Skip to main content
SpringerLink
Log in

Effects of sodium bicarbonate concentration on growth, photosynthesis, and carbonic anhydrase activity of macroalgae Gracilariopsis lemaneiformis, Gracilaria vermiculophylla, and Gracilaria chouae (Gracilariales, Rhodophyta)

  • Original Article
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

There is potential for bicarbonate to improve crop yields and economic efficiency of marine algae. However, few studies have focused on the effect of bicarbonate on the growth, photosynthesis, and enzyme activity associated with carbon utilization, especially in commercial macroalgae. Here, the addition of bicarbonate (up to 420 mg L−1) to macroalgal cultures has been evaluated for Gracilariopsis lemaneiformis, Gracilaria vermiculophylla, and Gracilaria chouae with respect to growth rate, photosynthetic activity, carbonic anhydrase activity, and biochemical composition. The results showed that the effects of NaHCO3 on growth, chlorophyll a, phycoerythrin, photosynthetic oxygen evolution, photochemical parameters of PSI and PSII, carbonic anhydrase activity, and nitrogen content were significant (P < 0.05) and followed the same pattern in the three species. The parameter values were promoted in lower NaHCO3 concentrations (up to 252 or 336 mg L−1) and inhibited in higher NaHCO3 concentrations (>336 mg L−1 for Gp. lemaneiformis and >420 mg L−1 for the other two species). Moreover, species–specific differences induced by supplementation with bicarbonate were discovered during culture. Optimal concentrations of NaHCO3 used in this study were 252 mg L−1 for Gp. lemaneiformis and 336 mg L−1 for G. vermiculophylla and G. chouae. These results suggest that an adequate supplementation of sodium bicarbonate is a viable strategy for promoting growth and photosynthetic activity in some macroalgae as well as for improving biochemical composition. The study will help to accelerate the growth rate of algae and improve the quality of thalli, and will also be useful for enhancing the understanding of carbon utilization in macroalgae.

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
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Amthor JS (1995) Terrestrial higher-plant response to increasing atmospheric CO2 in relation to the global carbon cycle. Global Change Biol 1:243–274. doi:10.1111/j.1365-2486.1995.tb00025.x

    Article  Google Scholar 

  • Bozzo GG, Colman B, Matsuda Y (2000) Active transport of CO2 and bicarbonate is induced in response to external CO2 concentration in the green alga Chlorella kessleri. J Exp Bot 51:1341–1348. doi:10.1093/jexbot/51.349.1341

    Article  CAS  PubMed  Google Scholar 

  • Chen SY, Qi HS (2008) Photolithotrophic cultivation of Laminaria japonica gametophyte cells in a silicone tubular membrane-aerated photobioreactor. Plant Cell Tissue Organ 93:29–38. doi:10.1007/s11240-008-9339-3

    Article  CAS  Google Scholar 

  • Cosgrove J, Borowitzka MA (2011) Chlorophyll fluorescence terminology: an introduction. In: Sugett D, Prášil O, Borowitzka MA (eds) Chlorophyll a fluorescence in aquatic sciences: methods and applications. 1st edn. Springer, Dordrecht Heidelberg London New York, pp 1–17. doi:10.1007/978-90-481-9268-7

  • Dubinsky Z, Schofield O (2010) From the light to the darkness: thriving at the light extremes in the oceans. Hydrobiologia 639:153–171. doi:10.1007/s10750-009-0026-0

    Article  CAS  Google Scholar 

  • Gao KS, McKinley KR (1994) Use of macroalgae for marine biomass production and CO2 remediation: a review. J Appl Phycol 6:45–60. doi:10.1007/BF02185904

    Article  Google Scholar 

  • Gao S, Chen XY, Yi QQ, Wang GC, Pan GH, Ap Lin, Peng G (2010) A strategy for the proliferation of Ulva prolifera, main causative species of green tides, with formation of sporangia by fragmentation. Plos One 5:e8571. doi:10.1371/journal.pone.0008571

    Article  PubMed  PubMed Central  Google Scholar 

  • Gardner RD et al (2012) Use of sodium bicarbonate to stimulate triacylglycerol accumulation in the chlorophyte Scenedesmus sp. and the diatom Phaeodactylum tricornutum. J Appl Phycol 24:1311–1320. doi:10.1007/s10811-011-9782-0

    Article  CAS  Google Scholar 

  • Giordano M, Maberly SC (1989) Distribution of carbonic anhydrase in British marine macroalgae. Oecologia 81:534–539. doi:10.1007/BF00378965

    Article  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. doi:10.1146/annurev.arplant.56.032604.144052

