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

Abstract

Cyanobacteria evolved an inorganic carbon-concentrating mechanism (CCM) to perform effective oxygenic photosynthesis and prevent photorespiratory carbon losses. This process facilitates the acclimation of cyanobacteria to various habitats, particularly in CO2-limited environments. To date, there is limited information on the CCM of thermophilic cyanobacteria whose habitats limit the solubility of inorganic carbon. Here, genome-based approaches were used to identify the molecular components of CCM in 17 well-described thermophilic cyanobacteria. These cyanobacteria were from the genus Leptodesmis, Leptolyngbya, Leptothermofonsia, Thermoleptolyngbya, Thermostichus, and Thermosynechococcus. All the strains belong to β-cyanobacteria based on their β-carboxysome shell proteins with 1B form of Rubisco. The diversity in the Ci uptake systems and carboxysome composition of these thermophiles were analyzed based on their genomic information. For Ci uptake systems, two CO2 uptake systems (NDH-13 and NDH-14) and BicA for HCO3– transport were present in all the thermophilic cyanobacteria, while most strains did not have the Na+/HCO3– Sbt symporter and HCO3– transporter BCT1 were absent in four strains. As for carboxysome, the β-carboxysomal shell protein, ccmK2, was absent only in Thermoleptolyngbya strains, whereas ccmK3/K4 were absent in all Thermostichus and Thermosynechococcus strains. Besides, all Thermostichus and Thermosynechococcus strains lacked carboxysomal β-CA, ccaA, the carbonic anhydrase activity of which may be replaced by ccmM proteins as indicated by comparative domain analysis. The genomic distribution of CCM-related genes was different among the thermophiles, suggesting probably distinct expression regulation. Overall, the comparative genomic analysis revealed distinct molecular components and organization of CCM in thermophilic cyanobacteria. These findings provided insights into the CCM components of thermophilic cyanobacteria and fundamental knowledge for further research regarding photosynthetic improvement and biomass yield of thermophilic cyanobacteria with biotechnological potentials.

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

“…Herein, the ML phylogram of rbcL positions strain B231 within the category of β-cyanobacteria ( Figure 3 ), indicating the presence of RubisCO 1B form in this thermophile. This result was in accordance with a previous study that surveyed 17 thermophilic cyanobacteria and allocated them to the β-cyanobacteria ( Tang et al, 2022d ). Nevertheless, strain B231 clusters with none of these thermophilic cyanobacteria but is uniquely positioned among mesophilic cyanobacteria ( Figure 3 ), suggesting considerable genetic diversity of rbcL amino acid sequences among these thermophiles.…”

“…Orthologous proteins involved in CCM of strain B231 were identified as previously described ( Tang et al, 2022d ). Briefly, amino acid sequences of 28 proteins involved in CCM of Synechocystis sp.…”

Comparative analysis reveals distinctive genomic features of Taiwan hot-spring cyanobacterium Thermosynechococcus sp. TA-1

“…The taxonomy of these cyanobacteria has been under active revision in recent years ( Liang et al, 2019 ; Komarek et al, 2020 ; Prondzinsky et al, 2021 ; Tang et al, 2022 ). To avoid confusion, we utilized strain names as the major identifiers in this work and described the scientific names based on the associated GenBank records ( Table 1 ) when necessary for trackability.…”

“…One MAG, OHK43 from Japan, was omitted because this assembly (accession JACOMP000000000 ) has > 99.6% ANI with NK55, is highly fragmented with 273 contigs, and lacks annotation. S. lividus PCC 6715, which has been demonstrated as a sister lineage of Thermosynechococcus ( Liang et al, 2019 ; Komarek et al, 2020 ; Tang et al, 2022 ), was included as an outgroup. The annotation was based on those provided in the GenBank files.…”

Characterization of Molecular Diversity and Organization of Phycobilisomes in Thermophilic Cyanobacteria

“…C9 [ 56 ]; Thermostichaceae: Thermostichus sp. 60AY4M2, 63AY4M2, 65AY6A5, 65AY6Li [ 57 ], JA-2-3B, and JA-3-3Ab [ 58 ]; Thermosynechococcaceae: Thermosynechococcus lividus PCC 6715 [ 59 ], Thermosynechococcus sp. CL-1 [ 60 ] and TA-1 [ 61 ], T. vestitus BP-1 [ 62 ], and E542 [ 63 ], T. vulcanus NIES-2134 [ 16 ]; and Trichocoleusaceae: Trichothermofonsia sichuanensis B231.…”