Abstract
The nutritional value of the marine cryptophyte Rhodomonas lens for the filter feeder Brachionus plicatilis as well as its biotechnological potential as a source of phycoerythrin (PE) and polyunsaturated fatty acids (PUFA) were evaluated in semi-continuous cultures maintained with different daily renewal rates (RR), from 10% (R10) to 50% (R50) of the total volume. Steady-state cell density decreased from 22 to 7 × 106 cells mL−1 with increasing RR, with the maximum cell productivity, nearly 0.4 g L−1 day−1, observed with R40. PE cell content attained the highest values with the highest RR (circa 9 pg cell−1). All treatments of R. lens maintained under nitrate-saturated conditions (R20-R50) showed a similar high content of PUFAs, > 60% of total fatty acids (FA), with linolenic acid (18:3n-3) and 18:4n-3, representing 12 and 29% of total FA respectively. The PUFA level in the nitrogen-limited R10 cultures was significantly lower (37%). R. lens promoted higher weight gain in the rotifer B. plicatilis than Tisochrysis lutea (T-ISO), a species commonly used for rotifer culture and enrichment. Significant differences were found in the protein content and in the ratio n-3/n-6 fatty acids among rotifers fed with R. lens from different RRs, with higher values being found in those fed with R. lens from higher RRs. The enrichment of the rotifers for short periods of 3 h was sufficient to modify the biochemical composition of the rotifers, but it was evidenced as too short for the accumulation of PUFAs, when compared to long-term (24 h) enrichment. The rotifers reflected the higher protein and PUFA content of R. lens cultivated with nutrient sufficient microalgae (R40) after only 3 h of enrichment. These results demonstrate that semi-continuous culture of R. lens under appropriate conditions can strongly enhance the nutritional value of this species, being reflected in the growth and biochemical composition of the filter feeder, even in short exposure periods.
Similar content being viewed by others
References
Bartual A, Lubián LM, Gálvez JA, Niell FX (2002) Effect of irradiance on growth, photosynthesis, pigment content and nutrient consumption in dense cultures of Rhodomonas salina (Wislouch) (Cryptophyceae). Cienc Mar 28:381–392
Bennett A, Bogorad L (1973) Complementary chromatic adaptation in a filamentous blue-green alga. J Cell Biol 58:419–435
Bermúdez J, Rosales N, Loreto C et al (2004) Exopolysaccharide, pigment and protein production by the marine microalga Chroomonas sp. in semicontinuous cultures. World J Microbiol Biotechnol 20:179–183
Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917
Borowitzka MA (1997) Microalgae for aquaculture: opportunities and constraints. J Appl Phycol 9:393–401
Brown MR, McCausland MA, Kowalski K (1998) The nutritional value of four Australian microalgal strains fed to Pacific oyster Crassostrea gigas spat. Aquaculture 165:281–293
Bryant DA, Guglielmi G, de Marsac NT et al (1979) The structure of cyanobacterial phycobilisomes: a model. Arch Microbiol 123:113–127
Chaloub RM, Motta NMS, de Araujo SP et al (2015) Combined effects of irradiance, temperature and nitrate concentration on phycoerythrin content in the microalga Rhodomonas sp. (Cryptophyceae). Algal Res 8:89–94
Collos Y, Mornet F, Sciandra A, Waser N, Larson A, Harrison PJ (1999) An optical method for the rapid measurement of micromolar concentrations of nitrate in marine phytoplankton cultures. J Appl Phycol 11:179–184
Costard GS, Machado RR, Barbarino E et al (2012) Chemical composition of five marine microalgae that occur on the Brazilian coast. Int J Fish Aquac 4:191–201
Coutteau P, Geurden I, Camara MR et al (1997) Review on the dietary effects of phospholipids in fish and crustacean larviculture. Aquaculture 155:149–164
da Silva AF, Lourenço SO, Chaloub RM (2009) Effects of nitrogen starvation on the photosynthetic physiology of a tropical marine microalga Rhodomonas sp. (Cryptophyceae). Aquat Bot 91:291–297
