Skip to main content
SpringerLink
Log in

Effects of increased CO2 levels on growth, photosynthesis, ammonium uptake and cell composition in the macroalga Hypnea spinella (Gigartinales, Rhodophyta)

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

Abstract

The red seaweed Hypnea spinella (Gigartinales, Rhodophyta), was cultured at laboratory scale under three different CO2 conditions, non-enriched air (360 ppm CO2) and CO2-enriched air at two final concentrations (750 and 1,600 ppm CO2), in order to evaluate the influence of increased CO2 concentrations on growth, photosynthetic capacity, nitrogen removal efficiency, and chemical cellular composition. Average specific growth rates of H. spinella treated with 750 and 1,600 ppm CO2-enriched air increased by 85.6% and 63.2% compared with non-enriched air cultures. CO2 reduction percentages close to 12% were measured at 750 ppm CO2 with respect to 5% and 7% for cultures treated with air and 1,600 ppm CO2, respectively. Maximum photosynthetic rates were enhanced significantly for high CO2 treatments, showing P max values 1.5-fold higher than that for air-treated cultures. N–NH +4 consumption rates were also faster for algae growing at 750 and 1,600 ppm CO2 than that for non-enriched air cultures. As a consequence of these experimental conditions, soluble carbohydrates increased and soluble protein contents decreased in algae treated with CO2-enriched air. However, internal C and N contents remained constant at the different CO2 concentrations. No significant differences in data obtained with both elevated CO2 treatments, under the assayed conditions, indicate that H. spinella is saturated at dissolved inorganic carbon concentrations close by twice the actual atmospheric levels. The results show that increased CO2 concentrations might be considered a key factor in order to improve intensively cultured H. spinella production yields and carbon and nitrogen bioremediation efficiencies.

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

Similar content being viewed by others

References

  • Andría JR, Pérez-Llorens JL, Vergara J (1999) Mechanisms of inorganic carbon acquisition in Gracilaria gaditana nom. prov. (Rhodophyta). Planta 208:564–573

    Article  Google Scholar 

  • Andría JR, Brun FG, Pérez-Llorens JL, Vergara JJ (2001) Acclimation responses of Gracilaria sp. (Rhodophyta) and Enteromorpha intestinalis (Chlorophyta) to changes in the external inorganic carbon concentration. Bot Mar 44:361–370

    Article  Google Scholar 

  • Axelsson L (1988) Changes in pH as a measure of photosynthesis by marine macroalgae. Mar Biol 97:287–294

    Article  Google Scholar 

  • Beardall J, Beer S, Raven JA (1998) Biodiversity of marine plants in an era of climate change: some predictions based on physiological performance. Bot Mar 41:113–123

    Article  CAS  Google Scholar 

  • Beer S, Koch E (1996) Photosynthesis of seagrasses and marine macroalgae in globally changing CO2 environments. Mar Ecol Prog Ser 141:199–204

    Article  Google Scholar 

  • Bidwell RGS, McLachlan J, Lloyd NDH (1985) Tank cultivation of Irish moss, Chondrus crispus Stackh. Bot Mar 28:87–97

    Article  Google Scholar 

  • Bowes GW (1993) Facing the inevitable: plants and increasing atmospheric CO2. Ann Rev Plant Phys 44:732–762

    Google Scholar 

  • Collins S, Bell G (2004) Phenotypic consequences of 1,000 generations of selection at elevated CO2 in a green alga. Nature 431:566–569

    Article  PubMed  CAS  Google Scholar 

  • Costas S, Gómez-Pinchetti JL, García Reina G (2004) Photosynthetic performance characteristics of seaweed species from Canary Islands with potential interest for intensive culture applications. In: Lorenzo JM, Pajuelo JG, Ramos A (eds) Abstracts XIII Symposio Ibérico de Estudios del Bentos Marino, 73. Oceanográfica, Las Palmas de G.C

    Google Scholar 

  • D’Elia CF, DeBoer J (1978) Nutritional studies of two red algae. II. Kinetics of ammonium and nitrate uptake. J Phycol 14:266–272

    Article  Google Scholar 

  • Doucha J, Straka F, Lívansky K (2005) Utilization of flue gas for cultivation of microalgae (Chlorella sp.) in an outdoor open thin-layer photobioreactor. J Appl Phycol 17:403–412

    Article  Google Scholar 

  • Dowd JE, Riggs DS (1965) A comparison of estimates of Michaelis–Menten kinetic constants from various linear transformations. J Biol Chem 240:863–869

    PubMed  CAS  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

    Article  CAS  Google Scholar 

  • Friedlander M, Levy I (1995) Cultivation of Gracilaria in outdoor tanks and ponds. J Appl Phycol 7:315–324

    Article  Google Scholar 

  • Ganesan M, Thiruppathi S, Jha B (2006) Mariculture of Hypnea musciformis (Wulfen) Lamouroux in South east coast of India. Aquaculture 256:201–211

    Article  Google Scholar 

  • Gao K, McKinley KR (1994) Use of macroalgae for marine biomass production and CO2 remediation: a review. J Appl Phycol 6:45–60

