Photosynthetica 2018, 56(1):322-333 | DOI: 10.1007/s11099-018-0787-7

Function, regulation and distribution of IsiA, a membrane-bound chlorophyll a-antenna protein in cyanobacteria

H. Y.S. Chen1, A. Bandyopadhyay2, H. B. Pakrasi1,2,*
1 Department of Energy, Environmental, and Chemical Engineering, Washington University, St. Louis, USA
2 Department of Biology, Washington University, St. Louis, USA

IsiA is a membrane-bound Chl a-antenna protein synthesized in cyanobacteria under iron deficiency. Since iron deficiency is a common nutrient stress in significant fractions of cyanobacterial habitats, IsiA is likely to be essential for some cyanobacteria. However, the role it plays in cyanobacteria is not fully understood. In this review paper, we summarize the research efforts directed towards characterizing IsiA over the past three decades and attempt to bring all the pieces of the puzzle together to get a more comprehensive understanding of the function of this protein. Moreover, we analyzed the genomes of over 390 cyanobacterial strains available in the JGI/IMG database to assess the distribution of IsiA across the cyanobacterial kingdom. Our study revealed that only 125 such strains have an IsiA homolog, suggesting that the presence of this protein is a niche specific requirement, and cyanobacterial strains that lack IsiA might have developed other mechanisms to survive iron deficiency.

Keywords: environmental stress; excitation energy transfer; gene regulation; photoprotection; photosynthesis; phylogenetic analysis

Received: August 24, 2017; Accepted: December 14, 2017; Published: March 1, 2018Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Chen, H.Y.S., Bandyopadhyay, A., & Pakrasi, H.B. (2018). Function, regulation and distribution of IsiA, a membrane-bound chlorophyll a-antenna protein in cyanobacteria. Photosynthetica, 56(1), 322-333. doi: 10.1007/s11099-018-0787-7.
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)

    • Open full article

    References

    1. Andrizhiyevskaya E.G., Frolov D., van Grondelle R. et al.: Energy transfer and trapping in the Photosystem I complex of Synechococcus PCC 7942 and in its supercomplex with IsiA.-BBA-Bioenergetics 1656: 104-113, 2004. Go to original source...
    2. Andrizhiyevskaya E.G., Schwabe T.M., Germano M. et al.: Spectroscopic properties of PSI-IsiA supercomplexes from the cyanobacterium Synechococcus PCC 7942.-BBA-Bioenergetics 1556: 265-272, 2002. Go to original source...
    3. Ardelean I., Matthijs H.C., Havaux M. et al.: Unexpected changes in photosystem I function in a cytochrome c6-deficient mutant of the cyanobacterium Synechocystis PCC 6803.-FEMS Microbiol. Lett. 213: 113-119, 2002. Go to original source...
    4. Bailey S., Mann N.H., Robinson C. et al.: The occurrence of rapidly reversible non-photochemical quenching of chlorophyll a fluorescence in cyanobacteria.-FEBS Lett. 579: 275-280, 2005. Go to original source...
    5. Bandyopadhyay A., Elvitigala T., Welsh E. et al.: Novel metabolic attributes of the genus Cyanothece, comprising a group of unicellular nitrogen-fixing cyanobacteria.-MBio. 2: e00214-00211, 2011. Go to original source...
    6. Barber J., Morris E., Büchel C.: Revealing the structure of the photosystem II chlorophyll binding proteins, CP43 and CP47.-BBA-Bioenergetics 1459: 239-247, 2000. Go to original source...
    7. Behrenfeld M.J., Worthington K., Sherrell R. M. et al.: Controls on tropical Pacific Ocean productivity revealed through nutrient stress diagnostics.-Nature 442: 1025-1028, 2006. Go to original source...
    8. Berera R., van Stokkum I.H., d'Haene S. et al: A mechanism of energy dissipation in cyanobacteria.-Biophys. J. 96: 2261-2267, 2009. Go to original source...
    9. Berera R., van Stokkum I.H., Kennis J. T. et al.: The lightharvesting function of carotenoids in the cyanobacterial stressinducible IsiA complex.-Chem. Phys. 373: 65-70, 2010. Go to original source...
