Skip to main content

Advertisement

Log in

Efficient use of bicarbonate for mass production and carbon isotopic labelling of the green alga Ulva ohnoi under natural conditions

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

Abstract

Mass aquaculture production of the green seaweed Ulva is advancing under the stimulus of many interesting applications. Increasing the efficiency of carbon use in Ulva mass cultures is important to improve its production and diversify biomass applications. Given the high capacity of Ulva species to use bicarbonate as a C source, mass cultures of Ulva ohnoi carried out under natural conditions and controlled pH were stoichiometrically supplied with sodium bicarbonate on demand. The specific growth rate (average 0.108 ± 0.008 day−1) and the biochemical composition of U. ohnoi remained stable over three consecutive production cycles, in which C conversion from added bicarbonate into net produced biomass ranged between 88.5 ± 4.2 and 95.9 ± 0.9%. C conversion was significantly higher (p < 0.05) than conversion of nitrogen (73.4 to 87.4%) and phosphorus (68.7 to 80.2%). By enriching the total bicarbonate at 4% with H13CO3, the algal isotopic signature δ13C increased from − 7.5 ± 0.38 to 1505 ± 56‰ after 8 days of growth. Uptake of 13C was steady throughout the culturing period and resulted in biomass production estimates very similar to those calculated from the growth rate. The use of bicarbonate in Ulva cultures represents an important improvement in C conversion efficiency. It is also an easy alternative to produce biomass sufficiently enriched in 13C, which is demanded in studies on the nutritional value of algae. Reliable production estimates in mass cultures can be expected from the 13C uptake rate in algae with high bicarbonate utilization capacity.

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

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

Data availability

Data will be made available on reasonable request.

References

  • Acién-Fernández G, Fernández-Sevilla JM, Egorova-Zachernyuk TA, Molina-Grima E (2005) Cost-effective production of 13C, 15N stable isotope-labelled biomass from phototrophic microalgae for various biotechnological applications. Biomol Eng 22:193–200

    Article  PubMed  CAS  Google Scholar 

  • Allen DK, Bates PD, Tjellström H (2015) Tracking the metabolic pulse of plant lipid production with isotopic labeling and flux analyses: past, present and future. Prog Lipid Res 58:97–120

    Article  CAS  PubMed  Google Scholar 

  • Angell AR, Mata L, de Nys R, Paul NA (2014) Variation in amino acid content and its relationship to nitrogen content and growth rate in Ulva ohnoi (Chlorophyta). J Phycol 50:216–226

    Article  CAS  PubMed  Google Scholar 

  • Angell AR, Mata L, de Nys R, Paul NA (2016) The protein content of seaweeds: a universal nitrogen-to-protein conversion factor of five. J Appl Phycol 28:511–524

    Article  CAS  Google Scholar 

  • Bews E, Booher L, Polizzi T, Long C, Kim JH, Edwards MS (2021) Effects of salinity and nutrients on metabolism and growth of Ulva lactuca: implications for bioremediation of coastal watersheds. Mar Pollut Bull 166:112199

    Article  CAS  PubMed  Google Scholar 

  • Björk M, Haglund K, Ramazanov Z, García-Reina G, Pedersén M (1992) Inorganic-carbon assimilation in the green seaweed Ulva rigida C.Ag. (Chlorophyta). Planta 187:152–156

    Article  PubMed  Google Scholar 

  • Braeckman U, Pasotti F, Vázquez S, Zacher K, Hoffmann R, Elvert M, Marchant H, Buckner C, Quartino ML, Cormack WM, Soetaert K, Wenzhöfer F, Vanreusel A (2019) Degradation of macroalgal detritus in shallow coastal Antarctic sediments. Limnol Oceanogr 64:1423–1441

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chi Z, O’Fallon JV, Chen S (2011) Bicarbonate produced from carbon capture for algae culture. Trends Biotechnol 29:537–541

    Article  CAS  PubMed  Google Scholar 

  • Chopin T, Tacon AGJ (2021) Importance of seaweeds and extractive species in global aquaculture production. Rev Fish Sci Aquacult 29:139–148

