Skip to main content

Advertisement

Springer Nature Link
Log in

Expression and characterization of a codon-optimized alkaline-stable carbonic anhydrase from Aliivibrio salmonicida for CO2 sequestration applications

  • Research Paper
  • Published:
Bioprocess and Biosystems Engineering Aims and scope Submit manuscript

Abstract

The CO2 mineralization process, accelerated by carbonic anhydrase (CA) was proposed for the efficient capture and storage of CO2, the accumulation of which in the atmosphere is the main cause of global warming. Here, we characterize a highly stable form of the cloned CA from the Gram-negative marine bacterium Aliivibrio salmonicida, named ASCA that can promote CO2 absorption in an alkaline solvent required for efficient carbon capture. We designed a mature form of ASCA (mASCA) using a codon optimization of ASCA gene and removal of ASCA signal peptide. mASCA was highly expressed (255 mg/L) with a molecular weight of approximately 26 kDa. The mASCA enzyme exhibited stable esterase activity within a temperature range of 10–60 °C and a pH range of 6–11. mASCA activity remained stable for 48 h at pH 10. We also investigated its inhibition profiles using inorganic anions, such as acetazolamide, sulfanilamide, iodide, nitrate, and azide. We also demonstrate that mASCA is capable of catalyzing the conversion of CO2 to CaCO3 (calcite form) in the presence of Ca2+. It should be noted that mASCA enzyme exhibits high production yield and sufficient stabilities against relatively high temperature and alkaline pH, which are required conditions for the development of more efficient enzymatic CCS systems.

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

Access this article

Log in via an institution

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Explore related subjects

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

References

  1. Kupriyanova E, Villarejo A, Markelova A, Gerasimenko L, Zavarzin G, Samuelsson G, Los DA, Pronina N (2007) Extracellular carbonic anhydrases of the stromatolite-forming cyanobacterium Microcoleus chthonoplastes. Microbiology 153:1149–1156

    Article  CAS  Google Scholar 

  2. Yang H, Xu Z, Fan M, Gupta R, Slimane RB, Bland AE, Wright I (2008) Progress in carbon dioxide separation and capture: a review. J Environ Sci 20:14–27

    Article  CAS  Google Scholar 

  3. Puxty G, Rowland R, Allport A, Yang Q, Bown M, Burns R, Maeder M, Attalla M (2009) Carbon dioxide postcombustion capture: a novel screening study of the carbon dioxide absorption performance of 76 amines. Environ Sci Technol 43:6427–6433

    Article  CAS  Google Scholar 

  4. Barbero R, Carnelli L, Simon A, Kao A, Monforte AD, Ricco M, Bianchi D, Belcher A (2013) Engineered yeast for enhanced CO mineralization. Energy Environ Sci 6:660–674

    Article  CAS  Google Scholar 

  5. Jo BH, Kim IG, Seo JH, Kang DG, Cha HJ (2013) Engineered Escherichia coli with periplasmic carbonic anhydrase as a biocatalyst for CO2 sequestration. Appl Environ Microbiol 79:6697–6705

    Article  CAS  Google Scholar 

  6. Jo BH, Seo JH, Cha HJ (2014) Bacterial extremo-alpha-carbonic anhydrases from deep-sea hydrothermal vents as potential biocatalysts for CO2 sequestration. J Mol Catal B-Enzym 109:31–39

    Article  CAS  Google Scholar 

  7. Satoh A, Iwasaki T, Odani S, Shiraiwa Y (1998) Purification, characterization and cDNA cloning of soluble carbonic anhydrase from Chlorella sorokiniana grown under ordinary air. Planta 206:657–665

    Article  CAS  Google Scholar 

  8. Puskas LG, Inui M, Zahn K, Yukawa H (2000) A periplasmic, alpha-type carbonic anhydrase from Rhodopseudomonas palustris is essential for bicarbonate uptake. Microbiology 146(Pt 11):2957–2966

    Article  CAS  Google Scholar 

  9. Vandenberg JI, Carter ND, Bethell HW, Nogradi A, Ridderstrale Y, Metcalfe JC, Grace AA (1996) Carbonic anhydrase and cardiac pH regulation. Am J Physiol 271:C1838–C1846

    CAS  Google Scholar 

  10. Badger MR, Price GD (1992) The CO2 concentrating mechanism in cyanobacteria and microalgae. Physiol Plantarum 84:606–615

    Article  CAS  Google Scholar 

  11. De Luca V, Del Prete S, Carginale V, Vullo D, Supuran CT, Capasso C (2015) A failed tentative to design a super carbonic anhydrase having the biochemical properties of the most thermostable CA (SspCA) and the fastest (SazCA) enzymes. J Enzyme Inhib Med Chem 30:989–994