    10. Bibby T.S., Nield J., Barber J.: Iron deficiency induces the formation of an antenna ring around trimeric photosystem I in cyanobacteria.-Nature 412: 743-745, 2001a. Go to original source...
    11. Bibby T.S., Nield J., Barber J.: Three-dimensional model and characterization of the iron stress-induced CP43'-photosystem I supercomplex isolated from the cyanobacterium Synechocystis PCC 6803.-J. Biol. Chem. 276: 43246-43252, 2001b. Go to original source...
    12. Bibby T.S., Zhang Y., Chen M.: Biogeography of photosynthetic light-harvesting genes in marine phytoplankton.-PLoS ONE 4: e4601, 2009. Go to original source...
    13. Boekema E.J., Hifney A., Yakushevska A.E. et al: A giant chlorophyll-protein complex induced by iron deficiency in cyanobacteria.-Nature 412: 745-748, 2001. Go to original source...
    14. Burnap R.L., Troyan T., Sherman L.A.: The highly abundant chlorophyll-protein complex of iron-deficient Synechococcus sp. PCC7942 (CP43) is encoded by the isiA gene.-Plant Physiol. 103: 893-902, 1993. Go to original source...
    15. Cadoret J. C., Demoulière R., Lavaud J. et al.: Dissipation of excess energy triggered by blue light in cyanobacteria with CP43' (isiA).-BBA-Bioenergetics 1659: 100-104, 2004. Go to original source...
    16. Chauhan D., Folea I.M., Jolley C.C. et al: A novel photosynthetic strategy for adaptation to low-iron aquatic environments.-Biochemistry 50: 686-692, 2011. Go to original source...
    17. Chen H.S., Liberton M., Pakrasi H.B. et al.: Reevaluating the mechanism of excitation energy regulation in iron-starved cyanobacteria.-BBA-Bioenergetics 1858: 249-258, 2017.
    18. Coale K.H., Johnson K.S., Fitzwater S.E. et al: A massive phytoplankton bloom induced by an ecosystem-scale iron fertilization experiment in the equatorial Pacific Ocean.-Nature 383: 495-501, 1996. Go to original source...
    19. Daddy S., Zhan J., Jantaro S. et al: A novel high light-inducible carotenoid-binding protein complex in the thylakoid membranes of Synechocystis PCC 6803.-Sci. Rep. 5: 9480, 2015. Go to original source...
    20. Donia M.S., Fricke W.F., Partensky F. et al.: Complex microbiome underlying secondary and primary metabolism in the tunicate-Prochloron symbiosis.-P. Natl. Acad. Sci. USA 108: E1423-E1432, 2011. Go to original source...
    21. Duhring U., Axmann I.M., Hess W.R. et al.: An internal antisense RNA regulates expression of the photosynthesis gene isiA.-P. Natl. Acad. Sci. USA 103: 7054-7058, 2006. Go to original source...
    22. Falk S., Samson G., Bruce D. et al.: Functional analysis of the iron-stress induced CP 43' polypeptide of PS II in the cyanobacterium Synechococcus sp. PCC 7942.-Photosynth. Res. 45: 51-60, 1995. Go to original source...
    23. Felsenstein J.: Confidence-limits on phylogenies-an approach using the bootstrap.-Evolution 39: 783-791, 1985. Go to original source...
    24. Feng X., Neupane B., Acharya K. et al.: Spectroscopic study of the CP43' complex and the PSI-CP43' supercomplex of the cyanobacterium Synechocystis PCC 6803.-J. Phys. Chem. B 115: 13339-13349, 2011.
    25. Ferreira K.N., Iverson T.M., Maghlaoui K. et al.: Architecture of the photosynthetic oxygen-evolving center.-Science 303: 1831-1838, 2004. Go to original source...
    26. Fitzgerald M.P., Husain A., Hutber G.N. et al.: Studies on the flavodoxins from a cyanobacterium and a red alga.-Biochem. Soc. T. 5: 1505-1506, 1977. Go to original source...