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Copertino MS, Tormena T, Seeliger U (2009) Biofiltering efficiency, uptake and assimilation rates of Ulva clathrata (Roth) J. Agardh (Chlorophyceae) cultivated in shrimp aquaculture waste water. J Appl Phycol 21:31–45

    Article  CAS  Google Scholar 

  • Coplen TB (2011) Guidelines and recommended terms for expression of stable-isotope-ratio and gas-ratio measurement results. Rapid Commun Mass Spectrom 25:2538–2560

    Article  CAS  PubMed  Google Scholar 

  • Cyrus MD, Bolton JJ, Macey BM (2020) The use of stable isotope ratios δ13C and δ15N to track the incorporation of Ulva and other important dietary ingredients into the gonads of the sea urchin Tripneustes gratilla. Aquacult Nutr 26:174–185

    Article  CAS  Google Scholar 

  • de Farias-Silva CE, Gris B, Sforza E, La Rocca N, Bertucco A (2016) Effects of sodium bicarbonate on biomass and carbohydrate production in Synechococcus PCC 7002. Chem Eng Trans 49:241–246

    Google Scholar 

  • de Kluijver A, Soetaert K, Czerny J, Schulz KG, Boxhammer T, Riebesell U, Middelburg JJ (2013) A 13C labelling study on carbon fluxes in Arctic plankton communities under elevated CO2 levels. Biogeosciences 10:1425–1440

    Article  CAS  Google Scholar 

  • de Paula Silva PH, McBride S, de Nys R, Paul NA (2008) Integrating filamentous ‘green tide’ algae into tropical pond-based aquaculture. Aquaculture 284:74–80

    Article  Google Scholar 

  • Dickson AG, Sabine CL, Christian JR (2007) Guide to best practices for ocean CO2 measurement. PICES Spec Publication 3:191

    Google Scholar 

  • Dijkman NA, Boschker HTS, Middelburg JJ, Kromkamp JC (2009) Group-specific primary production based on stable-isotope labeling of phospholipid-derived fatty acids. Limnol Oceanogr-Meth 7:612–625

    Article  CAS  Google Scholar 

  • Dominguez H, Loret EP (2019) Ulva lactuca, a source of troubles and potential riches. Mar Drugs 17:357

    Article  CAS  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Folch J, Lees M, Sloane-Stanley GH (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509

    Article  CAS  PubMed  Google Scholar 

  • Gamboa-Delgado J, Peña-Rodríguez A, Ricque-Marie D, Cruz-Suárez LE (2011) Assessment of nutrient allocation and metabolic turnover rate in Pacific white shrimp Litopenaeus vannamei co-fed live macroalgae Ulva clathrata and inert feed: dual stable isotope analysis. J Shellfish Res 30:969–978

    Article  Google Scholar 

  • Gao G, Clare AS, Rose C, Caldwell GS (2018) Ulva rigida in the future ocean: potential for carbon capture, bioremediation and biomethane production. GCB Bioenergy 10:39–51

    Article  CAS  Google Scholar 

  • Giordano M, Beardall J, Raven JA (2005) CO2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. Annu Rev Plant Biol 56:99–131

    Article  CAS  PubMed  Google Scholar 

  • Hama T, Miyazaki T, Ogawa Y, Iwakuma T, Takahashi M, Otsuki A, Ichimura S (1983) Measurement of photosynthetic production of a marine phytoplankton population using a stable 13C isotope. Mar Biol 73:31–36

    Article  CAS  Google Scholar 

  • Hardison AK, Canuel EA, Anderson IC, Veuger B (2010) Fate of macroalgae in benthic systems: carbon and nitrogen cycling within the microbial community. Mar Ecol Prog Ser 414:41–55

    Article  CAS  Google Scholar 

  • Helenius L, Budge SM, Johnson CL (2020) Stable isotope labeling reveals patterns in essential fatty acid growth efficiency in a lipid-poor coastal calanoid copepod. Mar Biol 167:178

    Article  CAS  Google Scholar 

  • Hernández I, Fernández-Engo MA, Pérez-Lloréns JL, Vergara JJ (2005) Integrated outdoor culture of two estuarine macroalgae as biofilters for dissolved nutrients from Sparus aurata waste waters. J Appl Phycol 17:557–567

