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Alpha-Carbonic Anhydrases from Hydrothermal Vent Sources As Potential Carbon Dioxide Sequestration Agents: in Silico Sequence, Structure and Dynamics Analyses

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Alpha-Carbonic Anhydrases from Hydrothermal Vent Sources As Potential Carbon Dioxide Sequestration Agents: in Silico Sequence, Structure and Dynamics Analyses International Journal of Molecular Sciences Article Alpha-Carbonic Anhydrases from Hydrothermal Vent Sources as Potential Carbon Dioxide Sequestration Agents: In Silico Sequence, Structure and Dynamics Analyses Colleen Varaidzo Manyumwa 1 , Reza Zolfaghari Emameh 2 and Özlem Tastan Bishop 1,* 1 Research Unit in Bioinformatics (RUBi), Department of Biochemistry and Microbiology, Rhodes University, Makhanda/Grahamstown 6140, South Africa; [email protected] 2 Department of Energy and Environmental Biotechnology, National Institute of Genetic Engineering and Biotechnology (NIGEB), Tehran 14965/161, Iran; [email protected] * Correspondence: [email protected]; Tel.: +27-46-603-8072; Fax: +27-46-603-7576 Received: 28 September 2020; Accepted: 27 October 2020; Published: 29 October 2020 Abstract: With the increase in CO2 emissions worldwide and its dire effects, there is a need to reduce CO2 concentrations in the atmosphere. Alpha-carbonic anhydrases (α-CAs) have been identified as suitable sequestration agents. This study reports the sequence and structural analysis of 15 α-CAs from bacteria, originating from hydrothermal vent systems. Structural analysis of the multimers enabled the identification of hotspot and interface residues. Molecular dynamics simulations of the homo-multimers were performed at 300 K, 363 K, 393 K and 423 K to unearth potentially thermostable α-CAs. Average betweenness centrality (BC) calculations confirmed the relevance of some hotspot and interface residues. The key residues responsible for dimer thermostability were identified by comparing fluctuating interfaces with stable ones, and were part of conserved motifs. Crucial long-lived hydrogen bond networks were observed around residues with high BC values. Dynamic cross correlation fortified the relevance of oligomerization of these proteins, thus the importance of simulating them in their multimeric forms. A consensus of the simulation analyses used in this study suggested high thermostability for the α-CA from Nitratiruptor tergarcus. Overall, our novel findings enhance the potential of biotechnology applications through the discovery of alternative thermostable CO2 sequestration agents and their potential protein design. Keywords: alpha-carbonic anhydrase; homology modelling; motif analysis; MD simulations; dynamic residue network analysis; hydrothermal vents 1. Introduction The accumulating concentrations of greenhouse gases (GHGs) over the years have led to the warming of the earth’s atmosphere [1–3]. CO2 is considered to be one of the GHGs contributing to a significant amount of global warming, with the major source of these gases being the combustion of fossil fuels, rice paddies, and livestock fields [3–6]. CO2 concentrations have increased from approximately 280 ppm (parts per million) in the pre-industrial period to approximately 410 ppm in 2019 [7]. Thus, the discovery and implementation of mitigation strategies is crucial. Sequestration of CO2 via biomineralization, which involves the aqueous precipitation of minerals in the presence of CO2 to form mineral carbonates, is a storage strategy currently being explored [8,9]. The use of a catalyst in this process is important, because otherwise the hydration of CO2 is very slow [10]. Some of the reactions that take place during biomineralization, however, require conditions, Int. J. Mol. Sci. 2020, 21, 8066; doi:10.3390/ijms21218066 www.mdpi.com/journal/ijms Int.Int. J. J. Mol. Mol. Sci. Sci. 20202020, ,2121, ,x 8066 FOR PEER REVIEW 22 of of 34 32 CO2 is very slow [10]. Some of the reactions that take place during biomineralization, however, requireincluding conditions, high temperatures including exceeding high temperatures 100 ◦C and anexceeding alkaline pH100 [11 °C,12 and]. Consequently, an alkaline thermo-alkalipH [11,12]. Consequently,stable enzymatic thermo-alkali catalysts are stable being enzymatic sought. catalysts are being sought. CarbonicCarbonic anhydrasesanhydrases (CAs)(CAs) are are enzymes enzymes responsible responsible for thefor reversible the reversible catalytic catalytic reaction reaction between betweenCO2 and CO H22O. and They H2O. are They viable are CO viable2 sequestration CO2 sequestration agents due agents to their due fastto their CO2 fasthydration CO2 hydration with catalytic with 4 1 catalyticturnover turnover rates (kcat )rates exceeding (kcat) 10exceedings− for the104 majoritys−1 for the of CAsmajority [11,13 ,of14 ].CAs They [11,13,14]. are metalloenzymes They are 2+ 2+ metalloenzymescontaining a Zn containingmetal ion a in Zn the2+ metal active ion site, in with the