Photosynthesis Research

, Volume 76, Issue 1–3, pp 145–155 | Cite as

Light-induced behavioral responses (`phototaxis') in prokaryotes


Light-induced sensory responses are among the oldest scientific observations on bacterial behavior. Various types of response have been characterized physiologically in detail. However, the molecular basis of this type of response is only slowly emerging. In many of these systems photosynthetic pigments absorb the light. This then generates a signal via electron transport, feeding into a canonical chemotaxis signal transduction pathway. Nevertheless, several examples have been identified in which dedicated photoreceptor proteins do play a role. The intrinsic complexity of some of these signal transduction systems is overwhelming, in part because of the significant apparent redundancy. The genomics information that is now available for several model organisms (in particular Rhodobacter sphaeroides and Synechocystis sp. PCC6803) facilitates obtaining an increasingly detailed view of the molecular basis of the partial reactions that jointly form the basis of this type of elementary behavioral response.

J. Armitage bacteriophytochrome C.E. Bauer R. Clayton chemotaxis cyanobacteria C. Ehrenberg T. Engelmann H. Gest A. Grossman K. Hellingwerf photoactive yellow protein photoreceptor phototaxis purple bacteria sensory rhodopsin J. Spudich 


  1. Akbar S, Gaidenko TA, Kang CM, O'Reilly M, Devine KM and Price CW (2001) New family of regulators in the environmental signaling pathway which activates the general stress transcription factor sigma(B) of Bacillus subtilis. J Bacteriol 183: 1329–1338PubMedCrossRefGoogle Scholar
  2. Armitage JP (1997) Behavioural responses of bacteria to light and oxygen. Arch Microbiol 168: 249–261PubMedCrossRefGoogle Scholar
  3. Armitage JP (1999) Bacterial tactic responses. Adv Microb Physiol 41: 229–289PubMedCrossRefGoogle Scholar
  4. Armitage JP and Evans MCW (1981) The reaction centre in the phototactic and chemotactic responses of Rhodopseudomonas sphaeroides. FEMS Microbiol Lett 11: 89–92CrossRefGoogle Scholar
  5. Beja O, Aravind L, Koonin EV, Suzuki MT, Hadd A, Nguyen LP, Jovanovich SB, Gates CM, Feldman RA, Spudich JL, Spudich EN and DeLong EF (2000) Bacterial rhodopsin: evidence for a new type of phototrophy in the sea. Science 289: 1902–1906PubMedCrossRefGoogle Scholar
  6. Beja O, Spudich EN, Spudich JL, Leclerc M and DeLong EF (2001) Proteorhodopsin phototrophy in the ocean. Nature (London) 411: 786–789PubMedCrossRefGoogle Scholar
  7. Berry RM and Armitage JP (2000) Response kinetics of tethered Rhodobacter sphaeroides to changes in light intensity. Biophys J 78: 1207–1215PubMedCrossRefGoogle Scholar
  8. Bhaya D, Takahashi A and Grossman AR (2001a) Light regulation of type IV pilus-dependent motility by chemosensory-like elements in Synechocystis PCC6803 Proc Natl Acad Sci USA 98: 7540–7545Google Scholar
  9. Bhaya D, Takahashi A, Shahi P and Grossman AR (2001b) Novel motility mutants of Synechocystis strain PCC 6803 generated by in vitro transposon mutagenesis. J Bacteriol 183: 6140–6143PubMedCrossRefGoogle Scholar
  10. Bibikov SI, Biran R, Rudd KE and Parkinson JS (1997) A signal transducer for aerotaxis in Escherichia coli. J Bacteriol 179: 4075–4079PubMedGoogle Scholar
  11. Bibikov SI, Barnes LA, Gitin Y and Parkinson JS (2000) Domain organization and flavin adenine dinucleotide-binding determinants in the aerotaxis signal transducer Aer of Escherichia coli. Proc Natl Acad Sci USA 97: 5830–5835PubMedCrossRefGoogle Scholar
  12. Bogomolni RA, Stoeckenius W, Szundi I, Perozo E, Olson KD and Spudich JL (1994) Removal of transducer Htr I allows electrogenic proton translocation by sensory rhodopsin I. Proc Natl Acad Sci USA 91: 10188–10192PubMedCrossRefGoogle Scholar
  13. Choi JS, Chung YH, Moon YJ, Kim C, Watanabe M, Song PS, Joe CO, Bogorad L and Park YM (1999) Photomovement of the gliding cyanobacterium Synechocystis sp. PCC6803. Photochem Photobiol 70: 95–102PubMedCrossRefGoogle Scholar
