Adaptation of a cyanobacterium to a biochemically rich environment in experimental evolution as an initial step toward a chloroplast-like state

Kazufumi Hosoda, Masumi Habuchi, Shingo Suzuki, Mikako Miyazaki, Go Takikawa, Takahiro Sakurai, Akiko Kashiwagi, Makoto Sueyoshi, Yusuke Matsumoto, Ayako Kiuchi, Kotaro Mori, Tetsuya Yomo

Research output: Contribution to journalArticle

4 Citations (Scopus)

Abstract

Chloroplasts originated from cyanobacteria through endosymbiosis. The original cyanobacterial endosymbiont evolved to adapt to the biochemically rich intracellular environment of the host cell while maintaining its photosynthetic function; however, no such process has been experimentally demonstrated. Here, we show the adaptation of a model cyanobacterium, Synechocystis sp. PCC 6803, to a biochemically rich environment by experimental evolution. Synechocystis sp. PCC 6803 does not grow in a biochemically rich, chemically defined medium because several amino acids are toxic to the cells at approximately 1 mM. We cultured the cyanobacteria in media with the toxic amino acids at 0.1 mM, then serially transferred the culture, gradually increasing the concentration of the toxic amino acids. The cells evolved to show approximately the same specific growth rate in media with 0 and 1 mM of the toxic amino acid in approximately 84 generations and evolved to grow faster in the media with 1 mM than in the media with 0 mM in approximately 181 generations. We did not detect a statistically significant decrease in the autotrophic growth of the evolved strain in an inorganic medium, indicating the maintenance of the photosynthetic function. Whole-genome resequencing revealed changes in the genes related to the cell membrane and the carboxysome. Moreover, we quantitatively analyzed the evolutionary changes by using simple mathematical models, which evaluated the evolution as an increase in the halfmaximal inhibitory concentration (IC 50) and estimated quantitative characteristics of the evolutionary process. Our results clearly demonstrate not only the potential of a model cyanobacterium to adapt to a biochemically rich environment without a significant decrease in photosynthetic function but also the properties of its evolutionary process, which sheds light of the evolution of chloroplasts at the initial stage.

Original languageEnglish
Article numbere98337
JournalPloS one
Volume9
Issue number5
DOIs
Publication statusPublished - May 29 2014

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Poisons
Cyanobacteria
Chloroplasts
chloroplasts
Synechocystis sp. PCC 6803
Synechocystis
Amino Acids
amino acids
Autotrophic Processes
Genes
Symbiosis
endosymbionts
cells
Cell membranes
specific growth rate
symbiosis
Inhibitory Concentration 50
inhibitory concentration 50
cell membranes
Theoretical Models

All Science Journal Classification (ASJC) codes

  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)

Cite this

Adaptation of a cyanobacterium to a biochemically rich environment in experimental evolution as an initial step toward a chloroplast-like state. / Hosoda, Kazufumi; Habuchi, Masumi; Suzuki, Shingo; Miyazaki, Mikako; Takikawa, Go; Sakurai, Takahiro; Kashiwagi, Akiko; Sueyoshi, Makoto; Matsumoto, Yusuke; Kiuchi, Ayako; Mori, Kotaro; Yomo, Tetsuya.

In: PloS one, Vol. 9, No. 5, e98337, 29.05.2014.

Research output: Contribution to journalArticle

Hosoda, K, Habuchi, M, Suzuki, S, Miyazaki, M, Takikawa, G, Sakurai, T, Kashiwagi, A, Sueyoshi, M, Matsumoto, Y, Kiuchi, A, Mori, K & Yomo, T 2014, 'Adaptation of a cyanobacterium to a biochemically rich environment in experimental evolution as an initial step toward a chloroplast-like state', PloS one, vol. 9, no. 5, e98337. https://doi.org/10.1371/journal.pone.0098337
Hosoda, Kazufumi ; Habuchi, Masumi ; Suzuki, Shingo ; Miyazaki, Mikako ; Takikawa, Go ; Sakurai, Takahiro ; Kashiwagi, Akiko ; Sueyoshi, Makoto ; Matsumoto, Yusuke ; Kiuchi, Ayako ; Mori, Kotaro ; Yomo, Tetsuya. / Adaptation of a cyanobacterium to a biochemically rich environment in experimental evolution as an initial step toward a chloroplast-like state. In: PloS one. 2014 ; Vol. 9, No. 5.
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