Skip to main content

Advertisement

SpringerLink
Log in

Novel alkalistable α-carbonic anhydrase from the polyextremophilic bacterium Bacillus halodurans: characteristics and applicability in flue gas CO2 sequestration

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

The emissions of CO2 into the atmosphere have been constantly rising due to anthropogenic activities, which have led to global warming and climate change. Among various methods proposed for mitigating CO2 levels in the atmosphere, carbonic anhydrase (CA)-mediated carbon sequestration represents a greener and safer approach to capture and convert it into stable mineral carbonates. Despite the fact that CA is an extremely efficient metalloenzyme that catalyzes the hydration of CO2 (CO2 + H2O ↔ HCO3 − + H+) with a kcat of ∼106 s−1, a thermostable, and alkalistable CA is desirable for the process to take place efficiently. The purified CA from alkaliphilic, moderately thermophilic, and halotolerant Bacillus halodurans TSLV1 (BhCA) is a homodimeric enzyme with a subunit molecular mass of ~37 kDa with stability in a broad pH range between 6.0 and 11.0. It has a moderate thermostability with a T1/2 of 24.0 ± 1.0 min at 60 °C. Based on the sensitivity of CA to specific inhibitors, BhCA is an α-CA; this has been confirmed by nucleotide/amino acid sequence analysis. This has a unique property of stimulation by SO4 2−, and it remains unaffected by SO3 2−, NOx, and most other components present in the flue gas. BhCA is highly efficient in accelerating the mineralization of CO2 as compared to commercial bovine carbonic anhydrase (BCA) and is also efficient in the sequestration of CO2 from the exhaust of petrol driven car, thus, a useful biocatalyst for sequestering CO2 from flue gas.

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

Similar content being viewed by others

References

  • Barabesi C, Galizzi A, Mastromei G, Rossi M, Tamburini E, Perito B (2007) Bacillus subtilis gene cluster involved in calcium carbonate biomineralization. J Bacteriol 189:228–235

    Article  CAS  Google Scholar 

  • Bhattacharya S, Schiavone M, Chakrabarti S, Bhattacharya SK (2003) CO2 hydration by immobilized carbonic anhydrase. Biotechnol Appl Biochem 38:111–117

    Article  CAS  Google Scholar 

  • Bond GM, Stringer J, Brandvold DK, Simsek AM, Margaret-Gail EG (2001) Development of integrated system for biomimetic CO2 sequestration using the enzyme carbonic anhydrase. Energy Fuels 15:309–316

    Article  CAS  Google Scholar 

  • Bonra K, Ekrem O (2010) Thermal stability of carbonic anhydrase immobilized within polyurethane foam. Amer Inst Chem Engs 26:1474–1480

    Google Scholar 

  • Ciullo PA Industrial minerals and their uses (1996) In: Ciullo PA (ed) A handbook and formulatory. William Andrew Publishing/Noyes, New Jersy, pp 17–82

  • Cowan RM, Ge JJ, Qin YJ, McGregor ML, Trachtenberg MC (2003) CO2 capture by means of an enzyme-based reactor. Ann New York Acad Sci 984:453–469

    Article  CAS  Google Scholar 

  • Cuesta-Seijo JA, Borchert MS, Navarro-Poulsen JC, Schnorr KM, Mortensen SB, Leggio LL (2015) Structure of a dimeric fungal α type carbonic anhydrase. FEBS Lett 585:1042–1048

    Article  Google Scholar 

  • Dey G, Palit S, Banerjee R, Maiti BR (2002) Purification and characterization of maltooligosaccharide-forming amylase from Bacillus circulans GRS 313. J Indust Microbiol Biotechnol 28:193–200

    Article  CAS  Google Scholar 

  • Ercole C, Cacchio P, Botta AL, Centi V, Lepidi A (2007) Bacterially induced mineralization of calcium carbonate: the role of exopolysaccharide sand capsular polysaccharides. Microsc Microanal 13:42–50

    Article  CAS  Google Scholar 

  • Exhaust gas. Wikipedia, The Free Encyclopedia https://en.wikipedia.org/wiki/Exhaust_gas#cite_note-AUDIEmiss1-11. Assessed February 2, 2016

  • Faridi S, Satyanarayana T (2015a) Prospects in biomimetic carbon sequestration. In: Goel M, Sudhakar M, Sahi RV (eds) Carbon capture, storage and utilization: a possible climate change solution for energy industry. TERI Press, New Delhi, pp 167–187

    Google Scholar 

  • Faridi S, Satyanarayana T (2015b) Applicability of carbonic anhydrase in mitigating global wariming and development of useful products from CO2. Clim Change Environm Sustain 3:77–92

    Article  Google Scholar 

  • Faridi S, Satyanarayana T (2015). Bioconversion of industrial CO2 emissions into utilizable products by employing microbes and their enzymes, In: Chandra R (ed) Environmental waste management, CRC Press, pp 111–156

