Skip to main content

Advertisement

SpringerLink
Log in

Growth and biochemical variability of complete and lipid extracted Chlorella species (application for Artemia franciscana feeding)

  • Published:
Rendiconti Lincei Aims and scope Submit manuscript

Abstract

This work aims at culturing different Chlorella species, monitoring growth and estimating the nutritional quality for further application of complete cells and lipid extracted biomass in Artemia franciscana feeding. We conducted experiments using C. marina, C. salina, C. capsulata, C. stigmatophora and C. vulgaris that were batch cultured for 14 days. C. salina showed the maximal count on the sixth day while C. marina recorded the maximum growth rate (2 ± 0.177). However, C. capsulata and C. stigmatophora recorded the minimum rate (1.5 ± 0.11). Analyses of algal biomass showed that C. capsulata contains maximal lipids and carbohydrates, but the minimal protein (22.8 ± 1.4 %). However, C. salina contained the highest protein (33.1 ± 1.4 %). After oil extraction, there were no significant losses in the other biochemical constituents of the studied Chlorella species. Considering algae metabolites, saturated fatty acids were the main constituent in the fatty acids methyl esters (FAMEs). Palmitic and stearic acids were dominant. Amino acid pools of the experimental marine Chlorella species were found to contain lysine, methionine and histidine; but were deficient in cysteine. The present investigation showed that lipids, proteins and protein to lipid ratio of A. franciscana napulli enriched with mixed cells of Chlorella species were enhanced by (22 %); 1.96 and 1.33 folds, respectively. Furthermore, the growth and survival of A. franciscana showed significant increases when fed on lipid extracted algae residuals, especially that of a mixed diet; which is considered as an important achievement and confirms that the residual algae biomass can be significantly used for aquaculture feeding.

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

Similar content being viewed by others

References

  • Abomohra AE, El-Sheekh M, Hanelt D (2014) Pilot cultivation of the chlorophyte microalga Scenedesmus obliquus as a promising feedstock for biofuel. Biomass Bioenergy 64:237–244

    Article  CAS  Google Scholar 

  • Adarme-Vega TC, Lim DK, Timmins M, Vernen F, Li Y et al (2012) Microalgal biofactories: a promising approach towards sustainable omega-3 fatty acid production. Microb Cell Fact 11(1):96

    Article  CAS  Google Scholar 

  • AOAC (1995) Official methods of analysis of the association of official analytical chemists, 16th ed. Carotenoids and ascorbic acid composition from commercial products of cashew apple (Anacardium occidentale L.). J Food Comp Anal 16:647–657

  • Araújo S, Garcia VMT (2005) Growth and biochemical composition of the diatom Chaetoceros cf. wighamii brightwell under different temperature, salinity and carbon dioxide levels. I. Protein, carbohydrates and lipids. Aquaculture 246(1):405–412

    Article  Google Scholar 

  • Bakhtiarvandi NK, Kenari AA, Nazari RM, Makhdoomi C (2014) Ontogenetic changes in lipids, fatty acid, and body composition during larval stages of Caspian kutum (Rutilus frisii kutum). IJFS 13(2):365–383

    Google Scholar 

  • Barsanti L, Gualtieri P (2006) Algae—anatomy, biochemistry, and biotechnology. CRC Press, Boca Raton, p 301

    Google Scholar 

  • Becker EW (2007) Micro-algae as a source of protein. Biotechnol Adv 25(2):207–210

    Article  CAS  Google Scholar 

  • Bi Z, He BB (2013) Characterization of microalgae for the purpose of biofuel production. Trans ASABE 56(4):1529–1539

    CAS  Google Scholar 

  • Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37(8):911–917

    Article  CAS  Google Scholar 

  • Brown MR (2002) Nutritional value of microalgae for aquaculture. In: Cruz-Suárez LE, Ricque-Marie D, Tapia-Salazar M, Gaxiola-Cortés MG, Simoes N (eds) Avances en Nutrición Acuícola VI. Memorias del VI Simposium Internacional de Nutrición Acuícola.Cancún, Quintana Roo, México

  • Brown MR, Jeffrey SW, Volkman JK, Dunstan GA (1997) Nutritional properties of microalgae for mariculture. Aquaculture 151(1):315–331

    Article  CAS  Google Scholar 

  • Cho SH, Ji SC, Hur SB, Bae J, Park IS, Song YC (2007) Optimum temperature and salinity conditions for growth of green algae Chlorella ellipsoidea and Nannochloris oculata. Fish Sci 73(5):1050–1056