  14. Chung YH, Cho MS, Moon YJ, Choi JS, Yoo YC, Park YI, Lee KM, Kang KW and Park YM (2001) ctr1, a gene involved in a signal transduction pathway of the gliding motility in the cyanobacterium Synechocystis sp. PCC6803. FEBS Lett 492: 33–38PubMedCrossRefGoogle Scholar
  15. Clayton RK (1953a) Studies in the phototaxis of Rhodospirillum rubrum. I. Action spectrum, growth in green light andWeber-law adherence. Arch Microbiol 19: 107–124Google Scholar
  16. Clayton RK (1953b) Studies in the phototaxis of Rhodospirillum rubrum.II. The relation between phototaxis and photosynthesis. Arch Microbiol 19: 125–140Google Scholar
  17. Clayton RK (1953c) Studies in the phototaxis of Rhodospirillum rubrum. III. Quantitative relationship between stimulus and response Arch Microbiol 19: 141–165Google Scholar
  18. Clayton RK (1958) On the interplay of environmental factors affecting taxis and mobility in Rhodospirillum rubrum. Arch Microbiol 29: 189–212Google Scholar
  19. Clayton RK (1977) Light and Living Matter. Vol 2: The Biological Part, p 71. Robert E. Krieger Publishing Company, Huntington, New YorkGoogle Scholar
  20. Clayton RK (2002) Research on photosynthetic reaction centers from 1932 to 1987. Photosynth Res 73: 63–71PubMedCrossRefGoogle Scholar
  21. Delprato AM, Samadani A, Kudrolli A and Tsimring LS (2001) Swarming ring patterns in bacterial colonies exposed to ultraviolet radiation. Phys Rev Lett 87: 158102–1–158102–4CrossRefGoogle Scholar
  22. Ehrenberg GS (1883) Die Infusionstrierchen als vollkommene Organismen (Ed Engelmann TW), p 15. LeipzigGoogle Scholar
  23. Engelmann TW (1883) Bakterium photometricum. Ein Beitrag zur vergleichenden Physiologie des Licht-und Farbensinnes. Pfluegers Arch Gesamte Physiol Menschen Tiere 42: 183–186CrossRefGoogle Scholar
  24. Falke JJ, Bass RB, Butler SL, Chervitz SA and Danielson MA (1997) The two-component signaling pathway of bacterial chemotaxis: a molecular view of signal transduction by receptors, kinases, and adaptation enzymes. Annu Rev Cell Dev Biol 13: 457–512PubMedCrossRefGoogle Scholar
  25. Ferrando ME, Krah M, Marwan W and Oesterhelt D (1993) The methyl-accepting transducer protein Htr I is functionally associated with the photoreceptor sensory rhodopsin I in the archaeon Halobacterium salinarium. EMBO J 12: 2999–3005Google Scholar
  26. Frostl JM and Overmann J (2000) Phylogenetic affiliation of the bacteria that constitute phototrophic consortia. Arch Microbiol 174: 50–58PubMedCrossRefGoogle Scholar
  27. Gauden DE and Armitage JP (1995) Electron transport-dependent taxis in Rhodobacter sphaeroides. J Bacteriol 177: 5853–5859PubMedGoogle Scholar
  28. Glagolev AN (1984) Bacterial H+-sensing. Trends Biochem Sci 9: 397–400CrossRefGoogle Scholar
  29. Grishanin RN, Gauden DE and Armitage JP (1997) Photoresponses in Rhodobacter sphaeroides: role of photosynthetic electron transport. J Bacteriol 179: 24–30PubMedGoogle Scholar
  30. Hader DP (1987) Photosensory behavior in procaryotes. Microbiol Rev 51: 1–21PubMedGoogle Scholar
  31. Harayama S (1977) Phototaxis and membrane potential in the photosynthetic bacterium Rhodospirillum rubrum. J Bacteriol 131: 34–41PubMedGoogle Scholar
  32. Harayama S and Iino T (1976) Phototactic responses of aerobically cultivated Rhodospirillum rubrum. J Gen Microbiol 94: 173–179PubMedGoogle Scholar
  33. Hellingwerf KJ (2000) Key issues in the photochemistry and signalling-state formation of photosensor proteins. J Photochem Photobiol B 54: 94–102PubMedCrossRefGoogle Scholar
  34. Hellingwerf KJ, Hendriks J and Gensch T (2002) On the configurational and conformational changes in photoactive yellow protein that lead to signal generation in Ectothiorhodospira halophila. J Biol Phys 28:395–412CrossRefGoogle Scholar
  35. Hitomi K, Okamoto K, Daiyasu H, Miyashita H, Iwai S, Toh H, Ishiura M and Todo T (2000) Bacterial cryptochrome and photolyase: characterization of two photolyase-like genes of Synechocystis sp. PCC6803. Nucleic Acids Res 28: 2353–2362PubMedCrossRefGoogle Scholar