    Article  Google Scholar 

  • Hinga KR, Arthur MA, Pilson MEQ, Whitaker D (1994) Carbon isotope fractionation by marine phytoplankton in culture: the effects of CO2 concentration, pH, temperature, and species. Glob Biochem Cycles 8:91–102

    Article  CAS  Google Scholar 

  • Kang EJ, Han AR, Kim JH, Kim IN, Lee S, Min JO, Nam BR, Choi YJ, Edwards MS, Diaz-Pulido G, Kim C (2021) Evaluating bloom potential of the green-tide forming alga Ulva ohnoi under ocean acidification and warming. Sci Total Environ 769:144443

    Article  CAS  PubMed  Google Scholar 

  • Kim GY, Heo J, Kim HS, Han JI (2017) Bicarbonate-based cultivation of Dunaliella salina for enhancing carbon utilization efficiency. Bioresour Technol 237:72–77

    Article  CAS  PubMed  Google Scholar 

  • Kim GY, Han RK, JI, (2019) The use of bicarbonate for microalgae cultivation and its carbon footprint analysis. Green Chem 21:5053–5062

    Article  CAS  Google Scholar 

  • Larsson C, Axelsson L (1999) Bicarbonate uptake and utilization in marine macroalgae. Eur J Phycol 34:79–86

    Article  Google Scholar 

  • Lawton RJ, Mata L, de Nys R, Paul NA (2013) Algal bioremediation of waste waters from land-based aquaculture using Ulva: selecting target species and strains. PLoS ONE 8:e77344

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Legrand E, Martin S, Leroux C, Riera P (2018) Effect of temperature on an alga-grazer trophic transfer: a dual stable isotope (13C, 15N) labeling experiment. Mar Ecol 39:12495

    Article  CAS  Google Scholar 

  • Lichtenthaler HK, Buschman C (2001) Chlorophylls and carotenoids: measurement and characterization by UV-VIS spectroscopy. Curr Protocols Food Anal Chem 1:F4.3.1-F4.3.8

    Article  Google Scholar 

  • Lohman EJ, Gardner RD, Pedersen T, Peyton BM, Cooksey KE, Gerlach R (2015) Optimized inorganic carbon regime for enhanced growth and lipid accumulation in Chlorella vulgaris. Biotechnol Biofuels 8:82

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • López-Sandoval DC, Delgado-Huertas A, Agustí S (2018) The 13C method as a robust alternative to 14C-based measurements of primary productivity in the Mediterranean Sea. J Plankton Res 40:544–554

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Markou G, Vandamme D, Muylaert K (2014) Microalgal and cyanobacterial cultivation: the supply of nutrients. Water Res 65:186–202

    Article  CAS  PubMed  Google Scholar 

  • Mata L, Schuenhoff A, Santos R (2010) A direct comparison of the performance of the seaweed biofilters, Asparagopsis armata and Ulva rigida. J Appl Phycol 22:639–644

    Article  CAS  Google Scholar 

  • Mata L, Magnusson M, Paul NA, de Nys R (2016) The intensive land-based production of the green seaweeds Derbesia tenuissima and Ulva ohnoi: biomass and bioproducts. J Appl Phycol 28:365–375

    Article  CAS  Google Scholar 

  • Maugendre L, Gattuso JP, de Kluijver A, Soetaert K, van Oevelen D, Middelburg JJ, Gazeau F (2017) Carbon-13 labelling shows no effect of ocean acidification on carbon transfer in Mediterranean plankton communities. Estuar Coast Shelf Sci 186:100–111

    Article  CAS  Google Scholar 

  • Middelburg JJ, Barranguet C, Boschker HTS, Herman PMJ, Moens T, Heip CHR (2000) The fate of intertidal microphytobenthos carbon: an in situ 13C-labeling study. Limnol Oceanogr 45:1224–1234

    Article  CAS  Google Scholar 

  • Miller HL III, Dunton KH (2007) Stable isotope (13C) and O2 micro-optode alternatives for measuring photosynthesis in seaweeds. Mar Ecol Prog Ser 329:85–97

