MINI REVIEW

published: 15 July 2022

doi: 10.3389/fmars.2022.908818

Carbon Dioxide Sequestration by

Microbial Carbonic Anhydrases From
Submarine Hydrothermal Systems
Xiaoyi Ma , Le Liu and Kai Tang *

State Key Laboratory of Marine Environmental Science, Fujian Key Laboratory of Marine Carbon Sequestration, College of
Ocean and Earth Science, Xiamen University, Xiamen, China

Owing to serious environmental and climatic impacts of increasing carbon dioxide (CO2)
concentrations, there is an urgent need for the development of efficient CO2 capture
methods. Carbonic anhydrases (CAs) can mediate CO2 capture via a rapid reaction
between CO2 and bicarbonate ions. However, because of their stability, most of the
CAs are not suitable for use in hostile environments (high temperature, high alkalinity,
high pressure, and solvent). Therefore, this review explores thermophilic microorganisms
in submarine hydrothermal environments as a valuable source of thermostable tolerant
CAs, and highlights the questions and future directions that must be addressed for the
application of CAs in CO2 capture.
Edited by:
Lu Lin,
Keywords: carbonic anhydrases, marine, hydrothermal system, carbon capture, carbon dioxide
Shandong University, China

Reviewed by:
Abhay B. Fulke,
INTRODUCTION
National Institute of
Oceanography (CSIR), India
Continuous increases in carbon dioxide (CO2) concentrations have significantly affected the
Yongyu Zhang,
environment and climate, with the current global atmospheric CO2 levels reaching nearly 420 ppm
Qingdao Institute of
Bioenergy and Bioprocess (Min et al., 2016; Schweitzer et al., 2021). The estimated value for global CO2 emissions is about 48
Technology (CAS), China gigatons per year, and the CO2 emissions must be reduced to < 5 gigatons per year by 2050 to achieve
*Correspondence:
the goal of limiting global temperature rise to 2°C by 2100 (Valluri et al., 2022). However, reduction
Kai Tang of CO2 concentrations via conventional methods, including energy conversion, afforestation,
[email protected] clean energy, or carbon-free energy is very low (Nlü et al., 2021). By contrast, carbon capture,
utilization, and sequestration (CCUS) is an essential technical solution with high CO2 emission
Specialty section: reduction potential (Hasan et al., 2015). Carbon capture is a key process in CCUS, and the cost of
This article was submitted to CO2 reduction could increase by about 140% if carbon capture and storage technologies are not
Aquatic Microbiology, considered (Osman et al., 2020). The CO2 capture technologies include chemical absorption (e.g.,
a section of the journal using aqueous amine solutions) (Yu et al., 2012), physical absorption (e.g., using activated carbon
Frontiers in Marine Science
and natural ores or solid wastes (steel slag)) (Olivares-Marin and Maroto-Valer, 2012; Chen et al.,
Received: 31 March 2022 2014), and biological methods (e.g., plant photosynthesis) (Klinthong et al., 2015). However, these
Accepted: 14 June 2022
methods present challenges related to solvent degradation, volatility, and corrosion, requirement
Published: 15 July 2022
of large amount of adsorbent, and long uptake period of plant culture, which must be addressed
Citation: (Nguyen et al., 2010; Yu et al., 2012). Meanwhile, new techniques for CO2 capture should also be
Ma X, Liu L and Tang K (2022)
explored, and methods for highly specific and rapid enzymatic conversion of CO2 to other stable
Carbon Dioxide Sequestration by
Microbial Carbonic Anhydrases From
compounds using carbonic anhydrases (CAs) show promising potential (Ren et al., 2020).
Submarine Hydrothermal Systems. CAs promote the precipitation of ore ions as carbonates for the purpose of capturing CO2. They
Front. Mar. Sci. 9:908818. can effectively catalyze the reversible hydration of CO2 to achieve rapid reaction between CO2 and
doi: 10.3389/fmars.2022.908818 bicarbonate ions (HCO3−) (Bhattacharya et al., 2003), which subsequently targets appropriate metal

