholar 

  • White S, Anandraj A, Bux F (2011) PAM fluorometry as a tool to assess microalgal nutrient stress and monitor cellular neutral lipids. Bioresour Technol 102:1675–1682

    Article  CAS  PubMed  Google Scholar 

  • Whyte JNC (1987) Biochemical composition and energy content of six species of phytoplankton used in mariculture of bivalves. Aquaculture 60:231–241

    Article  CAS  Google Scholar 

  • Widdows J, Fieth P, Worrall CM (1979) Relationships between seston, available food and feeding activity in the common mussel Mytilus edulis. Mar Biol 50:195–207

  • Williams KC (2007) Nutritional requirements and feeds development for post-larval spiny lobster: a review. Aquaculture 263(1):1–14

    Article  Google Scholar 

  • Yen HW, Hu IC, Chen CY, Ho SH, Lee DJ, Chang JS (2013) Microalgae-based biorefinery–from biofuels to natural products. Bioresour Technol 135:166–174

    Article  CAS  PubMed  Google Scholar 

  • You T, Barnett SM (2004) Effect of light quality on production of extracellular polysaccharides and growth rate of Porphyridium cruentum. Biochem Eng J 19:251–258

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Nava-Ruiz V.M., Ruiz-Güereca D.A., Villagómez-Aranda A.L., and Siqueiros-Vargas F. acknowledge their Master in Science scholarship from CONACyT. We thank F.D. López-Figueroa for his help to photosynthetic parameters calculation. English language was edited by Blue Pencil Science and C.G. Paniagua-Chávez.

Funding

This work has been funded by Centro de Investigación Científica y de Educación Superior de Ensenada (CICESE), Fund for Scientific Research and Technological Development of CICESE (Project: 623801), and CICESE (Project: 623101).

Author information

Authors and Affiliations

  1. Department of Aquaculture, Centro de Investigación Científica y de Educación Superior de Ensenada (CICESE), Carretera Ensenada-Tijuana No. 3918, Zona Playitas, 22860, Ensenada, Baja California, Mexico

    M. del Pilar Sánchez-Saavedra, Fátima Y. Castro-Ochoa, Duahmet A. Ruiz-Güereca & Ceres A. Molina-Cárdenas

  2. Department of Marine Ecology, Centro de Investigación Científica y de Educación Superior de Ensenada (CICESE), Carretera Ensenada-Tijuana No. 3918, Zona Playitas, 22860, Ensenada, Baja California, Mexico

    Viridiana Margarita Nava-Ruiz

  3. Department of Microbiology, Centro de Investigación Científica y de Educación Superior de Ensenada (CICESE), Carretera Ensenada-Tijuana No. 3918, Zona Playitas, 22860, Ensenada, Baja California, Mexico

    Duahmet A. Ruiz-Güereca

  4. Department of Marine Biotechnology, Centro de Investigación Científica y de Educación Superior de Ensenada (CICESE), Carretera Ensenada-Tijuana No. 3918, Zona Playitas, 22860, Ensenada, Baja California, Mexico

    Ana Laura Villagómez-Aranda & Fabián Siqueiros-Vargas

Authors
  1. M. del Pilar Sánchez-Saavedra
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fátima Y. Castro-Ochoa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Viridiana Margarita Nava-Ruiz
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Duahmet A. Ruiz-Güereca
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ana Laura Villagómez-Aranda
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Fabián Siqueiros-Vargas
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ceres A. Molina-Cárdenas
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. del Pilar Sánchez-Saavedra.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sánchez-Saavedra, M.d.P., Castro-Ochoa, F.Y., Nava-Ruiz, V.M. et al. Effects of nitrogen source and irradiance on Porphyridium cruentum . J Appl Phycol 30, 783–792 (2018). https://doi.org/10.1007/s10811-017-1284-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-017-1284-2

Keywords

Search

Navigation