    Article  CAS  PubMed  Google Scholar 

  • Hsueh HT, Chu H, Yu ST (2007) A batch study on the bio-fixation of carbon dioxide in the absorbed solution from a chemical wet scrubber by hot spring and marine algae. Chemosphere 66:878–886. doi:10.1016/j.chemosphere.2006.06.022

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Jensen A (1978) Chlorophylls and carotenoids. In: Hellebust JA, Craigie JS (eds) Handbook of phycological methods: phycological and biochemical methods. Cambridge University Press, London, pp 59–70

    Google Scholar 

  • Kursar TA, var der Meer JP, Alberte RS (1983) Light-harvesting system of the red alga Gracilaria tekvahiae. I. Biochemical analysis of pigment mutations. Plant Physiol 73:353–360. doi:10.1104/pp.73.2.353

  • Li YX, Zhou S, Zhao FJ, Liu Y, Fan PP, Wang GC (2010) Physiological responses of Porphyra haitanesis to different copper and zinc concentrations. Braz J Oceanogr 58:261–267. doi:10.1590/S1679-87592010000400001

    Article  Google Scholar 

  • Pimolrat P, Direkbusarakom S, Chinajariyawong C, Powtongsook S (2010) The effect of sodium bicarbonate concentrations on growth and biochemical composition of Chaetoceros gracilis Schutt. Kasetsart Univ Fish Res Bull 34:40–47

    Google Scholar 

  • Provasoli L (1968) Media and prospects for the cultivation of marine algae. In: Watanabe A, Hattori A (eds) Cultures and collections of algae. Proceedings of the US-Japan Conference. Japanese Society for Plant Physiology, Hakone, pp 63–75

  • Rivkin RB (1990) Photoadaptation in marine phytoplankton: variations in ribulose 1, 5-bisphosphate activity. Mar Ecol Prog Ser 62:61–72. doi:10.3354/meps062061

    Article  CAS  Google Scholar 

  • Sampath-Wiley P, Neefus CD, Jahnke LS (2008) Seasonal effects of sun exposure and emersion on intertidal seaweed physiology: fluctuations in antioxidant contents, photosynthetic pigments and photosynthetic efficiency in the red alga Porphyra umbilicalis Kützing (Rhodophyta, Bangiales). J Exp Mar Biol Ecol 361:83–91. doi:10.1016/j.jembe.2008.05.001

    Article  CAS  Google Scholar 

  • Taştan BE, Duygu E, Dönmez G (2012) Boron bioremoval by a newly isolated Chlorella sp. and its stimulation by growth stimulators. Water Res 46:167–175. doi:10.1016/j.watres.2011.10.045

    Article  PubMed  Google Scholar 

  • Tortell PD, Reinfelder JR, Morel FMM (1997) Active uptake of bicarbonate by diatoms. Nature 390:243–244. doi:10.1038/36765

    Article  CAS  Google Scholar 

  • Turpin DH, Miller AG, Parslow JS, Elrifi IR, Canvin DT (1985) Predicting the kinetics of dissolved inorganic carbon limited growth from the short-term kinetics of photosynthesis in Synechococcus leopoliensis (Cyanophyta). J Phycol 21:409–418. doi:10.1111/j.0022-3646.1985.00409.x

    Article  CAS  Google Scholar 

  • Van Kooten O, Snel JFH (1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynth Res 25:147–150. doi:10.1007/BF00033156

    Article  PubMed  Google Scholar 

  • Vonshak A, Boussiba S, Abeliovich A, Richmond A (1983) Production of Spirulina biomass: maintenance of monoalgal culture outdoors. Biotechnol Bioeng 25:341–349. doi:10.1002/bit.260250204

    Article  CAS  PubMed  Google Scholar 

  • Wang B, Li Y, Wu N, Lan CQ (2008) CO2 bio-mitigation using microalgae. Appl Microbiol Biotechnol 79:707–718. doi:10.1007/s00253-008-1518-y

    Article  CAS  PubMed  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. doi:10.1007/s10811-012-9849-6

    Article  CAS  Google Scholar 

  • Wilson AJ, Critchley AT (1997) Studies on Gracilaria gracilis (Stackhouse) Steentoft, Farnham and Irvine and Gracilaria aculeata (Hering) Papenfuss from southern Africa. I. The influence of temperature, irradiance, salinity and nitrogen-nutrition on growth. S Afr J Bot 63:465–473. doi:10.1016/S0254-6299(15)30800-0

    Article  Google Scholar 

  • Wu HY, Zou DH, Gao KS (2008) Impacts of increased atmospheric CO2 concentration on photosynthesis and growth of micro-and macro-algae. Sci China Ser C 51:1144–1150. doi:10.1007/s11427-008-0142-5

