1887

Abstract

modifies the pigment composition of its major light-harvesting complexes, i.e. phycobilisomes, and cell and filament morphology according to ambient light quality in a process termed complementary chromatic adaptation (CCA). The cells are red in colour and rectangular shaped, and filaments are longer under green light (GL), in contrast with blue-green, spherical cells and shorter filaments under red light (RL). In this study, we report that wild-type (WT) UTEX 481 and WT-pigmented, shortened filament strain SF33 of accumulate reactive oxygen species (ROS) under both GL and RL, with the level of oxidative stress being higher under RL as compared with GL. During CCA, higher levels of ROS under RL are correlated with the RL-specific spherical cell shape and filament fragmentation – cells exhibiting elevated levels of ROS under RL have reduced cell length, yet the width of cells is not affected. Addition of ascorbic acid to RL-grown cultures resulted in lower ROS levels and a concomitant shift to GL-associated cellular morphology, i.e. an increased cell length. This observation identifies an RL-dependent oxidative-stress-mediated regulation of morphogenesis in a bacterial system. Spherical cell morphology may result from ROS-dependent changes in the cell membrane integrity or cell wall loosening and associated cell expansion.

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2012-09-01
2020-07-15
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References

  1. Bennett A., Bogorad L.. ( 1973;). Complementary chromatic adaptation in a filamentous blue-green alga. J Cell Biol58:419–435 [CrossRef][PubMed]
    [Google Scholar]
  2. Bogorad L.. ( 1975;). Phycobiliproteins and complementary chromatic adaptation. Annu Rev Plant Physiol26:369–401 [CrossRef]
    [Google Scholar]
  3. Bordowitz J. R., Montgomery B. L.. ( 2008;). Photoregulation of cellular morphology during complementary chromatic adaptation requires sensor-kinase-class protein RcaE in Fremyella diplosiphon . J Bacteriol190:4069–4074 [CrossRef][PubMed]
    [Google Scholar]
  4. Bordowitz J. R., Montgomery B. L.. ( 2010;). Exploiting the autofluorescent properties of photosynthetic pigments for analysis of pigmentation and morphology in live Fremyella diplosiphon cells. Sensors (Basel)10:6969–6979 [CrossRef][PubMed]
    [Google Scholar]
  5. Bordowitz J. R., Whitaker M. J., Montgomery B. L.. ( 2010;). Independence and interdependence of the photoregulation of pigmentation and development in Fremyella diplosiphon . Commun Integr Biol3:151–153 [CrossRef][PubMed]
    [Google Scholar]
  6. Campbell D.. ( 1996;). Complementary chromatic adaptation alters photosynthetic strategies in the cyanobacterium Calothrix . Microbiology142:1255–1263 [CrossRef]
    [Google Scholar]
  7. Campbell D., Houmard J., De Marsac N. T.. ( 1993;). Electron transport regulates cellular differentiation in the filamentous cyanobacterium Calothrix . Plant Cell5:451–463[PubMed][CrossRef]
    [Google Scholar]
  8. Carol R. J., Dolan L.. ( 2006;). The role of reactive oxygen species in cell growth: lessons from root hairs. J Exp Bot57:1829–1834 [CrossRef][PubMed]
    [Google Scholar]
  9. Cobley J. G., Zerweck E., Reyes R., Mody A., Seludo-Unson J. R., Jaeger H., Weerasuriya S., Navankasattusas S.. ( 1993;). Construction of shuttle plasmids which can be efficiently mobilized from Escherichia coli into the chromatically adapting cyanobacterium, Fremyella diplosiphon . Plasmid30:90–105 [CrossRef][PubMed]