    27. Foster J.S., Singh A.K., Rothschild L.J. et al.: Growth-phase dependent differential gene expression in Synechocystis sp. strain PCC 6803 and regulation by a group 2 sigma factor.-Arch. Microbiol. 187: 265-279, 2007. Go to original source...
    28. Fraser J.M., Tulk S.E., Jeans J.A. et al.: Photophysiological and photosynthetic complex changes during iron starvation in Synechocystis sp. PCC 6803 and Synechococcus elongatus PCC 7942.-PLoS ONE 8: e59861, 2013. Go to original source...
    29. Geiss U., Vinnemeier J., Kunert A. et al.: Detection of the isiA gene across cyanobacterial strains: Potential for probing iron deficiency.-Appl. Environ. Microbiol. 67: 5247-5253, 2001a.
    30. Geiss U., Vinnemeier J., Schoor A. et al.: The iron-regulated isiA gene of Fischerella muscicola strain PCC 73103 is linked to a likewise regulated gene encoding a Pcb-like chlorophyllbinding protein.-FEMS Microbiol. Lett. 197: 123-129, 2001b. Go to original source...
    31. Ghassemian M., Straus N.A.: Fur regulates the expression of iron-stress genes in the cyanobacterium Synechococcus sp. strain PCC 7942.-Microbiology 142: 1469-1476, 1996. Go to original source...
    32. Guikema J.A.: Fluorescence induction characteristics of Anacystis nidulans during recovery from iron-deficiency.-J. Plant Nutr. 8: 891-908, 1985. Go to original source...
    33. Guikema J.A., Sherman L.A.: Chlorophyll-protein organization of membranes from the cyanobacterium Anacystis nidulans.-Arch. Biochem. Biophys. 220: 155-166, 198
    34. Guikema J.A., Sherman L.A.: Organization and function of chlorophyll in membranes of cyanobacteria during iron starvation.-Plant Physiol. 73: 250-256, 1983b. Go to original source...
    35. Guikema J.A., Sherman L.A.: Influence of iron deprivation on the membrane composition of Anacystis nidulans.-Plant Physiol. 74: 90-95, 19
    36. Havaux M., Guedeney G., Hagemann M. et al.: The chlorophyllbinding protein IsiA is inducible by high light and protects the cyanobacterium Synechocystis PCC6803 from photooxidative stress.-FEBS Lett. 579: 2289-2293, 2005. Go to original source...
    37. Holland H.D.: The oxygenation of the atmosphere and oceans.-Philos. T. Roy. Soc. B 361: 903-915, 2006. Go to original source...
    38. Ihalainen J.A., D'Haene S., Yeremenko N. et al.: Aggregates of the chlorophyll-binding protein IsiA (CP43) dissipate energy in cyanobacteria.-Biochemistry 44: 10846-10853, 2005. Go to original source...
    39. Jeanjean R., Zuther E., Yeremenko N. et al: A photosystem I psaFJ-null mutant of the cyanobacterium Synechocystis PCC 6803 expresses the isiAB operon under iron replete conditions.-FEBS Lett. 549: 52-56, 2003. Go to original source...
    40. Jordan P., Fromme P., Witt H.T. et al.: Three-dimensional structure of cyanobacterial photosystem I at 2.5 A resolution.-Nature 411: 909-917, 2001. Go to original source...
    41. Karapetyan N.V.: Non-photochemical quenching of fluorescence in cyanobacteria.-Biochemistry 72: 1127-1135, 2007. Go to original source...
    42. Komenda J., Sobotka R.: Cyanobacterial high-light-inducible proteins-Protectors of chlorophyll-protein synthesis and assembly.-BBA-Bioenergetics 1857: 288-295, 2016.
    43. Kouril R., Arteni A.A., Lax J. et al.: Structure and functional role of supercomplexes of IsiA and Photosystem I in cyanobacterial photosynthesis.-FEBS Lett. 579: 3253-3257, 2005. Go to original source...
    44. Krishnamurthy A., Moore J.K., Mahowald N. et al.: Impacts of atmospheric nutrient inputs on marine biogeochemistry.-J. Geophys. Res. Biogeosci. 115: 1-14, 2010. Go to original source...