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Ma et al. Carbonic Anhydrases; Hydrothermal; Carbon Capture

ions to precipitate environmental-friendly solid carbonates. These Bhagat et al., 2018). However, the temperature of CO2-containing
metal ions are supplied by natural minerals rich in magnesium gas stream after combustion can reach > 100°C during the CO2
and calcium (wollastonite, forsterite, serpentine, steel slag, etc., capture process (Himadri and Tulasi, 2017), and exposure of CAs
with known reserves of 300, 800, 500, and 240 million tons, to high-temperature or alkaline conditions during CO2 capture
respectively) (Liu et al., 2021). The large quantities and wide can result in severe performance reduction and even denaturation
distribution of these natural minerals allow CAs to capture CO2 of CAs. Therefore, CAs resistant to high temperature and high
as carbonates in large-scale practical applications (Figure 1). The alkalinity are needed for CO2 capture.
utilization of CAs for CO2 capture in CCUS allows faster CO2 The temperature and pressure of submarine hydrothermal
absorption, permits the use of smaller process equipment, and environments can reach about 350–407°C and about 298 bar,
reduces more energy losses during the capture process (Alvizo respectively (Koschinsky et al., 2008), and the abundant microbial
et al., 2014). However, large-scale carbon capture processes populations in these ecosystems exhibit high temperature and
with CAs are limited by enzymatic stability at higher operating pressure tolerance (Dick, 2019). When compared with some
temperature and alkaline pH. CAs derived from microorganisms of the CAs from non-thermophilic bacteria (shorter half-lives
living in extreme environments have the characteristic of and lower enzymatic activity at temperature ≥ 60°C) (Bhagat
resistance to severe conditions, and are gradually emerging as a et al., 2018), thermophilic bacteria (optimum temperature ≥
promising candidate for practical application of CO2 capture. 75°C) and hyperthermophilic bacteria (optimum temperature
≥ 80°C) that thrive in hydrothermal environments can be a
source of heat-resistant CAs (Zeldes et al., 2015). For example,
EXTREMOPHILES AS SOURCE OF CAS the most representative thermostable α-CA (around 100°C)
FOR CO2 CAPTURE IN CCUS isolated from the thermophilic bacterium Sulfurihydrogenibium
azorense Az-Fu1 has been reported to present the highest CO2
CAs are widely distributed in eukaryotes and prokaryotes, hydratase activity (kcat = 4.40 × 106 s−1) among the known CAs
such as mammalian tissues, plants (Floryszak-Wieczorek and (Luca et al., 2013), indicating that excellent CAs can be obtained
Arasimowicz-Jelonek, 2017), algae (Hewett-Emmett and Tashian, from microorganisms living in hydrothermal environments.
1996), bacteria (Claudiu and Clemente, 2017), and archaea (Smith A number of thermally stable CAs have been used to
and Ferry, 2000), and have produced satisfactory outcomes in investigate the capture of CO2 from flue gas. For instance, CA
biomedical applications (Kaar et al., 2007; Kumar et al., 2021), such from Desulfovibrio vulgaris has been used in the adsorption
as biosensors (Thompson et al., 2000), physiological diagnoses process of amines to accelerate the removal of CO2 from flue
(Supuran, 2011, Jonsson and Liljas, 2020), etc. In recent years, gas, and a 25-fold increase in the CO2 absorption rate has been
more attention has been paid to develop strategies to mediate achieved after CA addition (Alvizo et al., 2014). Furthermore,
carbon sequestration via microbial CAs. On the one hand, CAs CA from Sulfurihydrogenibium yellowstonense YO3AOP1 has
can specifically recognize its substrate, CO2, from complex gases been utilized to capture CO2 from flue gas (Rossi, 2013), and
and react with it very quickly. On the other hand, the rapid has been subsequently immobilized in polyurethane foam for
microbial growth can help in the industrial production of CAs. To CO2 biomimetic absorption tests by three-phase trickle-bed
date, nearly 60 different CAs from bacterial and archaeal domains reactor (Migliardini et al., 2013). These studies show that CAs
have been characterized (Bhagat et al., 2018), and most remain from thermophilic microorganisms can be practically applied
active only in a temperature range of < 65°C (Joel et al., 2015; to the CO2 capture process.