    Article  CAS  Google Scholar 

  • Mokashi K, Shetty V, George SA, Sibi G (2016) Sodium bicarbonate as inorganic carbon source for higher biomass and lipid production integrated carbon capture in Chlorella vulgaris. Arch Life Sci 10:111–117

    Google Scholar 

  • Moutinho S, Linares F, Rodríguez JL, Sousa V, Valente LMP (2018) Inclusion of 10% seaweed meal in diets for juvenile and on-growing life stages of Senegalese sole (Solea senegalensis). J Appl Phycol 30:3589–3601

    Article  CAS  Google Scholar 

  • Msuya FE, Neori A (2008) Effect of water aeration and nutrient load level on biomass yield, N uptake and protein content of the seaweed Ulva lactuca cultured in seawater tanks. J Appl Phycol 20:1021–1031

    Article  CAS  Google Scholar 

  • Murphy S, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36

    CAS  Google Scholar 

  • Nakamura M, Kumagai NH, Tamaoki M, Koichi A, Yuichi I, Nobuyoshi N, Yabe T (2020) Photosynthesis and growth of Ulva ohnoi and Ulva pertusa (Ulvophyceae) under high light and high temperature conditions, and implications for green tide in Japan. Phycol Res 68:152–160

    Article  CAS  Google Scholar 

  • Neori A (2008) Essential role of seaweed cultivation in integrated multi-trophic aquaculture farms for global expansion of mariculture: an analysis. J Appl Phycol 20:567–570

    Article  Google Scholar 

  • Neori A, Cohen I, Gordin H (1991) Ulva lactuca biofilters for marine fishpond effluents II. Growth rate, yield and C:N ratio. Bot Mar 34:483–489

    Article  Google Scholar 

  • Neori A, Bronfman Y, van Rijn J, Guttman L, Krupnik N, Shpigel M, Samocha TM, Davis DA, Qiu X, Abelin P, Israel A (2020) The suitability of Ulva fasciata, Ulva compressa, and Hypnea musciformis for production in an outdoor spray cultivation system, with respect to biomass yield and protein content. J Appl Phycol 32:3183–3197

    Article  CAS  Google Scholar 

  • Oca J, Cremades J, Jiménez P, Pintado J, Masaló I (2019) Culture of the seaweed Ulva ohnoi integrated in a Solea senegalensis recirculating system: influence of light and biomass stocking density on macroalgae productivity. J Appl Phycol 31:2461–2467

    Article  Google Scholar 

  • Pancha I, Chokshi K, Ghosh T, Paliwal C, Maurya R, Mishra S (2015) Bicarbonate supplementation enhanced biofuel production potential as well as nutritional stress mitigation in the microalgae Scenedesmus sp. CCNM 1077. Bioresour Technol 193:315–323

    Article  CAS  PubMed  Google Scholar 

  • Pedersen TC, Gardner RD, Gerlach R, Peyton BM (2018) Assessment of Nannochloropsis gaditana growth and lipid accumulation with increased inorganic carbon delivery. J Appl Phycol 30:2155–2166

    Article  CAS  Google Scholar 

  • Peng L, Zhang Z, Lan CQ, Basak A, Bond N, Ding X, Du J (2017) Alleviation of oxygen stress on Neochloris oleoabundans: effects of bicarbonate and pH. J Appl Phycol 29:143–152

    Article  CAS  Google Scholar 

  • Rautenberger R, Fernández PA, Strittmatter M, Heesch S, Cornwall CE, Hurd CL, Roleda MY (2015) Saturating light and not increased carbon dioxide under ocean acidification drives photosynthesis and growth in Ulva rigida (Chlorophyta). Ecol Evol 5(4):874–888

    Article  PubMed  PubMed Central  Google Scholar 

  • Raven JA, Johnston AM, Kubler JE, Korb RE, McInroy SG, Handley LL, Scrimgeour CM, Walker DI, Beardall J, Vanderklift M, Fredricksen J, Dunton KH (2002) Mechanistic interpretation of carbon isotope discrimination by marine macroalgae and seagrasses. Funct Plant Biol 29:355–378