    Article  CAS  Google Scholar 

  • Cisneros R, Vinatea E (2009) Producción de biomasa de Artemia franciscana Kellogg 1906 utilizando diferentes dietas. Ecología aplicada 8(1–2):9–14

    Article  Google Scholar 

  • Courtois de Viçose GC, Viera MP, Huchette S, Izquierdo MS (2012) Improving nursery performances of Halioti stuberculata coccinea: nutritional value of four species of benthic diatoms and green macroalgae germlings. Aquaculture 334:124–131

    Article  Google Scholar 

  • Dib M (2012) Chlorela sp.: Lipid extracted algae utilization of algae biodiesel co-products as an alternative protein feed in animal production (Doctoral dissertation, Colorado State University)

  • do Amaral P, Freire M (2012) Evaluation of algae concentration in manure based media. PhD thesis, University of Kentucky, p 182

  • Dubois M, Gilles KA, HamiHon JK, Smith F (1959) Phenol-sulphic method in carbohydrates chemistry. Wistler LR, Wolform RL (eds) Academic Press, New York, pp 388–403

  • El-Sheekh MM, El-Kassas HY (2014) Biosynthesis, characterization and synergistic effect of phytogenic gold nanoparticles by marine picoeukaryote Picochlorum sp. in combination with antimicrobials. Rend Fis Acc Lincei 25:513–521. doi:10.1007/s12210-014-0341-x

    Article  Google Scholar 

  • El-Sheekh MM, Hamouda RA (2016) Lipids extraction from the green alga Ankistrodesmus falcatus using different methods. Rend Fis Acc Lincei 27:589–595. doi:10.1007/s12210-016-0528-4

    Article  Google Scholar 

  • El-Sheekh MM, Gheda SF, Khairy HM, El-Shenody RA (2015) Optimization of medium components using Plackett-Burman design for high production of protein, carbohydrates and lipids in the microalga Tetraselmis chuii. Egypt J Exp Bio (Botany) 11(1):77–88

    Google Scholar 

  • Fábregas J, Otero A, Morales ED, Arredondo-Vega BO, Patiño M (1998) Modification of the nutritive value of Phaeodactylum tricornutum for Artemia sp. in semicontinuous cultures. Aquaculture 169(3):167–176

    Article  Google Scholar 

  • Feng Y, Li C, Zhang D (2011) Lipid production of Chlorella vulgaris cultured in artificial wastewater medium. Bioresour Technol 102(1):101–105

    Article  CAS  Google Scholar 

  • Gerasimenko NI, Busarova NG, Moiseenko OP (2010) Seasonal changes in the content of lipids, fatty acids, and pigments in brown alga Costaria costata. Russ J Plant Physl 57(2):205–211

    Article  CAS  Google Scholar 

  • Godínez DE, Gallo R, Gelabert AH, Gamboa DJ, Landa V, Godínez EM (2004) Crecimientolarvario de Artemia franciscana (Kellog, 1906) alimentada con dos especies de microalgas vivas. Zootec Trop 22:265–275

    Google Scholar 

  • Grigorova S (2006) Dry biomass of fresh water algae of Chlorella genus in the combined forages for laying hens. JCEA 6(4):625–630

    Google Scholar 

  • Guccione A, Biondi N, Sampietro G, Rodolfi L et al (2014) Chlorella for protein and biofuels: from strain selection to outdoor cultivation in a Green Wall Panel photobioreactor. Biotechnol Biofuels 7(1):1

    Article  Google Scholar 

  • Guillard RR, Ryther JH (1962) Studies of marine planktonic diatoms: i. Cyclotella nana Hustedt, and Detonulacon fervacea (cleve) gran. Can J Microbiol 8(2):229–239

    Article  CAS  Google Scholar 

  • Hartee EF (1972) A modification of Lawry method that gives a linear photometric response. Anal Biochem 41:422–430

    Article  Google Scholar 

  • Huerlimann R, De Nys R, Heimann K (2010) Growth, lipid content, productivity, and fatty acid composition of tropical microalgae for scale up production. Biotechnol Bioeng 107(2):245–257

    Article  CAS  Google Scholar 

  • Ilavarasi A, Mubarakali D, Praveenkumar R, Baldev E, Thajuddin N (2011) Optimization of various growth media to freshwater microalgae for biomass production. Biotechnol 10:540–545

    Article  CAS  Google Scholar 

  • Jayasankar R, Valsala KK (2008) Influence of different concentrations of sodium bicarbonate on growth rate and chlorophyll content of Chlorella salina. JMBAI 50(1):74–78