FIGURE 1 | Schematic of the application of CAs from microorganisms thriving in submarine hydrothermal environment to CO2 sequestration.

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Ma et al. Carbonic Anhydrases; Hydrothermal; Carbon Capture

DIVERSITY OF MICROBIAL CAS most alkaline environment with a pH of 11, while CAs isolated
IN SUBMARINE HYDROTHERMAL from S. yellowstonense YO3AOP1, S. azorense Az-Fu1, P. marina
EX-H1, and H. crunogena XCL-2 have been recognized to be the
ENVIRONMENTS most resistant to high temperatures, with the ability to maintain
The known hydrothermal environments include 61 shallow- certain activity under 100°C. Overall, although the number of
sea hydrothermal vents (water depth < 200 m) and 201 deep- gene sequences encoding α-CAs is not dominant, α-CAs are the
sea hydrothermal vents (water depth ≥ 200 m), which are major CAs isolated and characterized with higher temperature
widely distributed all over the world (Figure 2A). Analysis and tolerance than β- and γ-CAs, and the majority of α-CAs are
genomic investigations of different CAs-producing microbial known to remain catalytically active at around 100°C. It has been
strains in submarine hydrothermal environments have shown reported that the presence of an N-terminal signal peptide is a
that CAs-producing strains are commonly found in the classes common feature of all known bacterial α-CAs, suggesting that
Epsilonproteobacteria, Gammaproteobacteria, Methanococci, α-CAs are located in the periplasmic space and are responsible
Aquificae, and Thermodesulfobacteria, with majority of the for converting diffused CO2 into HCO3−, which is essential for
strains belonging to the class Epsilonproteobacteria. These bacterial metabolism. By contrast, β- and γ-CAs are located in
microbial strains possess genes encoding α-, β-, and γ-CAs, with the cytoplasmic space and are responsible for providing CO2 for
genes encoding β- and γ-CAs being predominant. In addition, carboxylase enzymes, pH homeostasis, and other intracellular
many of these microbial strains can even possess genes encoding functions (Capasso and Supuran, 2015; Supuran and Capasso,
two or three types of CAs simultaneously (Figure 2B). At 2016). As α-CAs are more readily released from the periplasmic
present, α-CAs-producing microorganisms successfully isolated space of bacteria, with most of these enzymes having higher
from submarine hydrothermal environment mainly include S. catalytic constants (kcat≈ 105–106 s−1) than γ- and β-CAs (kcat ≈
yellowstonense YO3AOP1 (Capasso et al., 2012), S. azorense Az-Fu1 104 s−1), α-CAs are more exploitable, and further research on
(Luca et al., 2013), Thermovibrio ammonificans HB-1 (James engineering or immobilization of microbial CAs could lead to the
et al., 2014), Persephonella marina EX-H1 (Kanth et al., 2014), development of more effective CAs for CO2 capture applications.
Hydrogenovibrio crunogena XCL-2 (Chingkuang et al., 2015).
β-CAs-producing microorganisms include Methanobacterium
thermoautotrophicum ΔH (Smith and Ferry, 1999), and γ-CAs- DISCUSSION
producing microorganisms include Methanosarcina thermophila
TM-1 (Alber and Ferry, 1994; Capasso et al., 2012) and When compared with the cost of CO2 capture by aqueous
Aeribacillus pallidus TSHB1 (Bose and Satyanarayana, 2016) mineral carbonation using wollastonite as feedstock ($ 122/ton
(Figure 2C). The current research on CAs is mainly focused on CO2), application of CA to capture CO2 has been estimated to
enzyme adaptation to alkaline pH and high temperature. The CA save about 50% of the cost (Supplementary Table S1). Here, we
isolated from A. pallidus TSHB1 has been known to survive in the consider that the amount of CO2 that needs to be captured is 480

