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The siderophilic cyanobacterium Leptolyngbya sp. strain JSC-1 acclimates to iron starvation by expressing multiple isiA-family genes

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Abstract

In the evolution of different cyanobacteria performing oxygenic photosynthesis, the core complexes of the two photosystems were highly conserved. However, cyanobacteria exhibit significant diversification in their light-harvesting complexes and have flexible regulatory mechanisms to acclimate to changes in their growth environments. In the siderophilic, filamentous cyanobacterium, Leptolyngbya sp. strain JSC-1, five different isiA-family genes occur in two gene clusters. During acclimation to Fe limitation, relative transcript levels for more than 600 genes increased more than twofold. Relative transcript levels were ~250 to 300 times higher for the isiA1 gene cluster (isiA1-isiB-isiC), and ~440- to 540-fold for the isiA2-isiA3-isiA4-cpcG2-isiA5 gene cluster after 48 h of iron starvation. Chl-protein complexes were isolated and further purified from cells grown under Fe-replete and Fe-depleted conditions. A single class of particles, trimeric PSI, was identified by image analysis of electron micrographs of negatively stained PSI complexes from Fe-replete cells. However, three major classes of particles were observed for the Chl-protein supercomplexes from cells grown under iron starvation conditions. Based on LC–MS–MS analyses, the five IsiA-family proteins were found in the largest supercomplexes together with core components of the two photosystems; however, IsiA5 was not present in complexes in which only the core subunits of PSI were detected. IsiA5 belongs to the same clade as PcbC proteins in a phylogenetic classification, and it is proposed that IsiA5 is most likely involved in supercomplexes containing PSII dimers. IsiA4, which is a fusion of an IsiA domain and a C-terminal PsaL domain, was found together with IsiA1, IsiA2, and IsiA3 in complexes with monomeric PSI. The data indicate that horizontal gene transfer, gene duplication, and divergence have played important roles in the adaptive evolution of this cyanobacterium to iron starvation conditions.

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Acknowledgments

The authors thankfully acknowledge the contributions of Patrick Saboe from Department of Chemical Engineering for TEM image collection and Dr. Tracy Nixon from Department of Biochemistry and Molecular Biology for assisting EVAN2 particle refinement analysis, both of The Pennsylvania State University, University Park. We would like to thank Dr. Hao Zhang from PARC LC–MS facility in Washington University in St. Louis for assistance with the mass spectrometric analyses. This work was supported by the National Science Foundation grant MCB-1021725 to D.A.B. This research was also conducted under the auspices of the Photosynthetic Antenna Research Center (PARC), an Energy Frontier Research Center funded by the DOE, Office of Science, Office of Basic Energy Sciences under Award Number DE-SC 0001035.

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    1. Department of Biochemistry and Molecular Biology, 4406 Althouse Laboratory, The Pennsylvania State University, University Park, PA, 16802, USA

      Gaozhong Shen, Fei Gan & Donald A. Bryant

    2. Department of Chemistry and Biochemistry, Montana State University, Bozeman, MT, 59717, USA

      Donald A. Bryant

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    Gaozhong Shen and Fei Gan have contributed equally to this study.

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    Shen, G., Gan, F. & Bryant, D.A. The siderophilic cyanobacterium Leptolyngbya sp. strain JSC-1 acclimates to iron starvation by expressing multiple isiA-family genes. Photosynth Res 128, 325–340 (2016). https://doi.org/10.1007/s11120-016-0257-7

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