someactive having site, with shown some the having ability shown to utilize theiron ability (Fe to ) 2+ 2+ utilizeor cobalt iron (Co (Fe2+)) instead or cobalt of Zn(Co2+,) and instead still maintainof Zn2+, and their still catalytic maintain activity their [15 catalytic–17]. Three activity major [15–17]. classes Threeof the major CA family, classesα, βof, andthe γCA, have family, been α widely, β, and studied. γ, have The been other widely classes studied. identified The include otherδ ,classesζ, η, θ , identifiedand ι-CAs, include with the δ, ζι-CAs, η, θ, being and ι-CAs, the most with recently the ι-CAs discovered being the [18 most–22]. recently discovered [18–22]. COCO22 hydrationhydration proceeds proceeds as as shown shown in in Reaction Reaction (1) (1) (Figure (Figure 11A),A), resulting in thethe formationformation ofof carboniccarbonic acid acid which which dissociates dissociates to to bicarbonate bicarbonate an andd hydrogen hydrogen ions. ions. After After being being released released from from the the catalyticcatalytic site site into into the the solvent, solvent, the the bicarbonate bicarbonate ions ions further further dissociate dissociate to tocarbonate carbonate ions ions (Reaction (Reaction (2) (2)in 2+ 2+ 2+ Figurein Figure 1A)1A) which which then then react react with with the the metal metal ions (shown asas XX2+),), such such as CaCa2+ or MgMg2+, ,during during biomineralizationbiomineralization to toform form the the mineral mineral carbonate carbonate XCO XCO3 [10,23].3 [10 This,23]. is This illustrated is illustrated in Reaction in Reaction (3) (Figure (3) 1A).(Figure 1A). FigureFigure 1.1. BiologicalBiological assembly assembly of theof alpha-carbonicthe alpha-carbonic anhydrase anhydrase (α-CA) from (α-CA)Thermovibrio from Thermovibrio ammonificans ammonificans (TaCA, PDB ID: 4C3T). (A) illustrates the equations for CO2 hydration and dehydration (TaCA, PDB ID: 4C3T). (A) illustrates the equations for CO2 hydration and dehydration (1 and 2) as (1well and as 2) metal as well carbonation as metal (3), carbonation while (B) shows (3), while the tetrameric (B) shows structure the tetrameric of TaCA. structure (C) shows of the TaCA. disulfide (C) showscore formed the disulfide by four Cyscore residuesformed inby thefour tetramerization Cys residues interface.in the tetramerization The catalytic cavityinterface. is enlarged The catalytic in (D), 2+ cavitywith CO is 2enlargedbinding in pocket (D), with residues CO2 colored binding red, pocket proton residues transfer colored residues red, in proton blue and transfer Zn coordinating residues in blueHis residuesand Zn2+ coloredcoordinating green. His residues colored green. αα-CAs-CAs are are the the most most widely widely studied studied class class of of ca carbonicrbonic anhydrases, anhydrases, and and have have been been found found in in mammals,mammals, algae, algae, and and plants, plants, with with numerous numerous repo reportsrts in in bacteria bacteria as as well well [24–26]. [24–26]. Most Most human human αα-CAs-CAs havehave monomeric monomeric structures, structures, in in cont contrastrast to to their their bacterial bacterial counterparts counterparts which which have have been been revealed revealed to to havehave a a dimeric dimeric assembly assembly [27,28]. [27,28 ].A unique A unique tetrameric tetrameric assembly, assembly, absent absent in all in other all other α-CAsα-CAs to date, to date, has beenhas beenobserved observed for the for theα-CAα-CA from from ThermovibrioThermovibrio ammonificans ammonificans (TaCA,(TaCA, PDB PDB ID: ID: 4C3T) 4C3T) (Figure (Figure 1B),1B), whichwhich is heldheld together together by by a corea core of two of disulfidetwo disulfide bonds bonds (Figure (Figure1C) [ 29 ].1C) Each [29]. monomer Each monomer has a functional has a functional independent active site, containing a Zn2+ metal ion in tetrahedral coordination by three Int. J. Mol. Sci. 2020, 21, 8066 3 of 32 independent active site, containing a Zn2+ metal ion in tetrahedral coordination by three His residues as well as a water molecule [14,30–32]. They also have a hydrophobic pocket close to the active site where the CO2 molecule is normally held during catalysis (Figure1D). This pocket has been identified in most α-CAs, including the human CA II [33–37]. Given the high environmental temperatures, CAs from hydrothermal vents may already possess attributes to withstand the extreme conditions in the CO2 sequestration process, thus providing a viable alternative to engineering CAs. This has been observed in vitro on α-CAs from hydrothermal vent bacteria Caminibacter mediatlanticus (CmCA), Persephonella marina (PmCA) and TaCA, with CmCA and PmCA revealing stability up to 70 ◦C and 100 ◦C, respectively, and the wild-type and variants of TaCA appearing stable up to 95 ◦C[38–41]. Another CA, found in previously isolated DNA from the Logatchev hydrothermal field (LOGACA), has also proven to be thermostable, withstanding
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