    Article  Google Scholar 

  12. Del Prete S, Vullo D, De Luca V, AlOthman Z, Osman SM, Supuran CT, Capasso C (2014) Biochemical characterization of recombinant β-carbonic anhydrase (PgiCAb) identified in the genome of the oral pathogenic bacterium Porphyromonas gingivalis. J Enzyme Inhib Med Chem 30:366–370

    Article  Google Scholar 

  13. Capasso C, Supuran CT (2015) An overview of the alpha-, beta- and gamma-carbonic anhydrases from Bacteria: can bacterial carbonic anhydrases shed new light on evolution of bacteria? J Enzyme Inhib Med Chem 30:325–332

    Article  CAS  Google Scholar 

  14. Ferry JG (2010) The gamma class of carbonic anhydrases. Biochim Biophys Acta 1804:374–381

    Article  CAS  Google Scholar 

  15. Kim IG, Jo BH, Kang DG, Kim CS, Choi YS, Cha HJ (2012) Biomineralization-based conversion of carbon dioxide to calcium carbonate using recombinant carbonic anhydrase. Chemosphere 87:1091–1096

    Article  CAS  Google Scholar 

  16. Luca VD, Vullo D, Scozzafava A, Carginale V, Rossi M, Supuran CT, Capasso C (2013) An alpha-carbonic anhydrase from the thermophilic bacterium Sulphurihydrogenibium azorense is the fastest enzyme known for the CO2 hydration reaction. Bioorg Med Chem 21:1465–1469

    Article  CAS  Google Scholar 

  17. Smith KS, Ferry JG (2000) Prokaryotic carbonic anhydrases. FEMS Microbiol Rev 24:335–366

    Article  CAS  Google Scholar 

  18. Szilagyi A, Zavodszky P (2000) Structural differences between mesophilic, moderately thermophilic and extremely thermophilic protein subunits: results of a comprehensive survey. Structure 8:493–504

    Article  CAS  Google Scholar 

  19. Frost SC, McKenna R (eds) (2014) Carbonic anhydrase: mechanism, regulation, links to disease, and industrial applications. Springer, New York

  20. Premkumar L, Bageshwar UK, Gokhman I, Zamir A, Sussman JL (2003) An unusual halotolerant alpha-type carbonic anhydrase from the alga Dunaliella salina functionally expressed in Escherichia coli. Protein Expres Purif 28:151–157

    Article  CAS  Google Scholar 

  21. Kanth BK, Jun SY, Kumari S, Pack SP (2014) Highly thermostable carbonic anhydrase from Persephonella marina EX-H1: its expression and characterization for CO2-sequestration applications. Process Biochem 49:2114–2121

    Article  CAS  Google Scholar 

  22. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  Google Scholar 

  23. Verpoorte JA, Mehta S, Edsall JT (1967) Esterase activities of human carbonic anhydrases B and C. J Biol Chem 242:4221–4229

    CAS  Google Scholar 

  24. Rickli EE, Ghazanfar SA, Gibbons BH, Edsall JT (1964) Carbonic anhydrases from human erythrocytes. preparation and properties of two enzymes. J Biol Chem 239:1065–1078

    CAS  Google Scholar 

  25. Sharma A, Bhattacharya A (2010) Enhanced biomimetic sequestration of CO2 into CaCO3 using purified carbonic anhydrase from indigenous bacterial strains. J Mol Catal B-Enzym 67:122–128

    Article  CAS  Google Scholar 

  26. Ki MR, Min K, Kanth BK, Lee J, Pack SP (2013) Expression, reconstruction and characterization of codon-optimized carbonic anhydrase from Hahella chejuensis for CO2 sequestration application. Bioprocess Biosyst Eng 36:375–381

    Article  CAS  Google Scholar 

  27. Kanth BK, Min K, Kumari S, Jeon H, Jin ES, Lee J, Pack SP (2012) Expression and characterization of codon-optimized carbonic anhydrase from Dunaliella species for CO2 sequestration application. Appl Biochem Biotech 167:2341–2356

    Article  CAS  Google Scholar 

  28. Borchert MS (2012) Heat-stable persephonella carbonic anhydrases and their use. Google Patents

  29. Min KH, Son RG, Ki MR, Choi YS, Pack SP (2016) High expression and biosilica encapsulation of alkaline-active carbonic anhydrase for CO2 sequestration system development. Chemosphere 143:128–134

    Article  CAS  Google Scholar 

  30. Del Prete S, Vullo D, De Luca V, Carginale V, di Fonzo P, Osman SM, AlOthman Z, Supuran CT, Capasso C (2016) Anion inhibition profiles of the complete domain of the eta-carbonic anhydrase from Plasmodium falciparum. Bioorganic Med Chem 24:4410–4414