    Google Scholar 

  • Khairy HM, El-Sayed HS (2012) Effect of enriched Brachionus plicatilis and Artemia franciscana nauplii by microalga Tetraselmis chuii (Bütcher) grown on four different culture media on the growth and survival of Sparus aurata larvae. Afr J Biotech 11(2):399–415

    CAS  Google Scholar 

  • Kim K-W, Bai SC, Koo J-W, Wang X (2002) Effects of dietary Chlorella ellipsoidea supplementation on growth, blood characteristics, and whole-body composition in juvenile Japanese flounder Paralichthys olivaceus. J World Aquac Soc33(4):425e31

  • Lavens P, Sorgeloos P (1996) (eds) Manual on the production and use of live food for aquaculture. FAO Fisheries Technical Paper. No. 361. Rome, FAO, p 295

  • Maldonado-Montiel TD, Rodríguez-Canché LG (2005) Biomass production and nutritional value of Artemiasp. (Anostraca: Artemiidae) in Campeche, México. Rev Biol Trop 53(3–4):447–454

    Google Scholar 

  • Mandalam RK, Palsson BO (1997) Cell cycle of Chlorella vulgaris can deviate from the synchronous binary division model. Biotechnol Lett 19(6):587–591

    Article  CAS  Google Scholar 

  • Markou G, Chatzipavlidis I, Georgakakis D (2012) Carbohydrates production and bio-flocculation characteristics in cultures of Arthrospira (Spirulina) platensis: improvements through phosphorus limitation process. BioEnergy research 5(4):915–925

    Article  CAS  Google Scholar 

  • Milledge JJ (2011) Commercial application of microalgae other than as biofuels: a brief review. Rev Environ Sci Biotechnol 10(1):31–41

    Article  Google Scholar 

  • Moheimani NR (2013) Long-term outdoor growth and lipid productivity of Tetraselmis suecica, Dunaliella tertiolecta and Chlorella sp. (Chlorophyta) in bag photobioreactors. J Appl Phycol 25(1):167–176

    Article  CAS  Google Scholar 

  • Muller-Feuga A (2000) The role of microalgae in aquaculture: situation and trends. J Appl Phycol 12(3–5):527–534

    Article  Google Scholar 

  • Muthukumar A, Elayaraja S, Ajithkumar TT, Kumaresan S, Balasubramanian T (2012) Biodiesel production from marine microalgae Chlorella marina and Nannochloropsis salina. J Petrol Technol Altern Fuels 3:58–62

    CAS  Google Scholar 

  • Olsen AI, Olsen Y, Attramadal Y, Christie K, Birkbeck TH et al (2000) Effects of short term feeding of microalgae on the bacterial flora associated with juvenile Artemia franciscana. Aquaculture 190(1):11–25

    Article  Google Scholar 

  • Ötleş S, Pire R (2001) Fatty acid composition of Chlorella and Spirulina microalgae species. J AOAC Int 84(6):1708–1714

    Google Scholar 

  • Pacheco-Vega JM, Cadena-Roa MA, Ascencio F, Rangel-Dávalos C, Rojas-Contreras M (2015) Assessment of endemic microalgae as potential food for Artemia franciscana culture. Lat Am J Aquat Res 43(1):23–32

    Article  Google Scholar 

  • Patil V, Reitan KI, Knutsen G, Mortensen LM, Källqvist T et al (2005) Microalgae as source of polyunsaturated fatty acids for aquaculture. Plant Biol 6:57–65

    Google Scholar 

  • Pettersen AK, Turchini GM, Jahangard S, Ingram BA, Sherman CD (2010) Effects of different dietary microalgae on survival, growth, settlement and fatty acid composition of blue mussel (Mytilus galloprovincialis) larvae. Aquaculture 309(1):115–124

    Article  CAS  Google Scholar 

  • Prommuak C, Pavasant P, Quitain AT, Goto M, Shotipruk A (2013) Simultaneous production of biodiesel and free lutein from Chlorella vulgaris. Chem EngTechnol 36:733–739

    CAS  Google Scholar 

  • Pulz O, Gross W (2004) Valuable products from biotechnology of microalgae. Appl Microbiol Biotechnol 65(6):635–648

    Article  CAS  Google Scholar 

  • Radwan SS (1978) Coupling of two-dimensional thin-layer chromatography with gas chromatography for the quantitative analysis of lipid classes and their constituent fatty acids. J Chromatogr Sci 16(11):538–542

    Article  CAS  Google Scholar 

  • Rausch T (1981) The estimation of micro-algal protein content and its meaning to the evaluation of algal biomass I. Comparison of methods for extracting protein. Hydrobiologia 78:237–251