A B

FIGURE 2 | (A) Known hydrothermal environments, including shallow-sea hydrothermal vents and deep-sea hydrothermal vents. (B) A phylogenetic tree of different
types of CAs-producing microbial strains from submarine hydrothermal systems. The three CAs classes, namely, α-, β-, and γ-CAs and the sequence accession
number (https://img.jgi.doe.gov) after @ are shown. The rectangular bars representing the phyla of known strains are labeled with different background colors.
(C) Classification, sources, and features of CAs from microorganisms in submarine hydrothermal environment

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Ma et al. Carbonic Anhydrases; Hydrothermal; Carbon Capture

kt/year (8000 h), and that the immobilized CAs can increase the via site-directed mutagenesis to make them more compatible
CO2 capture rate by about 25 times. The use of CAs to capture with industrial requirements. The stability of recombinant CAs
CO2 has the potential to overcome barriers in terms of plant can be enhanced by using various immobilization techniques,
quantity requirements and carbon conversion efficiency, save and immobilization of CAs on specific carriers allows recycling
the investment of fixed assets (new plant space, equipment, of the enzyme. Various CAs immobilization methods, including
and operating costs), and generate valuable chemicals. With immobilization onto polyurethane foam (Migliardini et al., 2013),
the deepening of research on submarine hydrothermal magnetic particles (Ren et al., 2020), iron magnetic nanoparticles
microorganisms, CO2 capture using CAs is expected to reduce (Faridi et al., 2017), chitosan beads (Wanjari et al., 2011), silica
the cost of investment to cope with global environment and beads (Raju et al., 2012), and other carriers (adsorption, cross-
climate change. linked, covalent bonding, encapsulation or entrapment) have
Although the number of CAs-producing microorganisms that been investigated (Molina-Fernández and Luis, 2021), and
could be purely cultured has considerably increased over the past some of these techniques have been shown to improve CAs
80 years, only a small fraction of CAs-producing microorganisms activity and stability (e.g., CA from S. Yellowstonense YO3AOP1
isolated from submarine hydrothermal environments have been immobilized on polyurethane foam maintains good stability)
described in detail. Most of the microorganisms in submarine (Migliardini et al., 2013). Nevertheless, an unresolved problem
hydrothermal environments have been identified using only that still exists is how to efficiently and reliably overexpress
16S rRNA sequencing, and are still difficult to be cultured thermophilic enzyme genes in heterologous hosts. It is possible
and physiologically and metabolically characterized. For the that the expressed proteins may not be able to withstand harsh
application of CAs on an industrial scale, first, it is important environments (temperature, pressure, and pH) or may simply
to obtain more CAs from microorganisms in submarine be prone to become insoluble, limiting the application of CAs.
hydrothermal environments. Many culturable microorganisms Besides, the recovery and reuse of free enzymes is expensive, and
isolated from marine hydrothermal environments can fix it has been predicted that immobilized CAs will be employed
carbon; for instance, chemoautotrophic microorganisms are for industrial applications in the future. Therefore, there is a
very active in submarine hydrothermal environments and need to develop customized carrier materials that can withstand
their CAs can help them in carbon fixation (Nakagawa and high temperatures and are rigid, as well as balance the degree of
Takai, 2008). Therefore, these microorganisms can be cultured enzyme–carrier interaction so that CAs can be fully utilized for
to obtain thermostable and alkali-tolerant CAs. To investigate CO2 capture. The use of site-directed mutagenesis can specifically
the unculturable microorganisms in marine hydrothermal improve the complementarity of CAs and carrier surface, promote
environments, metagenomics can be employed (Roumpeka et al., site-directed immobilization and rigidization of industrial