  • Ghosh S, Ray M, Ray S (2004) Involvement of histidine residue His382 in pH regulation of MCT4 activity. Indian J Chem Biophys 41:7–13

    CAS  Google Scholar 

  • Hou WC, Chen HJ, Lin YH (2000) Dioscorins from different Dioscorea species all exhibit both carbonic anhydrase and trypsin inhibitor activities. Bot Bull Acad Sinica 41:191–196

    CAS  Google Scholar 

  • Iluata I, Larachi F (2012) New scrubber concept for catalytic CO2 hydration by immobilized carbonic anhydrase II and in-situ inhibitor removal in three-phase monolith slurry reactor. Sep Purif Technol 86:199–214

    Article  Google Scholar 

  • IPCC Special Report Carbon Dioxide Capture and Storage Summary for Policymakers (2011) Intergovernmental Panel on Climate Change

  • James P, Isupov MN, Sayer C, Saneei V, Berg S, Lioliou M, Kotlar HK, Littlechild JA (2014) The structure of a tetrameric α-carbonic anhydrase from Thermovibrio ammonificans reveals a core formed around intermolecular disulfides that contribute to its thermostability. Acta Cryst 70:2607–2618

    CAS  Google Scholar 

  • Jo BH, Kim IM, Seo JH, Kang DG, Chaa 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 

  • Karabencheva-Christova TG, Carlsson U, Balali-Mood K, Black GW, Christov CZ (2013) Unoconformational effects on the Circular Dichroism of human carbonic anhydrase II: a multilevel computational study. PLoS One 8:e56874

    Article  CAS  Google Scholar 

  • Kaur S, Bhattacharya A, Sharma A, Tripathi AK (2012) Diversity of microbial carbonic anhydrases, their physiological role and applications. In: Johri BN, Prakash A (eds) Satyanarayana T. Springer, Microorganisms in environmental management, pp 151–173

    Google Scholar 

  • Khalifah RG, Silverman DN (1991) In: Dodgson SJ, Tashian RE, Gros G, Carter ND (eds) The carbonic anhydrases: cellular physiology and molecular genetics. Plenum Press, New York, pp 49–70

    Chapter  Google Scholar 

  • Kumar V, Satyanarayana T (2013) Biochemical and thermodynamic characteristics of thermo-alkali-stable xylanase from a novel polyextremophilic Bacillus halodurans TSEV1. Extremophiles 17:797–808

    Article  CAS  Google Scholar 

  • Lane TW, Saito MA, George GN, Pickering IJ, Prince RC, Orel FMM (2000) Biochemistry: a cadmium enzyme from a marine diatom. Nature 435:42

    Article  Google Scholar 

  • Laois-Jeune C, Andrade-Navarro MA, Perez-Iratxeta C (2011) Prediction of proteins secondary structure from circular dichroism using theoretically derived spectra., Wiley periodicals, http://www.ogic.ca/projects/k2d3/

  • Lee SW, Park SB, Jeong SK, Lim KS, Lee SH, Trachtenberg MC (2010) On carbon dioxide storage based on biomineralization strategies. Micron 41:273–282

    Article  CAS  Google Scholar 

  • Li L, Fu M, Zhaou Y, Zhu Y (2012) Characterization of carbonic anhydrase II from Chlorella vulgaris in bio-CO2 capture. Environ Sci Pollut Res 19:4227–4232

    Article  CAS  Google Scholar 

  • Liu W, Shi P, Chen Q, Yang P, Wang G, Wang Y, Luo H, Yao B (2010) Gene cloning, over-expression, and characterization of a xylanase from Penicillium sp. CGMCC 1699. Appl Biochem Biotechnol 162:1–12

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Meeting C, Nguyen. Low-Cost Enzyme-Based Technology for Carbon Capture. (https://www.netl.doe.gov/File%20Library/Events/2012/CO2%20Capture%20Meeting/L-Nguyen-Codexis-ARPA-e-Enzyme-based-Capture.pdf)

  • Mikulski RL, Silverman DN (2010) Proton transfer in catalysis and the role of proton shuttles in carbonic anhydrase. Biochim Biophys Acta 1804:422–426

    Article  CAS  Google Scholar 

  • Mirjafari P, Asghari K, Mahinpey N (2007) Investigating the application of enzyme carbonic anhydrase for CO2 sequestration purposes. Ind Eng Chem Res 46:921–926

    Article  CAS  Google Scholar 

  • Nisha M, Satyanarayana T (2013) Characterization of recombinant amylopullulanase (gt-apu) and truncated amylopullulanase (gt-apuT) of the extreme thermophile Geobacillus thermoleovorans NP33 and their action in starch saccharification. Appl Microbiol Biotechnol 97:6279–6292

    Article  CAS  Google Scholar 

  • Oviya M, Giri SS, Sukumaran V, Natarajan P (2012) Immobilization of carbonic anhydrase enzyme purified from Bacillus subtilis VSG-4 and its application as CO2 sequesterer. Prep Biochem Biotech 42:462–475

