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

Abstract

Thermophilic cyanobacteria play a crucial role as primary producers in hot spring ecosystems, yet their microbiological, taxonomic, and ecological characteristics are not extensively studied. This study aimed to characterize a novel strain of thermophilic cyanobacteria, PKUAC-SCTA174 (A174), using a combination of traditional polyphasic methods and modern genomic-based approaches. The study included 16S rRNA-based phylogeny, ITS secondary structure prediction, morphological and habitat analyses, as well as high-quality genome sequencing with corresponding phylogenomic analyses. The results of the 16S rRNA, 16S-23S ITS secondary structure, morphology, and habitat analyses supported the classification of the strain as a member of a novel genus within the family Oculatellaceae, closely related to Albertania and Trichotorquatus. Genomic analysis revealed the presence of a sophisticated carbon-concentrating mechanism (CCM) in the strain, involving two CO2 uptake systems NDH-I3, and NDH-I4, three types of bicarbonate transporters (BCT1, bicA, sbtA,) and two distinct putative carboxysomal carbonic anhydrases (ccaA1 and ccaA2). The expression of CCM genes was investigated with a CO2 shift experiment, indicating varying transcript abundance among different carbon uptake systems. Based on the comprehensive characterization, the strain was delineated as Thermocoleostomius sinensis, based on the botanical code. The study of the complete genome of strain A174 contributes valuable insights into the genetic characteristics of the genus Thermocoleostomius and related organisms and provides a systematic understanding of thermophilic cyanobacteria. The findings presented here offer valuable data that can be utilized for future research in taxogenomics, ecogenomics, and geogenomics.

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

“…Briefly, the 22 thermophiles were taxonomically assigned to six families, including Leptolyngbyaceae: Leptodesmis sichuanensis A121 [ 19 ] and Leptothermofonsia sichuanensis E412 [ 20 ]; Oculatellaceae: Leptolyngbya sp. JSC-1 [ 21 ], Thermocoleostomius sinensis A174 [ 22 ], Thermoleptolyngbya sp. O-77 [ 23 ] and T. sichuanensis A183 [ 24 ]; Gloeomargaritaceae: Synechococcus sp.…”

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).…”

Microflora Danica: the atlas of Danish environmental microbiomes

“…Considering which prokaryotic orders were the most important in discriminating among habitats, the strongest signal was provided by Solirubrobacteriales, whose species have been found in soils and roots, but accounted for the largest relative abundance in deserts 37 . Coherently with literature, relative abundance of Solirubrobacterales showed a peak in "Fixed dunes" and "Xeric sand calcareous grasslands", whilst being present, to a minor extent, in other habitats and, perhaps, functioning as a general proxy for sand content in the samples.…”