    Article  CAS  PubMed  Google Scholar 

  • Revilla-Lovano S, Sandoval-Gil JM, Zertuche-González JA, Belando-Torrentes MD, Bernardeau-Esteller J, Rangel-Mendoza LK, Ferreira-Arrieta A, Guzmán-Calderón JM, Camacho-Ibar VM, Muñiz-Salazar R, Avila-López MC (2021) Physiological responses and productivity of the seaweed Ulva ohnoi (Chlorophyta) under changing cultivation conditions in pilot large land-based ponds. Algal Res 56:102316

    Article  Google Scholar 

  • Richmond A (2000) Microalgal biotechnology at the turn of the millennium: a personal view. J Appl Phycol 12:441–451

    Article  Google Scholar 

  • Rossi F, Viejo RM, Duarte L, Vaz-Pinto F, Gestoso I, Olabarria C (2019) Removal of an established invader can change gross primary production of native macroalgae and alter carbon flow in intertidal rock pools. PLoS ONE 14:e0217121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salbitani G, Bolinesi F, Affuso M, Carraturo F, Mangoni O, Carfagna S (2020) Rapid and positive effect of bicarbonate addition on growth and photosynthetic efficiency of the green microalgae Chlorella sorokiniana (Chlorophyta, Trebouxiophyceae). Appl Sci 10:4515

    Article  CAS  Google Scholar 

  • Samanta P, Shin S, Jang S, Song YC, Oh S, Kim JK (2019) Stable carbon and nitrogen isotopic characterization and tracing nutrient sources of Ulva blooms around Jeju coastal areas. Environ Pollut 254:113033

    Article  CAS  PubMed  Google Scholar 

  • Shahar B, Shpigel M, Barkana R, Masasa M, Neori A, Chernov H, Salomon E, Kiflawi M, Guttman L (2020) Changes in metabolism, growth and nutrient uptake of Ulva fasciata (Chlorophyta) in response to nitrogen source. Algal Res 46:101781

    Article  Google Scholar 

  • Shpigel M, Guttman L, Shauli L, Odintsov V, Ben-Ezra D, Harpaz S (2017) Ulva lactuca from an integrated multi-trophic aquaculture (IMTA) biofilter system as a protein supplement in gilthead seabream (Sparus aurata) diet. Aquaculture 481:112–118

    Article  CAS  Google Scholar 

  • Shpigel M, Shauli L, Odintsov V, Ashkenazi N, Ben-Ezra D (2018) Ulva lactuca biofilter from a land-based integrated multi trophic aquaculture (IMTA) system as a sole food source for the tropical sea urchin Tripneustes gratilla elatensis. Aquaculture 496:221–231

    Article  Google Scholar 

  • Shpigel M, Guttman L, Ben-Ezra D, Yu J, Chen S (2019) Is Ulva sp. able to be an efficient biofilter for mariculture effluents? J Appl Phycol 31:2449–2459

    Article  CAS  Google Scholar 

  • Skirrow G (1975) The dissolved gases carbon dioxide. In: Riley JP, Skirrow G (eds) Chemical oceanography. Academic Press, London, pp 1–92

    Google Scholar 

  • Slade R, Bauen A (2013) Micro-algae cultivation for biofuels: cost, energy balance, environmental impacts and future prospects. Biomass Bioenerg 53:29–38

    Article  Google Scholar 

  • Smetacek V, Zingone A (2013) Green and golden seaweed tides on the rise. Nature 504:84–88

    Article  CAS  PubMed  Google Scholar 

  • Srinivasan R, Mageswari A, Subramanian P, Suganthi C, Chaitanyakumar A, Aswini V, Gothandam KM (2018) Bicarbonate supplementation enhances growth and biochemical composition of Dunaliella salina V-101 by reducing oxidative stress induced during macronutrient deficit conditions. Sci Rep 8:6972

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tamburic B, Evenhuis CR, Crosswell JR, Ralph PJ (2018) An empirical process model to predict microalgal carbon fixation rates in photobioreactors. Algal Res 31:334–346

    Article  Google Scholar 

  • Taylor R, Fletcher RL, Raven JA (2001) Preliminary studies on the growth of selected ‘green tide’ algae in laboratory culture: effects of irradiance, temperature, salinity and nutrients on growth rate. Bot Mar 44:327–336

    Article  Google Scholar 

  • Thomas F, Le Duff N, Leroux C, Dartevelle L, Riera P (2020) Isotopic labelling of cultured macroalgae and isolation of 13C-labelled cell wall polysaccharides for trophic investigations. Adv Bot Res 90:1–17.