    Article  Google Scholar 

  31. Poulsen SA, Bornaghi LF, Healy PC (2005) Synthesis and structure-activity relationships of novel benzene sulfonamides with potent binding affinity for bovine carbonic anhydrase II. Bioorg Med Chem Lett 15:5429–5433

    Article  CAS  Google Scholar 

  32. Scozzafava A, Owa T, Mastrolorenzo A, Supuran CT (2003) Anticancer and antiviral sulfonamides. Curr Med Chem 10:925–953

    Article  CAS  Google Scholar 

  33. Pastorekova S, Casini A, Scozzafava A, Vullo D, Pastorek J, Supuran CT (2004) Carbonic anhydrase inhibitors: the first selective, membrane-impermeant inhibitors targeting the tumor-associated isozyme IX. Bioorg Med Chem Lett 14:869–873

    Article  CAS  Google Scholar 

  34. Vullo D, Flemetakis E, Scozzafava A, Capasso C, Supuran CT (2014) Anion inhibition studies of two alpha-carbonic anhydrases from Lotus japonicus, LjCAA1 and LjCAA2. J Inorg Biochem 136:67–72

    Article  CAS  Google Scholar 

  35. Alterio V, Di Fiore A, D’Ambrosio K, Supuran CT, De Simone G (2012) Multiple binding modes of inhibitors to carbonic anhydrases: how to design specific drugs targeting 15 different isoforms? Chem Rev 112:4421–4468

    Article  CAS  Google Scholar 

  36. Supuran CT (2008) Carbonic anhydrases: novel therapeutic applications for inhibitors and activators. Nat Rev Drug Discovery 7:168–181

    Article  CAS  Google Scholar 

  37. Sharma A, Bhattacharya A, Pujari R, Shrivastava A (2008) Characterization of carbonic anhydrase from diversified genus for biomimetic carbon-dioxide sequestration. Indian J Microbiol 48:365–371

    Article  CAS  Google Scholar 

  38. Smith KS, Jakubzick C, Whittam TS, Ferry JG (1999) Carbonic anhydrase is an ancient enzyme widespread in prokaryotes. P Natl Acad Sci USA 96:15184–15189

    Article  CAS  Google Scholar 

  39. de Leeuw NH, Parker SC (1998) Surface structure and morphology of calcium carbonate polymorphs calcite, aragonite, and vaterite: an atomistic approach. J Phys Chem B 102:2914–2922

    Article  Google Scholar 

  40. Ki MR, Kanth BK, Min KH, Lee J, Pack SP (2012) Increased expression level and catalytic activity of internally-duplicated carbonic anhydrase from Dunaliella species by reconstitution of two separate domains. Process Biochem 47:1423–1427

    Article  CAS  Google Scholar 

  41. Ki MR, Nguyen TKM, Kim SH, Kwon I, Pack SP (2016) Chimeric protein of internally duplicated alpha-type carbonic anhydrase from Dunaliella species for improved expression and CO2 sequestration. Process Biochem 51:1222–1229

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the Basic Core Technology Development Program for the Oceans and the Polar Regions of the National Research Foundation (NRF) (NRF-2015M1A5A1037054) funded by the Ministry of Science, ICT & Future Planning, Korea  and Research Fellow Funding Grant (NRF-2014R1A1A2008088) funded by the Ministry of Education, Korea.

Author information

Authors and Affiliations

  1. Department of Biotechnology and Bioinformatics, Korea University, 2511 Sejong-Ro, Sejong, 30019, Korea

    So-Young Jun, Sung Ho Kim, Bashista Kumar Kanth & Seung Pil Pack

  2. Department of Chemical and Biomolecular Engineering, Sogang University, 35 Baekbeom-ro, Seoul, 04107, Korea

    Jinwon Lee

Authors
  1. So-Young Jun
    View author publications

    Search author on:PubMed Google Scholar

  2. Sung Ho Kim
    View author publications

    Search author on:PubMed Google Scholar

  3. Bashista Kumar Kanth
    View author publications

    Search author on:PubMed Google Scholar

  4. Jinwon Lee
    View author publications

    Search author on:PubMed Google Scholar

  5. Seung Pil Pack
    View author publications

    Search author on:PubMed Google Scholar

Corresponding authors

Correspondence to Jinwon Lee or Seung Pil Pack.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jun, SY., Kim, S.H., Kanth, B.K. et al. Expression and characterization of a codon-optimized alkaline-stable carbonic anhydrase from Aliivibrio salmonicida for CO2 sequestration applications. Bioprocess Biosyst Eng 40, 413–421 (2017). https://doi.org/10.1007/s00449-016-1709-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00449-016-1709-3

Keywords