Characterization of a novel thermophilic cyanobacterium within Trichocoleusaceae, Trichothermofontia sichuanensis gen. et sp. nov., and its CO2-concentrating mechanism
Thermophiles from extreme thermal environments have shown tremendous potential regarding ecological and biotechnological applications. Nevertheless, thermophilic cyanobacteria remain largely untapped and are rarely characterized. Herein, a polyphasic approach was used to characterize a thermophilic...
| Main Authors: | , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2023-04-01
|
| Series: | Frontiers in Microbiology |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1111809/full |
| _version_ | 1797838618493976576 |
|---|---|
| author | Jie Tang Huizhen Zhou Ying Jiang Dan Yao Krzysztof F. Waleron Lian-Ming Du Maurycy Daroch |
| author_facet | Jie Tang Huizhen Zhou Ying Jiang Dan Yao Krzysztof F. Waleron Lian-Ming Du Maurycy Daroch |
| author_sort | Jie Tang |
| collection | DOAJ |
| description | Thermophiles from extreme thermal environments have shown tremendous potential regarding ecological and biotechnological applications. Nevertheless, thermophilic cyanobacteria remain largely untapped and are rarely characterized. Herein, a polyphasic approach was used to characterize a thermophilic strain, PKUAC-SCTB231 (hereafter B231), isolated from a hot spring (pH 6.62, 55.5°C) in Zhonggu village, China. The analyses of 16S rRNA phylogeny, secondary structures of 16S-23S ITS and morphology strongly supported strain B231 as a novel genus within Trichocoleusaceae. Phylogenomic inference and three genome-based indices further verified the genus delineation. Based on the botanical code, the isolate is herein delineated as Trichothermofontia sichuanensis gen. et sp. nov., a genus closely related to a validly described genus Trichocoleus. In addition, our results suggest that Pinocchia currently classified to belong to the family Leptolyngbyaceae may require revision and assignment to the family Trichocoleusaceae. Furthermore, the complete genome of Trichothermofontia B231 facilitated the elucidation of the genetic basis regarding genes related to its carbon-concentrating mechanism (CCM). The strain belongs to β-cyanobacteria according to its β-carboxysome shell protein and 1B form of Ribulose bisphosphate Carboxylase-Oxygenase (RubisCO). Compared to other thermophilic strains, strain B231contains a relatively low diversity of bicarbonate transporters (only BicA for HCO3− transport) but a higher abundance of different types of carbonic anhydrase (CA), β-CA (ccaA) and γ-CA (ccmM). The BCT1 transporter consistently possessed by freshwater cyanobacteria was absent in strain B231. Similar situation was occasionally observed in freshwater thermal Thermoleptolyngbya and Thermosynechococcus strains. Moreover, strain B231 shows a similar composition of carboxysome shell proteins (ccmK1-4, ccmL, -M, -N, -O, and -P) to mesophilic cyanobacteria, the diversity of which was higher than many thermophilic strains lacking at least one of the four ccmK genes. The genomic distribution of CCM-related genes suggests that the expression of some components is regulated as an operon and others in an independently controlled satellite locus. The current study also offers fundamental information for future taxogenomics, ecogenomics and geogenomic studies on distribution and significance of thermophilic cyanobacteria in the global ecosystem. |
| first_indexed | 2024-04-09T15:44:51Z |
| format | Article |
| id | doaj.art-110451366a8b4ce9abf65de2f93ec5dd |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-04-09T15:44:51Z |
| publishDate | 2023-04-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-110451366a8b4ce9abf65de2f93ec5dd2023-04-27T04:31:23ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-04-011410.3389/fmicb.2023.11118091111809Characterization of a novel thermophilic cyanobacterium within Trichocoleusaceae, Trichothermofontia sichuanensis gen. et sp. nov., and its CO2-concentrating mechanismJie Tang0Huizhen Zhou1Ying Jiang2Dan Yao3Krzysztof F. Waleron4Lian-Ming Du5Maurycy Daroch6School of Food and Bioengineering, Chengdu University, Chengdu, Sichuan, ChinaSchool of Food and Bioengineering, Chengdu University, Chengdu, Sichuan, ChinaSchool of Environment and Energy, Peking University Shenzhen Graduate School, Shenzhen, ChinaSchool of Food and Bioengineering, Chengdu University, Chengdu, Sichuan, ChinaDepartment of Pharmaceutical Microbiology, Faculty of Pharmacy Medical University of Gdańsk, Gdańsk, PolandSchool of Food and Bioengineering, Chengdu University, Chengdu, Sichuan, ChinaSchool of Environment and Energy, Peking University Shenzhen Graduate School, Shenzhen, ChinaThermophiles from extreme thermal environments have shown tremendous potential regarding ecological and biotechnological applications. Nevertheless, thermophilic cyanobacteria remain largely untapped and are rarely characterized. Herein, a polyphasic approach was used to characterize a thermophilic strain, PKUAC-SCTB231 (hereafter B231), isolated from a hot spring (pH 6.62, 55.5°C) in