    Article  Google Scholar 

  • Gao K, Aruga Y, Asada K, Ishihara T, Akano T, Kiyohara M (1991) Enhanced growth of the red alga Porphyra yezoensis Ueda in high CO2 concentrations. J Appl Phycol 3:355–362

    CAS  Google Scholar 

  • Gao K, Aruga Y, Asada K, Kiyohara M (1993) Influence of enhanced CO2 on growth and photosyntesis of the red algae Gracilaria sp. and Gracilaria chilensis. J Appl Phycol 5:563–571

    Article  CAS  Google Scholar 

  • Garcia-Sanchez MJ, Fernandez JA, Niell FX (1994) Effect of inorganic carbon supply on the photosyntetic physiology of Gracilaria tenuistipitata. Planta 194:55–61

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Gómez-Pinchetti JL, Ramazanov Z, García-Reina G (1992) Effect of inhibitors of carbonic anhydrase activity on photosynthesis in the red alga Solieria filiformis (Gigartinales: Rhodophyta). Mar Biol 114:335–339

    Article  Google Scholar 

  • Gómez-Pinchetti JL, Suárez Alvarez S, Martel Quintana A, García Reina G (2002) Alternative high-value seaweed species as biofilters for the purification of N–NH +4 enriched fishpond effluents. In: García Guerrero M, Molina Grima E, Acien Fernández FG, Fernández Sevilla JM, Sánchez Pérez JA, Brindley Alias C (eds) Algal biotechnology: a sea of opportunities, 267. Servicio Publicaciones Universidad de Almeria, Almería

    Google Scholar 

  • Gordillo FJL, Niell FX, Figueroa FL (2001) Non-photosynthetic enhancement of growth by high CO2 level in the nitrophilic seaweed Ulva rigida C. Agardh (Chlorophyta). Planta 213:64–70

    Article  PubMed  CAS  Google Scholar 

  • Gordillo FJL, Figueroa FL, Niell FX (2003) Photon- and carbon-use efficiency in Ulva rigida at different CO2 and N levels. Planta 218:315–322

    Article  PubMed  CAS  Google Scholar 

  • Guist GG, Dawes CJ, Castle JR (1982) Mariculture of the red seaweed, Hypnea musciformis. Aquaculture 28:375–384

    Article  Google Scholar 

  • Haglund K, Björk M, Ramazanov Z, García-Reina G, Pedersén M (1992) Role of carbonic anhydrase in photosynthesis and inorganic-carbon assimilation in the red alga Gracilaria tenuistipitata. Planta 187:275–281

    Article  CAS  Google Scholar 

  • Henley WJ (1993) Measurement and interpretation of photosynthetic light-response curves in algae in the context of photoinhibition and diel changes. J Phycol 29:729–739

    Article  Google Scholar 

  • Ho S-H, Chen C-Y, Lee D-J, Chang J-S (2011) Perspectives on microalgal CO2-emission mitigation systems—a review. Biotechnol Adv 29:189–198

    Article  PubMed  CAS  Google Scholar 

  • Huppe HC, Turpin DH (1994) Integration of carbon and nitrogen metabolism in plant and algal cells. Annu Rev Plant Physiol Plant Mol Biol 45:577–607

    CAS  Google Scholar 

  • Israel A, Beer S (1992) Photosynthetic carbon acquisition in the red alga Gracilaria conferta. II. Rubisco carboxylase kinetics, carbonic anhydrase and HCO −3 uptake. Mar Biol 112:697–700

    Article  CAS  Google Scholar 

  • Israel A, Hophy M (2002) Growth, photosynthetic properties and Rubisco activities and amounts of marine macroalgae grown under current and elevated seawater CO2 concentrations. Glob Chang Biol 8:831–840

    Article  Google Scholar 

  • Israel A, Gavrieli J, Glazer A, Friedlander M (2005) Utilization of flue gas from a power plant for tank cultivation of the red seaweed Gracilaria cornea. Aquaculture 249:311–316

    Article  CAS  Google Scholar 

  • Jassby AD, Platt T (1976) Mathematical formulation of the relationship between photosynthesis and light for phytoplankton. Limnol Oceanogr 21:540–547

    Article  CAS  Google Scholar 

  • Johnston AM, Raven JA (1990) Effects of culture in high CO2 on the photosynthetic physiology of Fucus serratus. Br Phycol J 25:513–515

    Google Scholar 

  • Keffer JE, Kleinheinz GT (2002) Use of Chlorella vulgaris for CO2 mitigation in a photobioreactor. J Ind Microbiol Biotechnol 29:275–280

    Article  PubMed  CAS  Google Scholar 

  • Kübler JA, Johnston AM, Raven JA (1999) The effects of reduced and elevated CO2 and O2 on the seaweed Lomentaria articulata. Plant Cell Environ 22:1303–1310

    Article  Google Scholar 

  • Laws EA, Berning JL (1991) Photosynthetic efficiency optimization studies with the macroalga Gracilaria tikvahiae: implications for CO2 emission control from power plants. Biores Technol 37:25–33

