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Membrane organization of photosystem I complexes in the most abundant phototroph on Earth

Nature Plants volume 5, pages 879–889 (2019)Cite this article

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Abstract

Prochlorococcus is a major contributor to primary production, and globally the most abundant photosynthetic genus of picocyanobacteria because it can adapt to highly stratified low-nutrient conditions that are characteristic of the surface ocean. Here, we examine the structural adaptations of the photosynthetic thylakoid membrane that enable different Prochlorococcus ecotypes to occupy high-light, low-light and nutrient-poor ecological niches. We used atomic force microscopy to image the different photosystem I (PSI) membrane architectures of the MED4 (high-light) Prochlorococcus ecotype grown under high-light and low-light conditions in addition to the MIT9313 (low-light) and SS120 (low-light) Prochlorococcus ecotypes grown under low-light conditions. Mass spectrometry quantified the relative abundance of PSI, photosystem II (PSII) and cytochrome b6f complexes and the various Pcb proteins in the thylakoid membrane. Atomic force microscopy topographs and structural modelling revealed a series of specialized PSI configurations, each adapted to the environmental niche occupied by a particular ecotype. MED4 PSI domains were loosely packed in the thylakoid membrane, whereas PSI in the low-light MIT9313 is organized into a tightly packed pseudo-hexagonal lattice that maximizes harvesting and trapping of light. There are approximately equal levels of PSI and PSII in MED4 and MIT9313, but nearly twofold more PSII than PSI in SS120, which also has a lower content of cytochrome b6f complexes. SS120 has a different tactic to cope with low-light levels, and SS120 thylakoids contained hundreds of closely packed Pcb–PSI supercomplexes that economize on the extra iron and nitrogen required to assemble PSI-only domains. Thus, the abundance and widespread distribution of Prochlorococcus reflect the strategies that various ecotypes employ for adapting to limitations in light and nutrient levels.

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Fig. 1: AFM of PSI in thylakoid membrane patches from LL-grown MED4.
Fig. 2: AFM of PSI in MED4 thylakoid membrane patches grown under HL.
Fig. 3: AFM of PSI in thylakoid membrane patches from MIT9313.
Fig. 4: AFM imaging of clustered Pcb–PSI supercomplexes in thylakoid membrane patches from SS120.
Fig. 5: Medium resolution AFM topograph of a large membrane patch from the SS120 ecotype.
Fig. 6: Structural models for the PSI trimer domains from the Prochlorococcus ecotypes MIT9313, MED4 and SS120 grown under LL.
Fig. 7: Comparison of the relative levels of PSI, PSII, cytochrome b6f, ATP synthase and Pcb proteins in Prochlorococcus ecotypes MED4, MIT9313 and SS120.

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Data availability

The mass spectrometry proteomics data have been deposited to the ProteomeXchange Consortium via the PRIDE partner repository (http://proteomecentral.proteomexchange.org) with the data set identifier PXD013506. All other data can be obtained from the corresponding author upon request. The following figures have associated raw data: Fig. 7, Supplementary Figs. 2–5.

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Acknowledgements

This work was supported by Advanced Award 338895 from the European Research Council which funded C.M.-C., P.J.J., J.W.C. and P.Q. and provided partial support for C.N.H. The authors C.N.H. and A.H. also gratefully acknowledge financial support from the Biotechnology and Biological Sciences Research Council (BBSRC UK), award number BB/M000265/1. C.N.H., M.S. and Z.L.-S. were supported by the Photosynthetic Antenna Research Center, an Energy Frontier Research Center funded by the US Department of Energy, Office of Science, Office of Basic Energy Sciences under award number DE-SC 0001035. M.S. and Z.L.-S. were also supported by the National Science Foundation (grant no. MCB1616590) and the National Institutes of Health (grant no. 9P41GM104601). D.J.S. acknowledges funding from NERC (grant no. NE/N003241/1) and The Leverhulme Trust (grant no. RPG-2014-354). M.J.D. acknowledges support from the BBSRC UK (grant no. BB/M012166/1). M.P.J. would like to acknowledge BBSRC grant no. BB/P002005/1 and the Grantham Centres for Sustainable Futures, University of Sheffield, for G.E.M.’s studentship.

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Authors and Affiliations

  1. Department of Molecular Biology and Biotechnology, University of Sheffield, Sheffield, UK

    C. MacGregor-Chatwin, P. J. Jackson, J. W. Chidgey, A. Hitchcock, P. Qian, G. E. Mayneord, M. P. Johnson & C. N. Hunter

  2. ChELSI Institute, Department of Chemical and Biological Engineering, University of Sheffield, Sheffield, UK

    P. J. Jackson & M. J. Dickman

  3. Beckman Institute for Advanced Science and Technology, University of Illinois at Urbana-Champaign, Urbana, IL, USA

    M. Sener & Z. Luthey-Schulten

  4. Department of Physics, University of Illinois at Urbana-Champaign, Urbana, IL, USA

    M. Sener & Z. Luthey-Schulten

  5. School of Life Sciences, University of Warwick, Coventry, UK

    D. J. Scanlan

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  1. C. MacGregor-Chatwin
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Contributions

C.M.-C., D.J.S. and C.N.H. designed the research. C.M.-C., P.J.J., M.S., J.W.C., A.H., P.Q., M.J.D., G.E.M. and D.J.S. performed the research. C.M.-C., M.S., M.P.J., Z.L.-S. and C.N.H. wrote the paper.

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Correspondence to C. N. Hunter.

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MacGregor-Chatwin, C., Jackson, P.J., Sener, M. et al. Membrane organization of photosystem I complexes in the most abundant phototroph on Earth. Nat. Plants 5, 879–889 (2019). https://doi.org/10.1038/s41477-019-0475-z

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