IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-48847-4.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-48847-4
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-48847-4?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    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.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Thomas J. Browning & C. Mark Moore, 2023. "Global analysis of ocean phytoplankton nutrient limitation reveals high prevalence of co-limitation," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    2. Joanne S. Boden & Juntao Zhong & Rika E. Anderson & Eva E. Stüeken, 2024. "Timing the evolution of phosphorus-cycling enzymes through geological time using phylogenomics," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    3. Dongyan Liu & Chongran Zhou & John K. Keesing & Oscar Serrano & Axel Werner & Yin Fang & Yingjun Chen & Pere Masque & Janine Kinloch & Aleksey Sadekov & Yan Du, 2022. "Wildfires enhance phytoplankton production in tropical oceans," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    4. Sanghwa Lee & Julia Showalter & Ling Zhang & Gaëlle Cassin-Ross & Hatem Rouached & Wolfgang Busch, 2024. "Nutrient levels control root growth responses to high ambient temperature in plants," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    5. Evangelos Tzanatos & Dionysios Raitsos & George Triantafyllou & Stylianos Somarakis & Anastasios Tsonis, 2014. "Indications of a climate effect on Mediterranean fisheries," Climatic Change, Springer, vol. 122(1), pages 41-54, January.
    6. Natalie R. Cohen & Arianna I. Krinos & Riss M. Kell & Rebecca J. Chmiel & Dawn M. Moran & Matthew R. McIlvin & Paloma Z. Lopez & Alexander J. Barth & Joshua P. Stone & Brianna A. Alanis & Eric W. Chan, 2024. "Microeukaryote metabolism across the western North Atlantic Ocean revealed through autonomous underwater profiling," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    7. Liuyang Li & Danyue Huang & Yaoxun Hu & Nicola M. Rudling & Daniel P. Canniffe & Fengping Wang & Yinzhao Wang, 2023. "Globally distributed Myxococcota with photosynthesis gene clusters illuminate the origin and evolution of a potentially chimeric lifestyle," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    8. Nils Giordano & Marinna Gaudin & Camille Trottier & Erwan Delage & Charlotte Nef & Chris Bowler & Samuel Chaffron, 2024. "Genome-scale community modelling reveals conserved metabolic cross-feedings in epipelagic bacterioplankton communities," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    9. Chen, Lingyun & Hu, Ziyi & Chen, Wenhui & Xu, Ziwei & Hao, Can & Lakshmanan, Prakash & Liu, Dunyi & Chen, Xinping, 2023. "Comparative study of the effectiveness of nano-sized iron-containing particles as a foliar top-dressing of peanut in rainy conditions," Agricultural Water Management, Elsevier, vol. 286(C).
    10. Asada, K. & Kanda, T. & Yamashita, N. & Asano, M. & Eguchi, S., 2022. "Interpreting stoichiometric homeostasis and flexibility of soil microbial biomass carbon, nitrogen, and phosphorus," Ecological Modelling, Elsevier, vol. 470(C).
    11. Haoyu Jin & Chao Zhang & Siyu Meng & Qin Wang & Xiaokun Ding & Ling Meng & Yunyun Zhuang & Xiaohong Yao & Yang Gao & Feng Shi & Thomas Mock & Huiwang Gao, 2024. "Atmospheric deposition and river runoff stimulate the utilization of dissolved organic phosphorus in coastal seas," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    12. Futing Zhang & Zuozhu Wen & Shanlin Wang & Weiyi Tang & Ya-Wei Luo & Sven A. Kranz & Haizheng Hong & Dalin Shi, 2022. "Phosphate limitation intensifies negative effects of ocean acidification on globally important nitrogen fixing cyanobacterium," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    13. Holly Edwards, 2013. "Potential impacts of climate change on warmwater megafauna: the Florida manatee example (Trichechus manatus latirostris)," Climatic Change, Springer, vol. 121(4), pages 727-738, December.
    14. Lee, Soonmi & Yoo, Sinjae, 2016. "Interannual variability of the phytoplankton community by the changes in vertical mixing and atmospheric deposition in the Ulleung Basin, East Sea: A modelling study," Ecological Modelling, Elsevier, vol. 322(C), pages 31-47.
    15. Han, Yue & Zhou, Yuntao, 2022. "Investigating biophysical control of marine phytoplankton dynamics via Bayesian mechanistic modeling," Ecological Modelling, Elsevier, vol. 474(C).
    16. David S. Ellsworth & Kristine Y. Crous & Martin G. Kauwe & Lore T. Verryckt & Daniel Goll & Sönke Zaehle & Keith J. Bloomfield & Philippe Ciais & Lucas A. Cernusak & Tomas F. Domingues & Mirindi Eric , 2022. "Convergence in phosphorus constraints to photosynthesis in forests around the world," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    17. Wang, Linlin & Xie, Junhong & Luo, Zhuzhu & Niu, Yining & Coulter, Jeffrey A. & Zhang, Renzhi & Lingling, Li, 2021. "Forage yield, water use efficiency, and soil fertility response to alfalfa growing age in the semiarid Loess Plateau of China," Agricultural Water Management, Elsevier, vol. 243(C).
    18. Yan Bai & Xianqiang He & Shujie Yu & Chen-Tung Arthur Chen, 2018. "Changes in the Ecological Environment of the Marginal Seas along the Eurasian Continent from 2003 to 2014," Sustainability, MDPI, vol. 10(3), pages 1-15, February.
    19. Minji Lee & Yun-Bae Kim & Chan-Hong Park & Seung-Ho Baek, 2022. "Characterization of Seasonal Phytoplankton Pigments and Functional Types around Offshore Island in the East/Japan Sea, Based on HPLC Pigment Analysis," Sustainability, MDPI, vol. 14(9), pages 1-17, April.
    20. Can Liu & Zhen Bai & Yu Luo & Yanfeng Zhang & Yongfeng Wang & Hexin Liu & Meng Luo & Xiaofang Huang & Anle Chen & Lige Ma & Chen Chen & Jinwei Yuan & Ying Xu & Yantao Zhu & Jianxin Mu & Ran An & Cuili, 2024. "Multiomics dissection of Brassica napus L. lateral roots and endophytes interactions under phosphorus starvation," Nature Communications, Nature, vol. 15(1), pages 1-18, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-48847-4. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.