Zhonggu village, China. The analyses of 16S rRNA phylogeny, secondary structures of 16S-23S ITS and morphology strongly supported strain B231 as a novel genus within Trichocoleusaceae. Phylogenomic inference and three genome-based indices further verified the genus delineation. Based on the botanical code, the isolate is herein delineated as Trichothermofontia sichuanensis gen. et sp. nov., a genus closely related to a validly described genus Trichocoleus. In addition, our results suggest that Pinocchia currently classified to belong to the family Leptolyngbyaceae may require revision and assignment to the family Trichocoleusaceae. Furthermore, the complete genome of Trichothermofontia B231 facilitated the elucidation of the genetic basis regarding genes related to its carbon-concentrating mechanism (CCM). The strain belongs to β-cyanobacteria according to its β-carboxysome shell protein and 1B form of Ribulose bisphosphate Carboxylase-Oxygenase (RubisCO). Compared to other thermophilic strains, strain B231contains a relatively low diversity of bicarbonate transporters (only BicA for HCO3− transport) but a higher abundance of different types of carbonic anhydrase (CA), β-CA (ccaA) and γ-CA (ccmM). The BCT1 transporter consistently possessed by freshwater cyanobacteria was absent in strain B231. Similar situation was occasionally observed in freshwater thermal Thermoleptolyngbya and Thermosynechococcus strains. Moreover, strain B231 shows a similar composition of carboxysome shell proteins (ccmK1-4, ccmL, -M, -N, -O, and -P) to mesophilic cyanobacteria, the diversity of which was higher than many thermophilic strains lacking at least one of the four ccmK genes. The genomic distribution of CCM-related genes suggests that the expression of some components is regulated as an operon and others in an independently controlled satellite locus. The current study also offers fundamental information for future taxogenomics, ecogenomics and geogenomic studies on distribution and significance of thermophilic cyanobacteria in the global ecosystem.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1111809/full16S rRNA16S-23S ITSCO2-concentrating mechanismthermophilic cyanobacteriumTrichocoleusaceaeLeptolyngbyaceae |
| spellingShingle | Jie Tang Huizhen Zhou Ying Jiang Dan Yao Krzysztof F. Waleron Lian-Ming Du Maurycy Daroch Characterization of a novel thermophilic cyanobacterium within Trichocoleusaceae, Trichothermofontia sichuanensis gen. et sp. nov., and its CO2-concentrating mechanism Frontiers in Microbiology 16S rRNA 16S-23S ITS CO2-concentrating mechanism thermophilic cyanobacterium Trichocoleusaceae Leptolyngbyaceae |
| title | Characterization of a novel thermophilic cyanobacterium within Trichocoleusaceae, Trichothermofontia sichuanensis gen. et sp. nov., and its CO2-concentrating mechanism |
| title_full | Characterization of a novel thermophilic cyanobacterium within Trichocoleusaceae, Trichothermofontia sichuanensis gen. et sp. nov., and its CO2-concentrating mechanism |
| title_fullStr | Characterization of a novel thermophilic cyanobacterium within Trichocoleusaceae, Trichothermofontia sichuanensis gen. et sp. nov., and its CO2-concentrating mechanism |
| title_full_unstemmed | Characterization of a novel thermophilic cyanobacterium within Trichocoleusaceae, Trichothermofontia sichuanensis gen. et sp. nov., and its CO2-concentrating mechanism |
| title_short | Characterization of a novel thermophilic cyanobacterium within Trichocoleusaceae, Trichothermofontia sichuanensis gen. et sp. nov., and its CO2-concentrating mechanism |
| title_sort | characterization of a novel thermophilic cyanobacterium within trichocoleusaceae trichothermofontia sichuanensis gen et sp nov and its co2 concentrating mechanism |
| topic | 16S rRNA 16S-23S ITS CO2-concentrating mechanism thermophilic cyanobacterium Trichocoleusaceae Leptolyngbyaceae |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1111809/full |
| work_keys_str_mv | AT jietang characterizationofanovelthermophiliccyanobacteriumwithintrichocoleusaceaetrichothermofontiasichuanensisgenetspnovanditsco2concentratingmechanism AT huizhenzhou characterizationofanovelthermophiliccyanobacteriumwithintrichocoleusaceaetrichothermofontiasichuanensisgenetspnovanditsco2concentratingmechanism AT yingjiang characterizationofanovelthermophiliccyanobacteriumwithintrichocoleusaceaetrichothermofontiasichuanensisgenetspnovanditsco2concentratingmechanism AT danyao characterizationofanovelthermophiliccyanobacteriumwithintrichocoleusaceaetrichothermofontiasichuanensisgenetspnovanditsco2concentratingmechanism AT krzysztoffwaleron characterizationofanovelthermophiliccyanobacteriumwithintrichocoleusaceaetrichothermofontiasichuanensisgenetspnovanditsco2concentratingmechanism AT lianmingdu characterizationofanovelthermophiliccyanobacteriumwithintrichocoleusaceaetrichothermofontiasichuanensisgenetspnovanditsco2concentratingmechanism AT maurycydaroch characterizationofanovelthermophiliccyanobacteriumwithintrichocoleusaceaetrichothermofontiasichuanensisgenetspnovanditsco2concentratingmechanism |