    Article  CAS  Google Scholar 

  • Levavasseur G, Edwards GE (1991) Inorganic carbon limitation of photosynthesis in Ulva rotundata (Chlorophyta). J Phycol 27:667–672

    Article  Google Scholar 

  • Maberly SC (1990) Exogenous sources of inorganic carbon for photosynthesis by marine macroalgae. J Phycol 26:439–449

    Article  CAS  Google Scholar 

  • Mercado JM, Niell FX (2000) Carbon dioxide uptake by Bostrychia scorpioides (Rhodophyceae) under emersed conditions. Eur J Phycol 35:45–51

    Article  Google Scholar 

  • Mercado JM, Gordillo FJ, Niell FX, Figueroa FL (1999) Effects of different levels of CO2 on photosynthesis and cell components of the red alga Porphyra leucosticta. J Appl Phycol 11:455–461

    Article  Google Scholar 

  • Murru M, Sandgren CD (2004) Habitat matters for inorganic carbon acquisition in 38 species of red macroalgae (Rhodophyta) from Puget Sound, Washington, USA. J Phycol 40:837–845

    Article  CAS  Google Scholar 

  • Neori A, Chopin T, Troell M, Buschmann AH, Kraemer P, Halling C, Shipigel M, Yarish C (2004) Integrated aquaculture: rationale, evolution and state of the art emphasizing seaweed biofiltration in modern mariculture. Aquaculture 231:361–391

    Article  Google Scholar 

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

    Google Scholar 

  • Raven J (1997) Putting the C in phycology. Eur J Phycol 32:319–333

    Article  Google Scholar 

  • Raven J, Falkowski PG (1999) Oceanic sinks for atmospheric CO2. Plant Cell Env 22:741–755

    Article  CAS  Google Scholar 

  • Smith RG, Bidwell RGS (1989) Mechanism of photosynthetic carbon dioxide uptake by the red macroalga, Chondrus crispus. Plant Physiol 89:93–99

    Article  PubMed  CAS  Google Scholar 

  • Stitt M, Krapp A (1999) The interaction between elevated carbon dioxide and nitrogen nutrition: the physiological and molecular background. Plant Cell Env 22:583–621

    Article  CAS  Google Scholar 

  • Stumm W, Morgan JJ (1981) Aquatic chemistry. An introduction emphasizing chemical equilibria in natural waters. Wiley, New York

    Google Scholar 

  • Troell M, Halling C, Neori A, Chopin T, Buschmann AH, Kautsky N, Yarish C (2003) Integrated mariculture: asking the right questions. Aquaculture 226:69–90

    Article  Google Scholar 

  • Viera MP, Gómez Pinchetti JL, Courtois de Vicose G, Bilbao A, Suárez Alvarez S, Haroun RJ, Izquierdo M (2005) Suitability of three red macroalgae as a feed for the abalone Haliotis tuberculata coccinea Reeve. Aquaculture 248:75–82

    Article  Google Scholar 

  • Wu H, Zou D, Gao K (2008) Impacts of increased atmospheric CO2 concentrations on photosynthesis and growth of micro- and macro-algae. Sci China C Life Sci 51:1144–1150

    Article  PubMed  Google Scholar 

  • Xu Z, Zou D, Gao K (2010) Effects if elevated CO2 and phosphorus supply on growth, photosynthesis and nutrient uptake in the marine macroalga Gracilaria lemaneiformis (Rhodophyta). Bot Mar 53:123–129

    Article  CAS  Google Scholar 

  • Zou D (2005) Effects of elevated atmospheric CO2 on growth, photosynthesis and nitrogen metabolism in the economic brown seaweed, Hizikia fusiforme (Sargassaceae, Phaeophyta). Aquaculture 250:726–735

    Article  CAS  Google Scholar 

  • Zou D, Gao K (2009) Effects of elevated CO2 on the red seaweed Gracilaria lemaneiformis (Gigartinales, Rhodophyta) growth at different irradiance levels. Phycologia 48:510–517

    Article  CAS  Google Scholar 

Download references

Acknowledgments

S.S.A. is granted by the Canarian Government (IDT-LP-04/023). The authors are thankful to Prof. Angel Santana (ULPGC) for helpful comments on statistics.

Author information

Authors and Affiliations

  1. Grupo de Algología Aplicada, Centro de Biotecnología Marina, Universidad de Las Palmas de G.C, Muelle de Taliarte s/n, 35214 Telde, Gran Canaria, Canary Islands, Spain

    Sonia Suárez-Álvarez, Juan Luis Gómez-Pinchetti & Guillermo García-Reina

Authors
  1. Sonia Suárez-Álvarez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Juan Luis Gómez-Pinchetti
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Guillermo García-Reina
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sonia Suárez-Álvarez.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Suárez-Álvarez, S., Gómez-Pinchetti, J.L. & García-Reina, G. Effects of increased CO2 levels on growth, photosynthesis, ammonium uptake and cell composition in the macroalga Hypnea spinella (Gigartinales, Rhodophyta). J Appl Phycol 24, 815–823 (2012). https://doi.org/10.1007/s10811-011-9700-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-011-9700-5

Keywords

Search

Navigation