Genome Study of α-, β-, and γ-Carbonic Anhydrases from the Thermophilic Microbiome of Marine Hydrothermal Vent Ecosystems

Mohammad Sadegh Gheibzadeh; Colleen Varaidzo Manyumwa; Özlem Tastan Bishop; Hossein Shahbani Zahiri; Seppo Parkkila; Reza Zolfaghari Emameh

doi:10.3390/biology12060770

Genome Study of α-, β-, and γ-Carbonic Anhydrases from the Thermophilic Microbiome of Marine Hydrothermal Vent Ecosystems

Biology (Basel). 2023 May 25;12(6):770. doi: 10.3390/biology12060770.

Authors

Mohammad Sadegh Gheibzadeh¹, Colleen Varaidzo Manyumwa², Özlem Tastan Bishop², Hossein Shahbani Zahiri¹, Seppo Parkkila^{3

4}, Reza Zolfaghari Emameh¹

Affiliations

¹ Department of Energy and Environmental Biotechnology, National Institute of Genetic Engineering and Biotechnology (NIGEB), Tehran 14965/161, Iran.
² Research Unit in Bioinformatics (Rubi), Department of Biochemistry and Microbiology, Rhodes University, Grahamstown 6140, South Africa.
³ Faculty of Medicine and Health Technology, Tampere University, 33520 Tampere, Finland.
⁴ Fimlab Ltd., Tampere University Hospital, 33520 Tampere, Finland.

Abstract

Carbonic anhydrases (CAs) are metalloenzymes that can help organisms survive in hydrothermal vents by hydrating carbon dioxide (CO₂). In this study, we focus on alpha (α), beta (β), and gamma (γ) CAs, which are present in the thermophilic microbiome of marine hydrothermal vents. The coding genes of these enzymes can be transferred between hydrothermal-vent organisms via horizontal gene transfer (HGT), which is an important tool in natural biodiversity. We performed big data mining and bioinformatics studies on α-, β-, and γ-CA coding genes from the thermophilic microbiome of marine hydrothermal vents. The results showed a reasonable association between thermostable α-, β-, and γ-CAs in the microbial population of the hydrothermal vents. This relationship could be due to HGT. We found evidence of HGT of α- and β-CAs between Cycloclasticus sp., a symbiont of Bathymodiolus heckerae, and an endosymbiont of Riftia pachyptila via Integrons. Conversely, HGT of β-CA genes from the endosymbiont Tevnia jerichonana to the endosymbiont Riftia pachyptila was detected. In addition, Hydrogenovibrio crunogenus SP-41 contains a β-CA gene on genomic islands (GIs). This gene can be transferred by HGT to Hydrogenovibrio sp. MA2-6, a methanotrophic endosymbiont of Bathymodiolus azoricus, and a methanotrophic endosymbiont of Bathymodiolus puteoserpentis. The endosymbiont of R. pachyptila has a γ-CA gene in the genome. If α- and β-CA coding genes have been derived from other microorganisms, such as endosymbionts of T. jerichonana and Cycloclasticus sp. as the endosymbiont of B. heckerae, through HGT, the theory of the necessity of thermostable CA enzymes for survival in the extreme ecosystem of hydrothermal vents is suggested and helps the conservation of microbiome natural diversity in hydrothermal vents. These harsh ecosystems, with their integral players, such as HGT and endosymbionts, significantly impact the enrichment of life on Earth and the carbon cycle in the ocean.

Keywords: big data mining; carbonic anhydrase; extreme ecosystems; horizontal gene transfer; hydrothermal vents; mobile genetic elements; thermophilic microbiome.

Abstract

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