    Article  Google Scholar 

  • Xu ZG, Zou DH, Gao KS (2010) Effects of elevated CO2 and phosphorus supply on growth, photosynthesis and nutrient uptake in the marine macroalga Gracilaria lemaneiformis (Rhodophyta). Bot Mar 53:123–129. doi:10.1515/BOT.2010.012

    Article  CAS  Google Scholar 

  • Xu D, Qiao HJ, Zhu JY, Xu P, Liang CW, Zhang XW, Ye NH, Yang WX (2012) Assessment of photosynthetic performance of Porphyra yezoensis Ueda (Bangiales, Rhodophyta) in conchocelis phase. J Phycol 48:467–470. doi:10.1111/j.1529-8817.2012.01121.x

    Article  PubMed  Google Scholar 

  • Yu J, Yang YF (2008) Physiological and biochemical response of seaweed Gracilaria lemaneiformis to concentration changes of N and P. J Exp Mar Biol Ecol 367:142–148. doi:10.1016/j.jembe.2008.09.009

    Article  CAS  Google Scholar 

  • Zhou W, Ding HY, Sui ZH, Wang ZX, Wang JG (2014a) Development of a SCAR marker for male gametophyte of Gracilariopsis lemaneiformis based on AFLP technique. Chin J Oceanol Limnol 32:522–526. doi:10.1007/s00343-014-3209-0

    Article  CAS  Google Scholar 

  • Zhou W et al (2014b) Biomass and carbon storage of Gracilariopsis lemaneiformis (Rhodophyta) in Zhanshan Bay, Qingdao, China. Chin J Oceanol Limnol 32:1009–1015. doi:10.1007/s00343-014-3305-1

    Article  CAS  Google Scholar 

  • Zou DH, Gao KS (2009) Effects of elevated CO2 on the red seaweed Gracilaria lemaneiformis (Gigartinales, Rhodophyta) grown at different irradiance levels. Phycologia 48:510–517. doi:10.2216/08-99.1

    Article  CAS  Google Scholar 

  • Zou DH, Gao KS, Xia JR (2003) Photosynthetic utilization of inorganic carbon in the economic brown alga, Hizikia Fusiforme (Sargassaceae) from the South China Sea. J Phycol 39:1095–1100. doi:10.1111/j.0022-3646.2003.03-038.x

    Article  CAS  Google Scholar 

  • Zou D, Xia J, Yang Y (2004) Photosynthetic use of exogenous inorganic carbon in the agarophyte Gracilaria lemaneiformis (Rhodophyta). Aquaculture 237:421–431. doi:10.1016/j.aquaculture.2004.04.020

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the National High Technology Research and Development Program of China (2012AA10A411), the National Special Research Fund for the Non-Profit Marine Sector (201105021-8), and the Technology Innovation Program of Shandong Province (2013CXC80202).

Funding

This study was funded by the National High Technology Research and Development Program of China (Grant number 2012AA10A411), the National Special Research Fund for the Non-Profit Marine Sector (Grant number 201105021-8), and the Technology Innovation Program of Shandong Province (Grant number 2013CXC80202). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Author information

Authors and Affiliations

  1. Key Laboratory of Marine Genetics and Breeding, Ministry of Education, College of Marine Life Sciences, Ocean University of China, Qingdao, Shandong, China

    Wei Zhou, Zhenghong Sui, Jinguo Wang, Yiyi Hu, Zeeshan Niaz, Huihui Wei, Qingwei Du, Chong Peng, Ping Mi & Zhou Que

  2. Department of Aquaculture, Chonnam National University, Yeosu, Jeonnam, 550-749, South Korea

    Kyoung Ho Kang & Hye Ran Hong

  3. Department of Microbiology, Hazara University, Mansehra, Khyber-Pakhtunkhwa, Pakistan

    Zeeshan Niaz

Authors
  1. Wei Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhenghong Sui
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jinguo Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yiyi Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kyoung Ho Kang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hye Ran Hong
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Zeeshan Niaz
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Huihui Wei
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Qingwei Du
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Chong Peng
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Ping Mi
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Zhou Que
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zhenghong Sui.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standards

All samples used in this study were macroalgae and thus did not involve ethical issues.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhou, W., Sui, Z., Wang, J. et al. Effects of sodium bicarbonate concentration on growth, photosynthesis, and carbonic anhydrase activity of macroalgae Gracilariopsis lemaneiformis, Gracilaria vermiculophylla, and Gracilaria chouae (Gracilariales, Rhodophyta). Photosynth Res 128, 259–270 (2016). https://doi.org/10.1007/s11120-016-0240-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-016-0240-3

Keywords

Search

Navigation