    [Google Scholar]
  10. Fischer W. W.. ( 2008;). Biogeochemistry: Life before the rise of oxygen. Nature455:1051–1052 [CrossRef][PubMed]
    [Google Scholar]
  11. Foreman J., Demidchik V., Bothwell J. H. F., Mylona P., Miedema H., Torres M. A., Linstead P., Costa S., Brownlee C.. & other authors ( 2003;). Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature422:442–446 [CrossRef][PubMed]
    [Google Scholar]
  12. Gutu A., Kehoe D. M.. ( 2012;). Emerging perspectives on the mechanisms, regulation, and distribution of light color acclimation in cyanobacteria. Mol Plant5:1–13 [CrossRef][PubMed]
    [Google Scholar]
  13. Häder D.-P., Helbling E. W., Williamson C. E., Worrest R. C.. ( 2011;). Effects of UV radiation on aquatic ecosystems and interactions with climate change. Photochem Photobiol Sci10:242–260 [CrossRef][PubMed]
    [Google Scholar]
  14. He Y.-Y., Häder D.-P.. ( 2002a;). UV-B-induced formation of reactive oxygen species and oxidative damage of the cyanobacterium Anabaena sp.: protective effects of ascorbic acid and N-acetyl-l-cysteine. J Photochem Photobiol B66:115–124 [CrossRef][PubMed]
    [Google Scholar]
  15. He Y. Y., Häder D. P.. ( 2002b;). Involvement of reactive oxygen species in the UV-B damage to the cyanobacterium Anabaena sp.. J Photochem Photobiol B66:73–80 [CrossRef][PubMed]
    [Google Scholar]
  16. Johnson E. A., Larson A. E.. ( 2005;). Lysozyme. Antimicrobials in Food, 3rd edn.361–387 Davidson P. M., Sofos J. N., Branen A. L.. Boca Raton, FL: CRC Press; [CrossRef]
    [Google Scholar]
  17. Kehoe D. M.. ( 2010;). Chromatic adaptation and the evolution of light color sensing in cyanobacteria. Proc Natl Acad Sci U S A107:9029–9030 [CrossRef][PubMed]
    [Google Scholar]
  18. Kehoe D. M., Grossman A. R.. ( 1996;). Similarity of a chromatic adaptation sensor to phytochrome and ethylene receptors. Science273:1409–1412 [CrossRef][PubMed]
    [Google Scholar]
  19. Kehoe D. M., Grossman A. R.. ( 1997;). New classes of mutants in complementary chromatic adaptation provide evidence for a novel four-step phosphorelay system. J Bacteriol179:3914–3921[PubMed]
    [Google Scholar]
  20. Kehoe D. M., Gutu A.. ( 2006;). Responding to color: the regulation of complementary chromatic adaptation. Annu Rev Plant Biol57:127–150 [CrossRef][PubMed]
    [Google Scholar]
  21. Li H. B., Qin Y. M., Pang Y., Song W. Q., Mei W. Q., Zhu Y. X.. ( 2007;). A cotton ascorbate peroxidase is involved in hydrogen peroxide homeostasis during fibre cell development. New Phytol175:462–471 [CrossRef][PubMed]
    [Google Scholar]
  22. Li L., Alvey R. M., Bezy R. P., Kehoe D. M.. ( 2008;). Inverse transcriptional activities during complementary chromatic adaptation are controlled by the response regulator RcaC binding to red and green light-responsive promoters. Mol Microbiol68:286–297 [CrossRef][PubMed]
    [Google Scholar]
  23. Los D. A., Zorina A., Sinetova M., Kryazhov S., Mironov K., Zinchenko V. V.. ( 2010;). Stress sensors and signal transducers in cyanobacteria. Sensors (Basel)10:2386–2415 [CrossRef][PubMed]
    [Google Scholar]
  24. Ma Z., Gao K.. ( 2009;). Photoregulation of morphological structure and its physiological relevance in the cyanobacterium Arthrospira (Spirulina) platensis . Planta230:329–337 [CrossRef][PubMed]
    [Google Scholar]
  25. Müller K., Linkies A., Vreeburg R. A., Fry S. C., Krieger-Liszkay A., Leubner-Metzger G.. ( 2009;). In vivo cell wall loosening by hydroxyl radicals during cress seed germination and elongation growth. Plant Physiol150:1855–1865 [CrossRef][PubMed]