    Google Scholar 

  • Tsubaki S, Zhu W, Hiraoka M (2017) Production and conversion of green macroalgae (Ulva spp.). In: Kerton FM, Yan N (eds) Fuels chemicals and materials from the oceans and aquatic sources. Wiley, New York, pp 19–41

    Chapter  Google Scholar 

  • Tsubaki S, Nishimura H, Imai T, Onda A, Hiraoka M (2020) Probing rapid carbon fixation in fast-growing seaweed Ulva meridionalis using stable isotope 13C-labelling. Sci Rep 10:20399

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tu Z, Liu L, Lin W, Xie Z, Luo J (2018) Potential of using sodium bicarbonate as external carbon source to cultivate microalga in non-sterile condition. Bioresour Technol 266:109–115

    Article  CAS  PubMed  Google Scholar 

  • van Engeland T, de Kluijver A, Soetaert K, Meysman F, Middelburg JJ (2012) Isotope data improve the predictive capabilities of a marine biogeochemical model. Biogeosci Discuss 9:9453–9486

    Google Scholar 

  • Vizcaíno AJ, Fumanal M, Sáez MI, Martínez TF, Moriñigo MA, Fernández-Díaz C, Anguis V, Balebona MC, Alarcón FJ (2019) Evaluation of Ulva ohnoi as functional dietary ingredient in juvenile Senegalese sole (Solea senegalensis): effects on the structure and functionality of the intestinal mucosa. Algal Res 42:101608

    Article  Google Scholar 

  • White DA, Pagarette A, Rooks P, Ali ST (2013) The effect of sodium bicarbonate supplementation on growth and biochemical composition of marine microalgae cultures. J Appl Phycol 25:153–165

    Article  CAS  Google Scholar 

  • Wolf-Gladrow DA, Zeebe RE, Klaas C, Körtzinger A, Dickson AG (2007) Total alkalinity: the explicit conservative expression and its application to biogeochemical processes. Mar Chem 106:287–300

    Article  CAS  Google Scholar 

  • Ye Z, Abraham J, Christodoulatos C, Prigiobbe V (2019) Mineral carbonation for carbon utilization in microalgae culture. Energ Fuels 33:8843–8851

    Article  CAS  Google Scholar 

  • Zanolla M, Carmona R, Kawai H, Stengel DB, Altamirano M (2019) Role of thermal photosynthetic plasticity in the dispersal and settlement of two global green tide formers: Ulva pertusa and U. ohnoi. Mar Biol 166:123

    Article  Google Scholar 

  • Zheng Q, Xu X, Martin GJ, Kentish SE (2018) Critical review of strategies for CO2 delivery to large-scale microalgae cultures. Chin J Chem Eng 26:2219–2228

    Article  CAS  Google Scholar 

  • Zhu C, Zhang R, Cheng L, Chi Z (2018) A recycling culture of Neochloris oleoabundans in a bicarbonate-based integrated carbon capture and algae production system with harvesting by auto-flocculation. Biotechnol Biofuels 11:204

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zidenga T, Teshima M, Perkins G, Rahn T, Twary S, Heikoop JM (2018) Carbon use efficiency diagnostics in Nannochloropsis salina. Algal Res 31:40–46

    Article  Google Scholar 

Download references

Acknowledgements

The authors are grateful for the valuable help with Ulva mass cultures and biochemical analysis of Eugenia Zuasti, María del Mar Landi and Esperanza García Sumariva.

Funding

This work was supported by the INIA project RTA2014-00023-CO2-01 co-financed with FEDER funds.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to José-Pedro Cañavate.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cañavate, JP., Anguís-Climent, V. & Fernández-Díaz, C. Efficient use of bicarbonate for mass production and carbon isotopic labelling of the green alga Ulva ohnoi under natural conditions. J Appl Phycol 33, 3987–3999 (2021). https://doi.org/10.1007/s10811-021-02567-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-021-02567-0

Keywords