2017), and techniques such as gene assembly, gene clustering, CAs, and produce CAs that can meet specific needs. Moreover,
and metagenomic binning of species genomes have significantly immobilization of enzymes on nanoparticles and graphene
enhanced our understanding of the taxonomic composition materials, which possess unique size and physical properties,
of microbial communities in submarine hydrothermal is a worthy future research direction. These nanomaterials can
environments (Frioux et al., 2020). The study of high-quality not only withstand high-temperature conditions, but can also
metagenome-assembled genomes of bacteria and archaea can maintain the folded structure of protein as much as possible and
facilitate robust comparative genomic analyses of bacterial improve storage stability and performance.
and archaeal diversity, allowing splicing of small fragmented Finally, application of thermostable and alkali-tolerant
genes into longer and complete CAs gene sequences as well as CAs to hydrothermal alteration rocks for CO2 sequestration
facilitating de novo assembly of CAs-producing microorganisms is a more interesting research direction. Cations are essential
that cannot be found in databases. to sequester CO2 as a solid carbonate, and magnesia olivine,
Second, it has become an indispensable new trend to obtain wollastonite, serpentine, and basalt can provide cations
thermostable and alkali-tolerant CAs based on engineering (calcium, magnesium, iron, etc.) that can readily react with
of microbial CAs, including genetic engineering, protein CO2 to produce solid inorganic carbonate minerals. Magnesia
engineering (e.g., directed evolution, site-directed mutagenesis, olivine and basalt can be altered and exhibit a fast dissolution
etc.), and enzyme immobilization. By using techniques such rate relative to other silicates (Wang et al., 2019), and addition
as gene cloning and expression, recombinant CAs of several of carbon sources (e.g., CO2, HCO3−) has been reported
thermophilic bacteria have been expressed in Escherichia coli, to significantly enhance the alteration of magnesia olivine
which can maintain thermo-alkali stability and accelerate (Gadikota et al., 2014). Therefore, we conjecture that CAs from
carbonate formation after expression (e.g., E. coli expressing microorganisms thriving in hydrothermal environments can
Neisseria gonorrhoeae CA) (Jo et al., 2013). Directed evolution be introduced into the alteration process of ores. On the one
allows enzyme variants to acquire catalytic capacity by changing hand, CAs can rapidly convert CO2 to HCO3− and enhance
the catalytic site of CAs, and its combination with statistical olivine alteration, so that ferrous ion could be released from
analysis strategies for protein sequence activity relationships olivine to participate in H2 production. On the other hand,
can generate new CAs (e.g., directed evolution can significantly the unconverted CO2 can lead to the formation of carbonates
enhance the properties of highly stable β-CAs derived from D. with Fe-bearing magnesite, which can be used in construction
vulgaris, which can maintain activity at 107°C) (Alvizo et al., 2014). materials, chemical materials, and refining of magnesium metal
The nature of CAs and their catalytic properties can be modified and magnesium compounds.

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Ma et al. Carbonic Anhydrases; Hydrothermal; Carbon Capture

AUTHOR CONTRIBUTIONS Science Center Program of Natural Science Foundation of

China on Marine Carbon Sequestration and Biogeochemistry
KT conceived the main frame of the manuscript and designed (42188102), and the National Natural Science Foundation of
the figures. XM and LL wrote the manuscript. All authors China (42141003).
contributed to the article and approved the submitted version.

SUPPLEMENTARY MATERIAL
FUNDING
The Supplementary Material for this article can be found online at:
This work was supported by the National Key Research and https://www.frontiersin.org/articles/10.3389/fmars.2022.908818/
Development Program of China (2020YFA0608300), the Basic full#supplementary-material

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Frontiers in Marine Science | www.frontiersin.org 6 July 2022 | Volume 9 | Article 908818