Polyphasic Identification and Genomic Insights of Leptothermofonsia sichuanensis gen. sp. nov., a Novel Thermophilic Cyanobacteria Within Leptolyngbyaceae

Abstract

Thermal environments are an important reservoir of thermophiles with significant ecological and biotechnological potentials. However, thermophilic isolates remain largely unrecovered from their habitats and are rarely systematically identified. In this study, we characterized using polyphasic approaches a thermophilic strain, PKUAC-SCTAE412 (E412 hereafter), recovered from Lotus Lake hot spring based in Ganzi prefecture, China. The results of 16S rRNA/16S-23S ITS phylogenies, secondary structure, and morphology comparison strongly supported that strain E412 represent a novel genus within Leptolyngbyaceae. This delineation was further confirmed by genome-based analyses [phylogenomic inference, average nucleotide/amino-acid identity, and the percentages of conserved proteins (POCP)]. Based on the botanical code, the isolate is herein delineated as Leptothermofonsia sichuanensis gen. sp. nov, a genus adjacent to recently delineated Kovacikia and Stenomitos. In addition, we successfully obtained the first complete genome of this new genus. Genomic analysis revealed its adaptations to the adverse hot spring environment and extensive molecular components related to mobile genetic elements, photosynthesis, and nitrogen metabolism. Moreover, the strain was capable of modifying the composition of its light-harvesting apparatus depending on the wavelength and photoperiod, showing chromatic adaptation capacity characteristic for T1 and T2 pigmentation types. Other physiological studies showed the strain’s ability to utilize sodium bicarbonate and various sulfur compounds. The strain was also shown to be diazotrophic. Interestingly, 24.6% of annotated protein-coding genes in the E412 genome were identified as putatively acquired, hypothesizing that a large number of genes acquired through HGT might contribute to the genome expansion and habitat adaptation of those thermophilic strains. Most the HGT candidates (69.4%) were categorized as metabolic functions as suggested by the KEGG analysis. Overall, the complete genome of strain E412 provides the first insight into the genomic feature of the genus Leptothermofonsia and lays the foundation for future global ecogenomic and geogenomic studies.

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

“…The phylogenetic analysis of the 16S rRNA gene suggests the clear affiliation of Neosynechococcus sphagnicola sy1 to the family Leptolyngbyaceae ( Figure 1 ; Dvorak et al, 2014 ), whereas sy1 was located in a position within the genome-scale phylogram, forming a clade with two genera from family Trichocoleusaceae ( Figure 2 ). This position of the strain was consistent with the phylogenomic results reported in previous studies ( Tang et al, 2022a , b ). Taken together, the discordant two trees suggest that currently used approaches cannot determine whether the taxonomic position of sy1 is accurate.…”

“…Approximately 48.2% of protein-coding genes (2,098 out of 4,352) protein-coding genes were predicted to be hypothetical proteins. It was not surprising to identify such a high percentage of hypothetical protein in the B231 genome since similar observations are typical in the genomes of other thermophilic cyanobacteria ( Cheng et al, 2020 ; Kono et al, 2022 ; Tang et al, 2022a , b ).…”

Characterization of Molecular Diversity and Organization of Phycobilisomes in Thermophilic Cyanobacteria

“…The missing cysteine in apcE implies the non-covalent binding of phycocyanobilin and might relate to an important red-shift in the absorbance (e.g., 700 nm in the far-red Synechococcus PCC 7335, as opposed to 660 nm for covalent binding) [ 29 ]. Photoacclimation of a far-red light by Leptolyngbya JSC-1 and Leptothermofonsia E412 has been experimentally verified [ 30 , 31 ], and the responses to the ambient light environment might be mediated by two-component systems involved in signal transduction [ 32 ]. Moreover, the Ocullathermofonsia strain might expand the diverse array of far-red photosynthesizing cyanobacteria.…”

“…Briefly, the 19 thermophiles were taxonomically affiliated to six families of order Pseudanabaenales, Synechococcales, and Thermostichales, including Leptolyngbyaceae: Leptolyngbya sp. JSC-1 [ 53 ] and Leptothermofonsia sichuanensis E412 [ 31 ]; Oculatellaceae: Ocullathermofonsia sinensis A174, Thermoleptolyngbya sp. O-77 [ 54 ], and T. sichuanensis A183 [ 55 ]; Synechococcaceae: Synechococcus sp.…”

Comparative Genomic Analysis Revealed Distinct Molecular Components and Organization of CO2-Concentrating Mechanism in Thermophilic Cyanobacteria

“…Briefly, the 16 thermophiles were affiliated to four families of order Pseudanabaenales and Synechococcales, including Leptolyngbyaceae: Leptodesmis sichuanensis A121 (Tang et al, 2022a), Leptolyngbya sp. JSC-1 (Brown et al, 2010), Leptothermofonsia sichuanensis E412 (Tang et al, 2022b); Oculatellaceae: Thermoleptolyngbya sp. O-77 (Yoon et al, 2017), T. sichuanensis A183 (Tang et al, 2021); Synechococcaceae: Synechococcus sp.…”