  36. Hoff WD, Jung KH and Spudich JL (1997) Molecular mechanism of photosignaling by archaeal sensory rhodopsins. Annu Rev Biophys Biomol Struct 26: 223–258PubMedCrossRefGoogle Scholar
  37. Hughes J, Lamparter T, Mittmann F, Hartmann E, Gartner W, Wilde A and Borner TA (1997) A prokaryotic phytochrome. Nature (London) 386: 663PubMedCrossRefGoogle Scholar
  38. Jiang ZY and Bauer CE (1997) Analysis of a chemotaxis operon from Rhodospirillum centenum. J Bacteriol 179: 5712–5719PubMedGoogle Scholar
  39. Jiang ZY and Bauer CE (2001) Component of the Rhodospirillum centenum photosensory apparatus with structural and functional similarity to methyl-accepting chemotaxis protein chemoreceptors. J Bacteriol 183: 171–177PubMedCrossRefGoogle Scholar
  40. Jiang ZY, Gest H and Bauer CE (1997) Chemosensory and photosensory perception in purple photosynthetic bacteria utilize common signal transduction components. J Bacteriol 179: 5720–5727PubMedGoogle Scholar
  41. Jiang ZY, Rushing BG, Bai Y, Gest H and Bauer CE (1998) Isolation of Rhodospirillum centenum mutants defective in phototactic colony motility by transposon mutagenesis. J Bacteriol 180: 1248–1255PubMedGoogle Scholar
  42. Kondou Y, Nakazawa M, Higashi S, Watanabe M and Manabe K (2001) Equal-quantum action spectra indicate fluence-rateselective action of multiple photoreceptors for photomovement of the thermophilic cyanobacterium Synechococcus elongatus. Photochem Photobiol 73: 90–95PubMedCrossRefGoogle Scholar
  43. Kort R, Crielaard W, Spudich JL and Hellingwerf KJ (2000) Colorsensitive motility and methanol release responses in Rhodobacter sphaeroides. J Bacteriol 182: 3017–3021PubMedCrossRefGoogle Scholar
  44. Kort R, Hoff WD, Van West M, Kroon AR, Hoffer SM, Vlieg KH, Crielaard W, Van Beeumen JJ and Hellingwerf KJ (1996) The xanthopsins: a new family of eubacterial blue-light photoreceptors. EMBO J 15: 3209–3218PubMedGoogle Scholar
  45. Lengeler JW and Jahreis K (1996) Phosphotransferase systems or PTSs as carbohydrate transport and as signal transduction systems. In: Konings WN, Kaback HR and Lolkema JS (eds) Handbook of Biological Physics, pp 573–598. Elsevier Science, AmsterdamGoogle Scholar
  46. Lux R, Munasinghe VR, Castellano F, Lengeler JW, Corrie JE and Khan S (1999) Elucidation of a PTS-carbohydrate chemotactic signal pathway in Escherichia coli using a time-resolved behavioral assay. Mol Biol Cell 10: 1133–1146PubMedGoogle Scholar
  47. Mattick JS, Whitchurch CB and Alm RA (1996) The molecular genetics of type-4 fimbriae in Pseudomonas aeruginosa -a review. Gene 179: 147–155PubMedCrossRefGoogle Scholar
  48. McBride MJ (2001) Bacterial gliding motility: multiple mechanisms for cell movement over surfaces. Annu Rev Microbiol 55: 49–75PubMedCrossRefGoogle Scholar
  49. Montrone M, Oesterhelt D and Marwan W(1996) Phosphorylationindependent bacterial chemoresponses correlate with changes in the cytoplasmic level of fumarate. J Bacteriol 178: 6882–6887PubMedGoogle Scholar
  50. Morton-Firth CJ, Shimizu TS and Bray D (1999) A free-energybased stochastic simulation of the Tar receptor complex. J Mol Biol 286: 1059–1074PubMedCrossRefGoogle Scholar
  51. Nultsch W (1961) Der Einfluss des Lichtes auf die Bewegung der Cyanophyceen. 1. Phototopotaxis von Phormidium autumnale. Planta 56: 632–647CrossRefGoogle Scholar
  52. Oh JI and Kaplan S (2001) Generalized approach to the regulation and integration of gene expression. Mol Microbiol 39: 1116–1123PubMedCrossRefGoogle Scholar
  53. Oh JI, Eraso JM and Kaplan S (2000) Interacting regulatory circuits involved in orderly control of photosynthesis gene expression in Rhodobacter sphaeroides 2.4.1. J Bacteriol 182: 3081–3087PubMedCrossRefGoogle Scholar
  54. Pfennig N (1968) Chromatium akenii (Thiorhodaceae), pp 3–9. Institut für den Wissenschaftlichen Film, Göttingen, GermanyGoogle Scholar
  55. Prasad K, Caplan SR and Eisenbach M (1998) Fumarate modulates bacterial flagellar rotation by lowering the free energy difference between the clockwise and counterclockwise states of the motor. J Mol Biol 280: 821–828PubMedCrossRefGoogle Scholar