Dunstan GA, Brown MR, Volkman JK (2005) Cryptophyceae and rhodophyceae; chemotaxonomy, phylogeny, and application. Phytochemistry 66:2557–2570
Eriksen N, Iversen J (1995) Photosynthetic pigments as nitrogen stores in the cryptophyte alga Rhodomonas sp. J Mar Biotechnol 9:193–195
Eryalçın KM (2018) Effects of different commercial feeds and enrichments on biochemical composition and fatty acid profile of rotifer (Brachionus plicatilis, Müller 1786) and Artemia franciscana. Turk J Fish Aquat Sci 18:81–90
Eryalçın K M (2019) Nutritional value and production performance of the rotifer Brachionus plicatilis Müller, 1786 cultured with different feeds at commercial scale. Aquaculture Int 27:875–890
Estévez A, Giménez G (2017) Optimization of emulsion properties and enrichment conditions used in live prey enrichment. Aquac Nutr 23:1264–1273
Fabregas J, Abalde J, Herrero C et al (1984) Growth of the marine microalga Tetraselmis suecica in batch cultures with different salinities and nutrient concentrations. Aquaculture 42:207–215
Fábregas J, García D, Morales E et al (1998) Renewal rate of semicontinuous cultures of the microalga Porphyridium cruentum modifies phycoerythrin, exopolysaccharide and fatty acid productivity. J Ferment Bioeng 86:477–481
Ferreira M, Maseda A, Fábregas J, Otero A (2008) Enriching rotifers with “premium” microalgae. Isochrysis aff. galbana clone T-ISO. Aquaculture 279:126–130
Ferreira M, Coutinho P, Seixas P, Fábregas J, Otero A (2009) Enriching rotifers with “premium” microalgae. Nannochloropsis gaditana. Mar Biotechnol 11:585–595
Ferreira M, Seixas P, Coutinho P, Fábregas J, Otero A (2011) Effect of the nutritional status of semi-continuous microalgal cultures on the productivity and biochemical composition of Brachionus plicatilis. Mar Biotechnol 13:1074–1085
Ferreira M, Cortina-Burgueño Á, Freire I, Otero A (2018) Effect of nutritional status and concentration of Nannochloropsis gaditana as enrichment diet for the marine rotifer Brachionus sp. Aquaculture 491:351–357
Glazer AN (1994) Phycobiliproteins — a family of valuable, widely used fluorophores. J Appl Phycol 6:105–112
Glazer AN, Stryer L (1984) Phycofluor probes. Trends Biochem Sci 9:423–427
Greenwold MJ, Cunningham BR, Lachenmyer EM, Pullman JM, Richardson TL, Dudycha JL (2019) Diversification of light capture ability was accompanied by the evolution of phycobiliproteins in cryptophyte algae. Proc R Soc B 286:20190655
Guevara M, Bastardo L, Cortez R, et al (2011) Pastas de Rhodomonas salina (Cryptophyta) como alimento para Brachionus plicatilis (Rotifera)
Guevara M, Arredondo-Vega BO, Palacios Y, Saéz K, Gómez PI (2016) Comparison of growth and biochemical parameters of two strains of Rhodomonas salina (Cryptophyceae) cultivated under different combinations of irradiance, temperature, and nutrients. J Appl Phycol 28:2651–2660
Guiry MD, Guiry GM (2019) No title. In: AlgaeBase. World-wide electron. Publ. Natl. Univ. Ireland, Galway. http://www.algaebase.org. Accessed 20 June 2019
Humphrey GF (1979) Photosynthetic characteristics of algae grown under constant illumination and light-dark regimes. J Exp Mar Biol Ecol 40:63–70
Izquierdo MS (1996) Essential fatty acid requirements of cultured marine fish larvae. Aquac Nutr 2:183–191
Jeffrey ST, Humphrey GF (1975) New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton. Biochem Physiol Pflanz 167:191–194
Knuckey RM, Semmens GL, Mayer RJ, Rimmer MA (2005) Development of an optimal microalgal diet for the culture of the calanoid copepod Acartia sinjiensis: effect of algal species and feed concentration on copepod development. Aquaculture 249:339–351
Kochert G (1978) Carbohydrate determination by the phenol-sulfuric acid method. In: Hellebust J, Craigie J (eds) Handbook of phycological methods. Physiological and biochemical methods. Cambridge University Press, London, pp 95–97
Koski M, Klein Breteler W, Schogt N (1998) Effect of food quality on rate of growth and development of the pelagic copepod Pseudocalanus elongatus (Copepoda, Calanoida). Mar Ecol Prog Ser 170:169–187
