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Phosphorus deficiency alleviates iron limitation in Synechocystis cyanobacteria through direct PhoB-mediated gene regulation

Author

Listed:
  • Guo-Wei Qiu

    (Central China Normal University)

  • Wen-Can Zheng

    (Central China Normal University)

  • Hao-Ming Yang

    (Central China Normal University)

  • Yu-Ying Wang

    (Central China Normal University)

  • Xing Qi

    (Central China Normal University)

  • Da Huang

    (Central China Normal University)

  • Guo-Zheng Dai

    (Central China Normal University)

  • Huazhong Shi

    (Texas Tech University)

  • Neil M. Price

    (McGill University)

  • Bao-Sheng Qiu

    (Central China Normal University)

Abstract

Iron and phosphorus are essential nutrients that exist at low concentrations in surface waters and may be co-limiting resources for phytoplankton growth. Here, we show that phosphorus deficiency increases the growth of iron-limited cyanobacteria (Synechocystis sp. PCC 6803) through a PhoB-mediated regulatory network. We find that PhoB, in addition to its well-recognized role in controlling phosphate homeostasis, also regulates key metabolic processes crucial for iron-limited cyanobacteria, including ROS detoxification and iron uptake. Transcript abundances of PhoB-targeted genes are enriched in samples from phosphorus-depleted seawater, and a conserved PhoB-binding site is widely present in the promoters of the target genes, suggesting that the PhoB-mediated regulation may be highly conserved. Our findings provide molecular insights into the responses of cyanobacteria to simultaneous iron/phosphorus nutrient limitation.

Suggested Citation

  • Guo-Wei Qiu & Wen-Can Zheng & Hao-Ming Yang & Yu-Ying Wang & Xing Qi & Da Huang & Guo-Zheng Dai & Huazhong Shi & Neil M. Price & Bao-Sheng Qiu, 2024. "Phosphorus deficiency alleviates iron limitation in Synechocystis cyanobacteria through direct PhoB-mediated gene regulation," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-48847-4
    DOI: 10.1038/s41467-024-48847-4
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    References listed on IDEAS

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    1. Joanne S. Boden & Kurt O. Konhauser & Leslie J. Robbins & Patricia Sánchez-Baracaldo, 2021. "Timing the evolution of antioxidant enzymes in cyanobacteria," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    2. Enqing Hou & Yiqi Luo & Yuanwen Kuang & Chengrong Chen & Xiankai Lu & Lifen Jiang & Xianzhen Luo & Dazhi Wen, 2020. "Global meta-analysis shows pervasive phosphorus limitation of aboveground plant production in natural terrestrial ecosystems," Nature Communications, Nature, vol. 11(1), pages 1-9, December.
    3. T. J. Browning & E. P. Achterberg & J. C. Yong & I. Rapp & C. Utermann & A. Engel & C. M. Moore, 2017. "Iron limitation of microbial phosphorus acquisition in the tropical North Atlantic," Nature Communications, Nature, vol. 8(1), pages 1-7, August.
    4. Thomas J. Browning & Eric P. Achterberg & Insa Rapp & Anja Engel & Erin M. Bertrand & Alessandro Tagliabue & C. Mark Moore, 2017. "Nutrient co-limitation at the boundary of an oceanic gyre," Nature, Nature, vol. 551(7679), pages 242-246, November.
    5. Hye-In Nam & Zaigham Shahzad & Yanniv Dorone & Sophie Clowez & Kangmei Zhao & Nadia Bouain & Katerina S. Lay-Pruitt & Huikyong Cho & Seung Y. Rhee & Hatem Rouached, 2021. "Interdependent iron and phosphorus availability controls photosynthesis through retrograde signaling," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    6. Scott C. Doney, 2006. "Plankton in a warmer world," Nature, Nature, vol. 444(7120), pages 695-696, December.
    7. Ye Tian & Chupei Shi & Carolina Urbina Malo & Steve Kwatcho Kengdo & Jakob Heinzle & Erich Inselsbacher & Franz Ottner & Werner Borken & Kerstin Michel & Andreas Schindlbacher & Wolfgang Wanek, 2023. "Long-term soil warming decreases microbial phosphorus utilization by increasing abiotic phosphorus sorption and phosphorus losses," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
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