    Article  CAS  Google Scholar 

  • Oviya M, Sukumaran V, Giri SS (2013) Immobilization and characterization of carbonic anhydrase purified from E. coli MO1 and its influence on CO2 sequestration. World J Microbiol Biotechnol 29:1813–1820

    Article  CAS  Google Scholar 

  • Park H, Song B, Morel FM (2007) Diversity of the cadmium-containing carbonic anhydrase in marine diatoms and natural waters. Environ Microbiol 9:403–413

    Article  CAS  Google Scholar 

  • Pomar L, Hallock (2008) Carbonate factories: a conundrum in sedimentary geology. Earth Sci Rev 287:134–169

    Article  Google Scholar 

  • Prabhu C, Wanjari S, Gawande S, Das S, Labhsetwar N, Kotwal S, Puri AK, Satyanarayana T, Rayalu S (2009) Immobilization of carbonic anhydrase enriched microorganism on biopolymer based materials. J Mol Catal B Enzym 60:13–21

    Article  CAS  Google Scholar 

  • Prabhu C, Wanjari S, Puri A, Bhattacharya A, Pujari R, Yadav R, Das S, Labhsetwar N, Sharma A, Satyanarayana Z, Rayalu S (2011) Region specific bacterial carbonic anhydrase for biomimetic sequestration of carbon dioxide. Energy Fuels 25:1327–1332

    Article  CAS  Google Scholar 

  • Pushkas LG, Inui M, Zahan K, Yukawa H (2000) A periplasmic, α-type carbonic anhydrase from Rhodopseudomonas palustris is essential for bicarbonate uptake. Microbiology 146:2957–2966

    Article  Google Scholar 

  • Ramanan R, Kannan K, Sivanesan SD (2009) Biosequestration of carbon dioxide using carbonic anhydrase enzyme purified from Citrobacter freundii. World J Microbiol Biotechnol 25:981–987

    Article  CAS  Google Scholar 

  • 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 

  • Sharma A, Bhattacharya A, Singh S (2009) Purification and characterization of an extracellular carbonic anhydrase from Pseudomonas fragi. Process Biochem 44:1293–1297

    Article  CAS  Google Scholar 

  • Sharma A, Satyanarayana T (2012) Cloning and expression of acidstable, high maltose-forming, Ca2+ independent α-amylase from an acidophile Bacillus acidicola and its applicability in starch hydrolysis. Extremophiles 16:515–522

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Steiner H, Jonsson BH, Lindskog S (1975) The catalytic mechanism of carbonic anhydrase. Hydrogen-isotope effects on the kinetic parameters of the human C isoenzyme. Eur J Biochem 59:253–259

    Article  CAS  Google Scholar 

  • Tashian RE (1989) The carbonic anhydrases: widening perspectives on their evolution, expression and function. BioEssays 10:186–192

    Article  CAS  Google Scholar 

  • Tripp BC, Smith K, Ferry JG (2001) Carbonic anhydrase: new insights for an ancient enzyme. J Biol Chem 276:48615–48618

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Vinoba M, Kim DH, Lim KS, Jeong SK, Lee SW, Alagar M (2011) Biomimetic sequestration of CO2 and reformation to CaCO3 using bovine carbonic anhydrase immobilized on SBA-15. Energy Fuels 25:438–445

    Article  CAS  Google Scholar 

  • Wilkins RG, Williams KR (1974) Kinetics of formation and dissociation of manganese-bovine carbonic anhydrase. B J Am Chem Soc 96:2241–2245

    Article  CAS  Google Scholar 

  • Yadav R, Wanjari S, Prabhu C, Vivek K, Labhsetwar N, Satyanarayana T, Kotwal S, Rayalu S (2010) Immobilized carbonic anhydrase for the biomimetic carbonation reaction. Energy Fuels 24:6198–6207

    Article  CAS  Google Scholar 

  • Yanyou W, Xinzhen Z, Pingping L, Huakun H (2007) Impact of Zn, Cu and Fe on the activity of carbonic anhydrase of erythrocytes in ducks. Biol Trace Elem Res 118:227–232

    Article  Google Scholar 

Download references

Acknowledgments

One of us (SF) is grateful to the University of Delhi, Delhi, for the award of fellowship during the course of this investigation.

Author information

Authors and Affiliations

  1. Department of Microbiology, University of Delhi South Campus, Benito Juarez Road, New Delhi, 110021, India

    Shazia Faridi & T. Satyanarayana

Authors
  1. Shazia Faridi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. T. Satyanarayana
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to T. Satyanarayana.

Additional information

Responsible editor: Santiago V. Luis

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 959 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Faridi, S., Satyanarayana, T. Novel alkalistable α-carbonic anhydrase from the polyextremophilic bacterium Bacillus halodurans: characteristics and applicability in flue gas CO2 sequestration. Environ Sci Pollut Res 23, 15236–15249 (2016). https://doi.org/10.1007/s11356-016-6642-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-016-6642-0

Keywords

Search

Navigation