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Cyanobacteria, one of the most widespread photoautotrophic microorganisms on Earth, have evolved an inorganic CO₂-concentrating mechanism (CCM) to adapt to a variety of habitats, especially in CO₂-limited environments. <i>Leptolyngbya boryana</i>, a filamentous cyanobacterium, is widespread in a variety of environments and is well adapted to low-inorganic-carbon environments. However, little is currently known about the CCM of <i>L. boryana</i>, in particular its efficient carbon fixation module. In this study, we isolated and purified the cyanobacterium CZ1 from the Xin’anjiang River basin and identified it as <i>L. boryana</i> by 16S rRNA sequencing. Genome analysis revealed that <i>L. boryana</i> CZ1 contains β-carboxysome shell proteins and form 1B of Rubisco, which is classify it as belonging to the β-cyanobacteria. Further analysis revealed that <i>L. boryana</i> CZ1 employs a fine CCM involving two CO₂ uptake systems NDH-1₃ and NDH-1₄, three HCO₃⁻ transporters (SbtA, BicA, and BCT1), and two carboxysomal carbonic anhydrases. Notably, we found that NDH-1₃ and NDH-1₄ are located close to each other in the <i>L. boryana</i> CZ1 genome and are back-to-back with the <i>ccm</i> operon, which is a novel gene arrangement. In addition, <i>L. boryana</i> CZ1 encodes two high-affinity Na⁺/HCO₃⁻ symporters (SbtA1 and SbtA2), three low-affinity Na⁺-dependent HCO₃⁻ transporters (BicA1, BicA2, and BicA3), and a BCT1; it is rare for a single strain to encode all three bicarbonate transporters in such large numbers. Interestingly, <i>L. boryana</i> CZ1 also uniquely encodes two active carbonic anhydrases, CcaA1 and CcaA2, which are also rare. Taken together, all these results indicated that <i>L. boryana</i> CZ1 is more efficient at CO₂ fixation. Moreover, compared with the reported CCM gene arrangement of cyanobacteria, the CCM-related gene distribution pattern of <i>L. boryana</i> CZ1 was completely different, indicating a novel gene organization structure. These results can enrich our understanding of the CCM-related gene arrangement of cyanobacteria, and provide data support for the subsequent improvement and increase in biomass through cyanobacterial photosynthesis.