    Article  CAS  Google Scholar 

  • Robert RLG (1979) Growth measurements. Division rate. In: RJ Stein (ed) Physiological methods. Culture methods and growth measurements. Cambridge University. Press, Cambridge, pp 29–311

  • Rocha JM, Gracia JE, Henriques MH (2003) Growth aspects of the marine microalga Nannochloropsis gaditana. Biomol Eng 20(4–6):237–242

    Article  CAS  Google Scholar 

  • Ronquillo JD, Fraser J, McConkey AJ (2012) Effect of mixed microalgal diets on growth and polyunsaturated fatty acid profile of European oyster (Ostrea edulis) juveniles. Aquaculture 360:64–68

    Article  Google Scholar 

  • Scarsella M, Belotti G, De Filippis P, Bravi M (2010) Study on the optimal growing conditions of Chlorella vulgaris in bubble column photobioreactors. Chem Eng 20:85–90

    Google Scholar 

  • Senthil SL, MaruthuPandi T, Kumar TA, Devi KN, Balasubramanian T (2012) Exigent of microalgae for the enrichment of Artemia salina. J Aquacult Feed Sci Nutr 4(2)

  • Shahar S (2014) Biochemical composition and antioxidant capacity of marine microalgae Chlorella salina Butcher and Isochrysis maritima Billard and Gayral isolated from Penang coastal waters (Doctoral dissertation, UniversitiSains Malaysia)

  • Shields RJ, Lupatsch I (2012) Algae for aquaculture and animal feeds. J Anim Sci 21:23–37

    Google Scholar 

  • Sorgeloos P, Dhert P, Candreva P (2001) Use of the brine shrimp, Artemia spp., in marine fish larviculture. Aquaculture 200:147–159

    Article  Google Scholar 

  • Spackman DH, Stein WH, Moore S (1958) Automatic recording apparatus for use in chromatography of amino acids. Anal Chem 30(7):1190–1206

    Article  CAS  Google Scholar 

  • Spolaore P, Joannis-Cassan C, Duran E, Isambert A (2006) Commercial applications of microalgae. J Biosci Bioeng 101(2):87–96

    Article  CAS  Google Scholar 

  • Sudha KSS, Shalma SM, Naveena BE, Prakash S (2013) Effect of nitrogen concentration on growth and lipid content of Chlorella marina and Dunellialla salina for biodiesel production (IJIIT) 2(3):28–32

  • Sun Y, Wang C (2009) The optimal growth conditions for the biomass production of and the effects that phosphorus, Zn, CO, and light intensity have on the biochemical composition of and the activity of extracellular CA. B B E2(14):225–231

    Google Scholar 

  • Wijffels RH, Barbosa MJ (2010) An outlook on microalgal biofuels. Science (Washington) 329(5993):796–799

    Article  CAS  Google Scholar 

  • Wiley PE, Campbell JE, McKuin B (2011) Production of biodiesel and biogas from algae: a review of process train options. WER 83(4):326–338

    Article  CAS  Google Scholar 

  • Wong PK, Chan KY (1980) Algal single cell protein production from sewage effluent with high salinity. Experientia 36(9):1065–1066

    Article  CAS  Google Scholar 

  • Zaki MI, Saad H (2010) Comparative study on growth and survival of larval and juvenile Dicentrarchus labrax rearing on rotifer and Artemia enriched with four different microalgae species. Afr J Biotech 9(24):3676–3688

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Hydrobiology Laboratory, National Institute of Oceanography and Fisheries, Alexandria, Egypt

    Hala Y. El-Kassas & Basma A. ELSherbiny

  2. Botany and Microbiology Department, Faculty of Science, Alexandria University, Alexandria, Egypt

    Nagwa G.-E. Mohammady

  3. Fish Reproduction Laboratory, National Institute of Oceanography and Fisheries, Alexandria, Egypt

    Heba S. El-Sayed

Authors
  1. Hala Y. El-Kassas
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nagwa G.-E. Mohammady
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Heba S. El-Sayed
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Basma A. ELSherbiny
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hala Y. El-Kassas.

Ethics declarations

Conflict of interest

There are no conflicts of interest.

Research involving human participants and/or animals

All procedures followed were in accordance with the ethical and there are no Human Participants or Animals.

Informed consent

Written Informed consent was obtained from all participants.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

El-Kassas, H.Y., Mohammady, N.GE., El-Sayed, H.S. et al. Growth and biochemical variability of complete and lipid extracted Chlorella species (application for Artemia franciscana feeding). Rend. Fis. Acc. Lincei 27, 761–774 (2016). https://doi.org/10.1007/s12210-016-0569-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12210-016-0569-8

Keywords

Search

Navigation