Loss of cytochrome cM stimulates cyanobacterial heterotrophic growth in the dark

• Published in: Plant and cell physiology 2015-02, Vol.56 (2), p.334-345
• Main Authors: Hiraide, Yuto, Oshima, Kenshiro, Fujisawa, Takatomo, Uesaka, Kazuma, Hirose, Yuu, Tsujimoto, Ryoma, Yamamoto, Haruki, Okamoto, Shinobu, Nakamura, Yasukazu, Terauchi, Kazuki, Omata, Tatsuo, Ihara, Kunio, Hattori, Masahira, Fujita, Yuichi
• Format: Article
• Language: English
• Subjects: Base Sequence; Cyanobacteria - genetics; Cyanobacteria - growth & development; Cytochromes c - genetics; Darkness; Gene Rearrangement; Genome, Bacterial; Heterotrophic Processes - genetics; Mutation - genetics; Phenotype; Phylogeny; Synechocystis - genetics; Synechocystis - growth & development; Synechocystis - metabolism; Transformation, Genetic
• ISSN: 0032-0781; 1471-9053
• DOI: 10.1093/pcp/pcu165

Although cyanobacteria are photoautotrophs, they have the capability for heterotrophic metabolism that enables them to survive in their natural habitat. However, cyanobacterial species that grow heterotrophically in the dark are rare. It remains largely unknown how cyanobacteria regulate heterotrophic activity. The cyanobacterium Leptolyngbya boryana grows heterotrophically with glucose in the dark. A dark-adapted variant dg5 isolated from the wild type (WT) exhibits enhanced heterotrophic growth in the dark. We sequenced the genomes of dg5 and the WT to identify the mutation(s) of dg5. The WT genome consists of a circular chromosome (6,176,364 bp), a circular plasmid pLBA (77,793 bp) and two linear plasmids pLBX (504,942 bp) and pLBY (44,369 bp). Genome comparison revealed three mutation sites. Phenotype analysis of mutants isolated from the WT by introducing these mutations individually revealed that the relevant mutation is a single adenine insertion causing a frameshift of cytM encoding Cyt c(M). The respiratory oxygen consumption of the cytM-lacking mutant grown in the dark was significantly higher than that of the WT. We isolated a cytM-lacking mutant, ΔcytM, from another cyanobacterium Synechocystis sp. PCC 6803, and ΔcytM grew in the dark with a doubling time of 33 h in contrast to no growth of the WT. The respiratory oxygen consumption of ΔcytM grown in the dark was about 2-fold higher than that of the WT. These results suggest a suppressive role(s) for Cyt cM in regulation of heterotrophic activity.