    45. Kunert A., Vinnemeier J., Erdmann N. et al.: Repression by Fur is not the main mechanism controlling the iron-inducible isiAB operon in the cyanobacterium Synechocystis sp. PCC 6803.-FEMS Microbiol. Lett. 227: 255-262, 2003. Go to original source...
    46. Kutzki C., Masepohl B., Bohme H.: The isiB gene encoding flavodoxin is not essential for photoautotrophic iron limited growth of the cyanobacterium Synechocystis sp. strain PCC 6803.-FEMS Microbiol. Lett. 160: 231-235, 1998. Go to original source...
    47. La Roche J., van der Staay G. W., Partensky F. et al.: Independent evolution of the prochlorophyte and green plant chlorophyll a/b light-harvesting proteins.-P. Natl. Acad. Sci. USA 93: 15244-15248, 1996. Go to original source...
    48. Laudenbach D., Reith M., Straus N.: Isolation, sequence analysis, and transcriptional studies of the flavodoxin gene from Anacystis nidulans R2.-J. Bacteriol. 170: 258-265, 1988. Go to original source...
    49. Laudenbach D.E., Straus N.A.: Characterization of a cyanobacterial iron stress-induced gene similar to psbC.-J. Bacteriol. 170: 5018-5026, 1988. Go to original source...
    50. Leonhardt K., Straus N.A.: An iron stress operon involved in photosynthetic electron transport in the marine cyanobacterium Synechococcus sp. PCC 7002.-J. Gen. Microbiol. 8: 1613-1621, 1992. Go to original source...
    51. Leonhardt K., Straus N.A.: Photosystem II genes isiA, psbDI and psbC in Anabaena sp. PCC 7120: cloning, sequencing and the transcriptional regulation in iron-stressed and iron-repleted cells.-Plant Mol. Biol. 24: 63-73, 1994. Go to original source...
    52. Li H., Singh A.K., McIntyre L.M. et al.: Differential gene expression in response to hydrogen peroxide and the putative PerR regulon of Synechocystis sp. strain PCC 6803.-J. Bacteriol. 186: 3331-3345, 2004. Go to original source...
    53. Ma F., Zhang X., Zhu X. et al.: Dynamic changes of IsiAcontaining complexes during long-term iron deficiency in Synechocystis sp. PCC 6803.-Mol. Plant 10: 143-154, 2017. Go to original source...
    54. Martin J.H., Fitzwater S.E.: Iron-deficiency limits phytoplankton growth in the Northeast Pacific subarctic.-Nature 331: 341-343, 1988. Go to original source...
    55. Melkozernov A.N., Bibby T.S., Lin S. et al.: Time-resolved absorption and emission show that the CP43' antenna ring of iron-stressed Synechocystis sp. PCC6803 is efficiently coupled to the photosystem I reaction center core.-Biochemistry 42: 3893-3903, 2003. Go to original source...
    56. Michel K.P., Pistorius E.K.: Adaptation of the photosynthetic electron transport chain in cyanobacteria to iron deficiency: The function of IdiA and IsiA.-Physiol. Plantarum 120: 36-50, 2004. Go to original source...
    57. Michel K.P., Thole H.H., Pistorius E.K.: IdiA, a 34 kDa protein in the cyanobacteria Synechococcus sp. strains PCC 6301 and PCC 7942, is required for growth under iron and manganese limitations.-Microbiology 142: 2635-2645, 1996. Go to original source...
    58. Moore C.M., Mills M.M., Arrigo K.R. et al.: Processes and patterns of oceanic nutrient limitation.-Nat. Geosci. 6: 701-710, 2013. Go to original source...
    59. Niedzwiedzki D.M., Tronina T., Liu H. et al.: Carotenoidinduced non-photochemical quenching in the cyanobacterial chlorophyll synthase-HliC/D complex.-BBA-Bioenergetics 1857: 1430-1439, 2016.
    60. Nield J., Morris E.P., Bibby T.S. et al.: Structural analysis of the photosystem I supercomplex of cyanobacteria induced by iron deficiency.-Biochemistry 42: 3180-3188, 2003. Go to original source...
    61. North R., Guildford S., Smith R. et al.: Evidence for phosphorus, nitrogen, and iron colimitation of phytoplankton communities in Lake Erie.-Limnol. Oceanogr. 52: 315-328, 2007. Go to original source...
