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

SIMPLE SUMMARY: Hydrothermal vents are regions such as hot springs found on the seafloor in the mid-ocean and near tectonic plates. They contain fluids with highly enriched carbon dioxide, which is the central element of life on Earth. Many organisms live in this environment and can survive in extreme conditions (extremophiles), such as up to 400 °C or higher, low pH, and high pressure. All organisms need the carbonic anhydrase (CA) enzyme to handle the acid-base imbalance through the hydration of carbon dioxide and the production of bicarbonate necessary for pH homeostasis and many cellular functions. The CAs have been categorized into eight families. In this study, we focused on α-, β-, and γ-CAs from the thermophilic microbiome of marine hydrothermal vents. Microorganisms in this environment need CA to capture CO(2), which is an important contribution to marine hydrothermal vent ecosystem functioning. Previously, we showed the transfer of β-CA gene sequences from prokaryotes to protozoans, insects, and nematodes via horizontal gene transfer (HGT). HGT is not only the transfer and movement of genetic information between organisms but is also a powerful tool in natural biodiversity. If the CA coding gene is transferred horizontally between microorganisms in hydrothermal vents, it is hypothesized that CA is essential for survival in these environments and one of the key players in the carbon cycle in the ocean. ABSTRACT: Carbonic anhydrases (CAs) are metalloenzymes that can help organisms survive in hydrothermal vents by hydrating carbon dioxide (CO(2)). 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.