  56. Ragatz L, Jiang Z-Y, Bauer CE and Gest H (1994) Phototactic purple bacteria. Nature (London) 370: 104CrossRefGoogle Scholar
  57. Ragatz L, Jiang Z-Y, Bauer CE and Gest H (1995) Macroscopic phototactic behavior of the purple photosynthetic bacterium Rhodospirillum centenum. Arch Microbiol 163: 1–6PubMedGoogle Scholar
  58. Ramsing NB, Ferris MJ and Ward DM (2000) Highly ordered vertical structure of Synechococcus populations within the onemillimeter-thick photic zone of a hot spring cyanobacterial mat. Appl Environ Microbiol 66: 1038–1049PubMedCrossRefGoogle Scholar
  59. Rebbapragada A, Johnson MS, Harding GP, Zuccarelli AJ, Fletcher HM, Zhulin IB and Taylor BL (1997) The Aer protein and the serine chemoreceptor Tsr independently sense intracellular energy levels and transduce oxygen, redox, and energy signals for Escherichia coli behavior. Proc Natl Acad Sci USA 94: 10541–10546PubMedCrossRefGoogle Scholar
  60. Romagnoli S and Armitage JP (1999) Role of the chemosensory pathways in transient changes in swimming speed of Rhodobacter sphaeroides induced by changes in photosynthetic electron transport. J Bacteriol 181: 34–39PubMedGoogle Scholar
  61. Sackett MJ, Armitage JP, Sherwood EE and Pitta TP (1997) Photoresponses of the purple nonsulfur bacteria Rhodospirillum centenum and Rhodobacter sphaeroides. J Bacteriol 179: 6764–6768PubMedGoogle Scholar
  62. Sprenger WW, Hoff WD, Armitage JP and Hellingwerf KJ (1993) The eubacterium Ectothiorhodospira halophila is negatively phototactic, with a wavelength dependence that fits the absorption spectrum of the photoactive yellow protein. J Bacteriol 175: 3096–3104PubMedGoogle Scholar
  63. Spudich JL (1985) Bacterial Sensory Rhodopsin (SR), a Dual Attractant and Repellent Phototaxis Receptor, pp 119–127. Elsevier Science, AmsterdamGoogle Scholar
  64. Spudich JL (1998) Variations on a molecular switch: transport and sensory signalling by archael rhodopsins. Mol Microbiol 28: 1051–1058PubMedCrossRefGoogle Scholar
  65. Taylor BL (1983) Role of proton motive force in sensory transduction in bacteria. Ann Rev Microbiol 37: 551–573CrossRefGoogle Scholar
  66. Taylor BL and Zhulin IB (1998) In search of higher energy: metabolism-dependent behaviour in bacteria. Mol Microbiol 28: 683–690PubMedCrossRefGoogle Scholar
  67. Taylor BL, Zhulin IB and Johnson MS (1999) Aerotaxis and other energy-sensing behavior in bacteria. Annu Rev Microbiol 53:103–128PubMedCrossRefGoogle Scholar
  68. Vierstra RD and Davis SJ (2000) Bacteriophytochromes: new tools for understanding phytochrome signal transduction. Semin Cell Dev Biol 11: 511–521PubMedCrossRefGoogle Scholar
  69. Wilde A, Churin Y, Schubert H and Borner T (1997) Disruption of a Synechocystis sp. PCC6803 gene with partial similarity to phytochrome genes alters growth under changing light qualities. FEBS Lett 406: 89–92PubMedCrossRefGoogle Scholar
  70. Yang X-H, Sasarman A, Inokuchi H and Adler J (1996) Non-iron porphyrins cause tumbling to blue light by an Escherichia coli mutant defective in hemG. Proc Natl Acad Sci USA 93: 2459–2463PubMedCrossRefGoogle Scholar
  71. Yao VJ and Spudich JL (1992) Primary structure of an archaebacterial transducer, a methyl-accepting protein associated with sensory rhodopsin I. Proc Natl Acad Sci USA 89: 11915–11919PubMedCrossRefGoogle Scholar
  72. Yoshihara S, Suzuki F, Fujita H, Geng XX and Ikeuchi M (2000) Novel putative photoreceptor and regulatory genes required for the positive phototactic movement of the unicellular motile cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol 41: 1299–1304PubMedCrossRefGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2003

Authors and Affiliations

  1. 1.Department of Biochemistry, Microbiology UnitUniversity of OxfordUK
  2. 2.Swammerdam Institute for Life Sciences, Laboratory for Microbiology, Science FacultyUniversity of AmsterdamAmsterdamThe Netherlands

Personalised recommendations