Lafarga-De la Cruz F, Valenzuela-Espinoza E, Millán-Núñez R et al (2006) Nutrient uptake, chlorophyll a and carbon fixation by Rhodomonas sp. (Cryptophyceae) cultured at different irradiance and nutrient concentrations. Aquac Eng 35:51–60
Li K, Kjørsvik E, Bergvik M, Olsen Y (2015) Manipulation of the fatty acid composition of phosphatidylcholine and phosphatidylethanolamine in rotifers Brachionus Nevada and Brachionus Cayman. Aquac Nutr 21:85–97
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275
Ludwig M, Gibbs SP (1989) Localization of phycoerythrin at the lumenal surface of the thylakoid membrane in Rhodomonas lens. J Cell Biol 108:875–884
Marsh JB, Weinstein DB (1966) Simple charring method for determination of lipids. J Lipid Res 7:574–576
McKinnon AD, Duggan S, Nichols PD et al (2003) The potential of tropical paracalanid copepods as live feeds in aquaculture. Aquaculture 223:89–106
Mejias C, Riquelme C, Sayes C, Plaza J, Silva-Aciares F (2018) Production of the rotifer Brachionus plicatilis (Müller 1786) in closed outdoor systems fed with the microalgae Nannochloropsis gaditana and supplemented with probiotic bacteria Pseudoalteromonas sp. (SLP1). Aquac Int 26:869–884
Muller-Feuga A (2000) The role of microalgae in aquaculture: situation and trends. J Appl Phycol 12:527–534
Novarino G (2012) Cryptomonad taxonomy in the 21 st century: the first two hundred years. In: Cryptomonad taxonomy in the 21st century: the first two hundred years. Psychological reports: current advances in algal taxonomy and its applications: phylogenetic, ecological and applied perspective. Institute of Botany, Polish Academy of Sciences, Kraków. pp 19–52
Ohs CL, Chang KL, Grabe SW et al (2010) Evaluation of dietary microalgae for culture of the calanoid copepod Pseudodiaptomus pelagicus. Aquaculture 307:225–232
Otero A, Fábregas J (1997) Changes in the nutrient composition of Tetraselmis suecica cultured semicontinuously with different nutrient concentrations and renewal rates. Aquaculture 159:111–123
Otero A, García D, Fábregas J (1997a) Factors controlling eicosapentaenoic acid production in semicontinuous cultures of marine microalgae. J Appl Phycol 9:465–469
Otero A, García D, Morales ED et al (1997b) Manipulation of the biochemical composition of the eicosapentaenoic acid-rich microalga Isochrysis galbana in semicontinuous cultures. Biotechnol Appl Biochem 26:171–177
Otero A, Domínguez A, Lamela T et al (1998) Steady-states of semicontinuous cultures of a marine diatom: effect of saturating nutrient concentrations. J Exp Mar Biol Ecol 227:23–33
Parrish CC, French VM, Whiticar MJ (2012) Lipid class and fatty acid composition of copepods (Calanus finmarchicus, C. glacialis, Pseudocalanus sp., Tisbe furcata and Nitokra lacustris) fed various combinations of autotrophic and heterotrophic protists. J Plankton Res 34:356–375
Patiño M (1995) Nutrición de Brachionus plicatilis y Artemia sp. con microalgas marinas. Universidad de Santiago de Compostela
Peltomaa E, Johnson M, Taipale S (2017) Marine cryptophytes are great sources of EPA and DHA. Mar Drugs 16:3
Phwan CK, Ong HC, Chen WH et al (2018) Overview: comparison of pretreatment technologies and fermentation processes of bioethanol from microalgae. Energy Convers Manag 173:81–94
Pulz O, Gross W (2004) Valuable products from biotechnology of microalgae. Appl Microbiol Biotechnol 65:635–648
Raghav Sonani R, Prasad Rastogi R, Patel R et al (2016) Recent advances in production, purification and applications of phycobiliproteins. World J Biol Chem 7:100–109
Renaud SM, Thinh L-V, Parry DL (1999) The gross chemical composition and fatty acid composition of 18 species of tropical Australian microalgae for possible use in mariculture. Aquaculture 170:147–159
Renaud SM, Thinh L-V, Lambrinidis G, Parry DL (2002) Effect of temperature on growth, chemical composition and fatty acid composition of tropical Australian microalgae grown in batch cultures. Aquaculture 211:195–214