    62. Öquist G.: Changes in pigment composition and photosynthesis induced by iron-deficiency in blue-green-alga Anacystis nidulans.-Physiol. Plantarum 25: 188-191, 19
    63. Orf G.S., Saer R.G., Niedzwiedzki D.M. et al.: Evidence for a cysteine-mediated mechanism of excitation energy regulation in a photosynthetic antenna complex.-P. Natl. Acad. Sci. USA 113: E4486-E4493, 2016. Go to original source...
    64. Pakrasi H.B., Goldenberg A., Sherman L.A.: Membrane development in the cyanobacterium, Anacystis nidulans, during recovery from iron starvation.-Plant Physiol. 79: 290-295, 1985a. Go to original source...
    65. Pakrasi H.B., Riethman H.C., Sherman L.A.: Organization of pigment proteins in the photosystem II complex of the cyanobacterium Anacystis nidulans R2.-P. Natl. Acad. Sci. USA 82: 6903-6907, 1985b. Go to original source...
    66. Park Y.I., Sandström S., Gustafsson P. et al.: Expression of the isiA gene is essential for the survival of the cyanobacterium Synechococcus sp. PCC 7942 by protecting photosystem II from excess light under iron limitation.-Mol. Microbiol. 32: 123-129, 1999. Go to original source...
    67. Reppert M., Zazubovich V., Dang N.C. et al.: Low-energy chlorophyll states in the CP43 antenna protein complex: simulation of various optical spectra. II.-J. Phys. Chem. B 112: 9934-9947, 2008. Go to original source...
    68. Richier S., Macey A.I., Pratt N.J. et al.: Abundances of ironbinding photosynthetic and nitrogen-fixing proteins of Trichodesmium both in culture and in situ from the North Atlantic.-PLoS ONE 7: e35571, 2012. Go to original source...
    69. Riethman H.C., Sherman L.A.: Purification and characterization of an iron stress-induced chlorophyll-protein from the cyanobacterium Anacystis nidulans R2.-BBA-Bioenergetics 935: 141-151, 1988. Go to original source...
    70. Riley K.J., Zazubovich V., Jankowiak R.: Frequency-domain spectroscopic study of the PS I-CP43' supercomplex from the cyanobacterium Synechocystis PCC 6803 grown under iron stress conditions.-J. Phys. Chem. B 110: 22436-22446, 2006.
    71. Ruban A.V., Berera R., Ilioaia C. et al.: Identification of a mechanism of photoprotective energy dissipation in higher plants.-Nature 450: 575-578, 2007. Go to original source...
    72. Ryan-Keogh T.J., Macey A.I., Cockshutt A.M. et al.: The cyanobacterial chlorophyll-binding-protein IsiA acts to increase the in vivo rffective absorption cross-section of PSI under iron limitation.-J. Phycol. 48: 145-154, 2012. Go to original source...
    73. Saitou N., Nei M.: The neighbor-joining method-a new method for reconstructing phylogenetic trees.-Mol. Biol. Evol. 4: 406-425, 1987.
    74. Salomon E., Keren N.: Acclimation to environmentally relevant Mn concentrations rescues a cyanobacterium from the detrimental effects of iron limitation.-Environ. Microbiol. 17: 2090-2098, 2015. Go to original source...
    75. Sandrini G., Tann R.P., Schuurmans J.M. et al.: Diel variation in gene expression of the CO2-concentrating mechanism during a harmful cyanobacterial bloom.-Front. Microbiol. 7: 551, 2016. Go to original source...
    76. Sandström S., Park Y.I., Öquist G. et al.: CP43', the isiA gene product, functions as an excitation energy dissipator in the 333 cyanobacterium Synechococcus sp PCC 7942.-Photochem. Photobiol. 74: 431-437, 2001. Go to original source...
    77. Sarcina M., Mullineaux C.W.: Mobility of the IsiA chlorophyllbinding protein in cyanobacterial thylakoid membranes.-J. Biol. Chem. 279: 36514-36518, 2004. Go to original source...
