Characterization of a novel thermophilic cyanobacterium within Trichocoleusaceae, Trichothermofontia sichuanensis gen. et sp. nov., and its CO2-concentrating mechanism

Abstract

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.

Genome-scale identification and comparative analysis of transcription factors in thermophilic cyanobacteria

“…taiwanensis CL-1 [ 29 ] and TA-1 [ 30 ], T. vestitus BP-1 [ 31 ], Thermosynechococcus sp. M46_R2017_013 and M98_K2018_005 (hereafter M46 and M98) [ 32 ]; and Trichocoleusaceae: Trichothermofontia sichuanensis B231 [ 33 ]. The genome, protein sequences, and genomic annotations of the thermophilic cyanobacteria collected were retrieved from the genomic resources of the NCBI.…”

Thermophilic cyanobacteria—exciting, yet challenging biotechnological chassis

“…Several series of studies looking at novel thermophilic isolates proved to be successful in significantly expanding knowledge about new thermophilic cyanobacteria. A research line originating from western Sichuan hot springs sampling project (Tang et al 2018) resulted in the delineation of three new genera (Tang et al 2022b(Tang et al , 2023Jiang et al 2023) and the sequencing of several new genomes of novel species (Tang et al 2021(Tang et al , 2022a. Elsewhere, a comprehensive study of cyanobacteria isolated from hot springs in Iceland, Poland, Greece, and Tajikistan resulted in thirteen new isolates and the delineation of two new genera (Jasser et al 2022).…”

“…In recent years, there has been a renewed interest in these organisms leading to a significant expansion of knowledge about their taxa, properties, metabolism, and biotechnological potential (Saini et al 2021). This is particularly evident in the recent surge in the delineation of novel thermophilic taxa such as the following Thermoleptolyngbya (Sciuto and Moro 2016), Thermostichus (Komárek et al 2020), Leptothermofonsia (Tang et al 2022b), Trichothermofontia (Tang et al 2023), or Thermocoleostomius (Jiang et al 2023). These are often combined with the collection and analysis of extensive genomic data about representative thermophilic isolates (Tang et al 2022c).…”

Polyphasic characterization of a novel hot-spring cyanobacterium Thermocoleostomius sinensis gen et sp. nov. and genomic insights into its carbon concentration mechanism

“…To enhance the credibility of taxonomic revisions, it is crucial, in our opinion, to incorporate comparative genomic analyses to strain descriptions that include morphological and ecological data. Examples of revisions that have been backed by genomic data include the delineation of Thermoleptolynbya (Sciuto and Moro, 2016 ) and Trichothermofontia (Tang et al, 2023 ). While many of the delineations that originally did not include comparative genomics were already confirmed and expanded thanks to those datasets (Strunecký et al, 2023 ), in many other instances it was not possible due to sequence unavailability.…”