Rodriguez C, Perez JA, Lorenzo A, Cejas JR (1994) Comparative nutrition papers n-3 HUFA requirement of larval gilthead seabream Sparus aurata when using high levels of eicosapentaenoic acid. Camp Biochem Physiol 107:693–698
Sales R, Derner RB, Tsuzuki MY (2019) Effects of different harvesting and processing methods on Nannochloropsis oculata concentrates and their application on rotifer Brachionus sp. cultures. J Appl Phycol. https://doi.org/10.1007/s10811-019-01877-8
Sathasivam R, Radhakrishnan R, Hashem A, Abd_Allah EF (2019) Microalgae metabolites: a rich source for food and medicine. Saudi J Biol Sci 26:709–722
Sato N, Murata N (1988) [24] Membrane lipids. Methods Enzymol 167:251–259
Seixas P, Coutinho P, Ferreira M, Otero A (2009) Nutritional value of the cryptophyte Rhodomonas lens for Artemia sp. J Exp Mar Biol Ecol. https://doi.org/10.1016/j.jembe.2009.09.007
Sekar S, Chandramohan M (2008) Phycobiliproteins as a commodity: trends in applied research, patents and commercialization. J Appl Phycol 20:113–136
Spolaore P, Joannis-Cassan C, Duran E, Isambert A (2006) Commercial applications of microalgae. J Biosci Bioeng 101:87–96
Thépot V, Mangott A, Pirozzi I (2016) Rotifers enriched with a mixed algal diet promote survival, growth and development of barramundi larvae, Lates calcarifer (Bloch). Aquacult Rep 3:147–158
Thoisen C, Vu MTT, Carron-Cabaret T, Jepsen PM, Nielsen SL, Hansen BW (2018) Small-scale experiments aimed at optimization of large-scale production of the microalga Rhodomonas salina. J Appl Phycol 30:2193–2202
Thomas EN, Lonsmann IJJ (1995) Photosynthetic pigments as nitrogen stores in the cryptophyte alga Rhodomonas sp. J Mar Biotechnol 3:193–195
Tremblay R, Cartier S, Miner P et al (2007) Effect of Rhodomonas salina addition to a standard hatchery diet during the early ontogeny of the scallop Pecten maximus. Aquaculture 262:410–418
Utting SD, Helm MM (1985) Improvement of sea water quality by physical and chemical pre-treatment in a bivalve hatchery. Aquaculture 44:133–144
Valenzuela-Espinoza E, Lafarga-De-La-Cruz F, Millán-Nuñez R, Núñez-Cebrero F (2005) Growth, nutrient uptake and proximate composition of Rhodomonas sp. cultured using f/2 medium and agricultural fertilizers. Cienc Mar 31:79–89
Vu MTT, Douëtte C, Rayner TA, Thoisen C, Nielsen SL, Hansen BW (2016) Optimization of photosynthesis, growth, and biochemical composition of the microalga Rhodomonas salina—an established diet for live feed copepods in aquaculture. J Appl Phycol 28:1485–1500
Wenzel A, Bergstrom A-K, Jansson M, Vrede T (2012) Survival, growth and reproduction of Daphnia galeata feeding on single and mixed Pseudomonas and Rhodomonas diets. Freshw Biol 57:835–846
Wijffels RH, Barbosa MJ (2010) An outlook on microalgal biofuels. Science 329:796–799
Yamamoto S, Yamato R, Yoshimatsu T (2018) Optimum culture conditions of Rhodomonas sp. Hf-1 strain as a live food for aquatic animals. Fish Sci 84:691–697
Zhang J, Wu C, Pellegrini D et al (2013) Effects of different monoalgal diets on egg production, hatching success and apoptosis induction in a Mediterranean population of the calanoid copepod Acartia tonsa (Dana). Aquaculture 400–401:65–72
Funding
This work was supported by the grant “Axudas do Programa de Consolidación e Estructuración de Unidades de Investigación Competitivas (GPC)” from the Consellería de Cultura, Educación e Ordenación Universitaria, Xunta de Galicia (ED431B2017/53).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare that there is no conflict of interest.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic Supplementary Material
ESM 1
(PDF 144 kb)
Rights and permissions
About this article
Cite this article
Coutinho, P., Ferreira, M., Freire, I. et al. Enriching Rotifers with “Premium” Microalgae: Rhodomonas lens. Mar Biotechnol 22, 118–129 (2020). https://doi.org/10.1007/s10126-019-09936-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10126-019-09936-4