    78. Schrader P.S., Milligan A.J., Behrenfeld M.J.: Surplus photosynthetic antennae complexes underlie diagnostics of iron limitation in a cyanobacterium.-PLoS ONE 6: e18753, 2011. Go to original source...
    79. Sherman D.M., Sherman L.A.: Effect of iron-deficiency and iron restoration on ultrastructure of Anacystis nidulans.-J. Bacteriol. 156: 393-401, 1983.
    80. Shih P.M., Wu D., Latifi A. et al.: Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing.-P. Natl. Acad. Sci. USA 110: 1053-1058, 2013. Go to original source...
    81. Singh A.K., Sherman L.A.: Iron-independent dynamics of IsiA production during the transition to stationary phase in the cyanobacterium Synechocystis sp. PCC 6803.-FEMS Microbiol. Lett. 256: 159-164, 2006. Go to original source...
    82. Stojiljkovic I., Hantke K.: Functional domains of the Escherichia coli ferric uptake regulator protein (Fur).-Mol. Gen. Genet 247: 199-205, 1995. Go to original source...
    83. Sun J., Golbeck J.H.: The presence of the IsiA-PSI supercomplex leads to enhanced photosystem I electron throughput in ironstarved cells of Synechococcus sp. PCC 7002.-J. Phys. Chem. B 119: 13549-13559, 2015.
    84. Tsuda A., Takeda S., Saito H. et al: A mesoscale iron enrichment in the western subarctic Pacific induces a large centric diatom bloom.-Science 300: 958-961, 2003. Go to original source...
    85. Turner S., Huang T.-C., Chaw S.-M.: Molecular phylogeny of nitrogen-fixing unicellular cyanobacteria.-Bot. Bull. Acad. Sinica 42: 2001.
    86. Umena Y., Kawakami K., Shen J.R. et al.: Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 A.-Nature 473: 55-60, 2011. Go to original source...
    87. van der Weij-de Wit C. D., Ihalainen J. A., van de Vijver E. et al.: Fluorescence quenching of IsiA in early stage of iron deficiency and at cryogenic temperatures.-Biochim. Biophys. Acta 1767: 1393-1400, 2007. Go to original source...
    88. Vinnemeier J., Kunert A., Hagemann M.: Transcriptional analysis of the isiAB operon in salt-stressed cells of the cyanobacterium Synechocystis sp. PCC 6803.-FEMS Microbiol. Lett. 169: 323-330, 1998. Go to original source...
    89. Vrede T., Tranvik L.J.: Iron constraints on planktonic primary production in oligotrophic lakes.-Ecosystems 9: 1094-1105, 2006. Go to original source...
    90. Wang Q., Hall C.L., Al-Adami M.Z. et al.: IsiA is required for the formation of photosystem I supercomplexes and for efficient state transition in Synechocystis PCC 6803.-PLoS ONE 5: e10432, 2010. Go to original source...
    91. Wang Q., Jantaro S., Lu B.S. et al.: The high light-inducible polypeptides stabilize trimeric photosystem I complex under high light conditions in Synechocystis PCC 6803.-Plant Physiol. 147: 1239-1250, 2008. Go to original source...
    92. Wilson A., Ajlani G., Verbavatz J.M. et al: A soluble carotenoid protein involved in phycobilisome-related energy dissipation in cyanobacteria.-Plant Cell 18: 992-1007, 2006. Go to original source...
    93. Yeremenko N., Kouril R., Ihalainen J. A. et al.: Supramolecular organization and dual function of the IsiA chlorophyll-binding protein in cyanobacteria.-Biochemistry 43: 10308-10313, 2004. Go to original source...
    94. Yousef N., Pistorius E.K., Michel K.P.: Comparative analysis of idiA and isiA transcription under iron starvation and oxidative stress in Synechococcus elongatus PCC 7942 wild-type and selected mutants.-Arch. Microbiol. 180: 471-483, 2003. Go to original source...
    95. Zehr J.P., Bench S.R., Carter B.J. et al.: Globally distributed uncultivated oceanic N2-Fixing cyanobacteria lack oxygenic Photosystem II.-Science 322: 1110-1112, 2008. Go to original source...

    Return to the content