    [Google Scholar]
  26. Pattanaik B., Montgomery B. L.. ( 2010;). FdTonB is involved in the photoregulation of cellular morphology during complementary chromatic adaptation in Fremyella diplosiphon . Microbiology156:731–741 [CrossRef][PubMed]
    [Google Scholar]
  27. Pattanaik B., Whitaker M. J., Montgomery B. L.. ( 2011a;). Convergence and divergence of the photoregulation of pigmentation and cellular morphology in Fremyella diplosiphon . Plant Signal Behav6:2038–2041 [CrossRef][PubMed]
    [Google Scholar]
  28. Pattanaik B., Whitaker M. J., Montgomery B. L.. ( 2011b;). Regulation of phycoerythrin synthesis and cellular morphology in Fremyella diplosiphon green mutants. Biochem Biophys Res Commun413:182–188 [CrossRef][PubMed]
    [Google Scholar]
  29. Pattanaik B., Whitaker M. J., Montgomery B. L.. ( 2012;). Light quantity affects the regulation of cell shape in Fremyella diplosiphon . Front Microbiol3:170[PubMed][CrossRef]
    [Google Scholar]
  30. Postius C., Neuschaefer-Rube O., Haid V., Böger P.. ( 2001;). N2-fixation and complementary chromatic adaptation in non-heterocystous cyanobacteria from Lake Constance. FEMS Microbiol Ecol37:117–125 [CrossRef]
    [Google Scholar]
  31. Potocký M., Jones M. A., Bezvoda R., Smirnoff N., Zárský V.. ( 2007;). Reactive oxygen species produced by NADPH oxidase are involved in pollen tube growth. New Phytol174:742–751 [CrossRef][PubMed]
    [Google Scholar]
  32. Rastogi R. P., Singh S. P., Häder D.-P., Sinha R. P.. ( 2010;). Detection of reactive oxygen species (ROS) by the oxidant-sensing probe 2′,7′-dichlorodihydrofluorescein diacetate in the cyanobacterium Anabaena variabilis PCC 7937. Biochem Biophys Res Commun397:603–607 [CrossRef][PubMed]
    [Google Scholar]
  33. Semighini C. P., Harris S. D.. ( 2008;). Regulation of apical dominance in Aspergillus nidulans hyphae by reactive oxygen species. Genetics179:1919–1932 [CrossRef][PubMed]
    [Google Scholar]
  34. Singh S. P., Montgomery B. L.. ( 2011;). Determining cell shape: adaptive regulation of cyanobacterial cellular differentiation and morphology. Trends Microbiol19:278–285 [CrossRef][PubMed]
    [Google Scholar]
  35. Singh S. P., Häder D.-P., Sinha R. P.. ( 2010;). Cyanobacteria and ultraviolet radiation (UVR) stress: mitigation strategies. Ageing Res Rev9:79–90 [CrossRef][PubMed]
    [Google Scholar]
  36. Speranza A., Crinelli R., Scoccianti V., Geitmann A.. ( 2012;). Reactive oxygen species are involved in pollen tube initiation in kiwifruit. Plant Biol (Stuttg)14:64–76[PubMed]
    [Google Scholar]
  37. Stanier R. Y., Cohen-Bazire G.. ( 1977;). Phototrophic prokaryotes: the cyanobacteria. Annu Rev Microbiol31:225–274 [CrossRef][PubMed]
    [Google Scholar]
  38. Terauchi K., Montgomery B. L., Grossman A. R., Lagarias J. C., Kehoe D. M.. ( 2004;). RcaE is a complementary chromatic adaptation photoreceptor required for green and red light responsiveness. Mol Microbiol51:567–577 [CrossRef][PubMed]
    [Google Scholar]
  39. Young K. D.. ( 2006;). The selective value of bacterial shape. Microbiol Mol Biol Rev70:660–703 [CrossRef][PubMed]
    [Google Scholar]
  40. Young K. D.. ( 2010;). Bacterial shape: two-dimensional questions and possibilities. Annu Rev Microbiol64:223–240 [CrossRef][PubMed]
    [Google Scholar]
  41. Zehr J. P.. ( 2011;). Nitrogen fixation by marine cyanobacteria. Trends Microbiol19:162–173 [CrossRef][PubMed]
    [Google Scholar]
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