Cyanobacteria use micro-optics to sense light direction

eLife

Volumn 5, Issue FEBRUARY2016, 2016, Pages

  Schuergers, Nils ^a,h   Lenn, Tchern ^b   Kampmann, Ronald ^c   Meissner, Markus V ^c   Esteves, Tiago ^d,e   Temerinac Ott, Maja ^a   Korvink, Jan G ^c   Lowe, Alan R ^f,g   Mullineaux, Conrad W ^a,b   Wilde, Annegret ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^c KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

^d UNIVERSITY OF PORTO   (Portugal)

^e INEB INSTITUTO DE ENGENHARIA BIOMÉDICA   (Portugal)

^f LONDON CENTRE FOR NANOTECHNOLOGY   (United Kingdom)

^g UNIVERSITY OF LONDON   (United Kingdom)

^h EPFL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN; PIGMENT;

ARTICLE; BACTERIUM PILUS; CELL MOTILITY; FLUORESCENCE IMAGING; ILLUMINATION; LIGHT INTENSITY; MICROSCOPY; MOVEMENT PERCEPTION; NONHUMAN; OPTICS; PHOTOTAXIS; SYNECHOCYSTIS; LIGHT; LOCOMOTION; PHYSIOLOGY; RADIATION RESPONSE;

LIGHT; LOCOMOTION; SYNECHOCYSTIS;

EID: 84961262955     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.12620     Document Type: Article

References (57)

1. Agostinelli C, Lund U 2013. R package "circular": circular statistics version 0 4-7 at https://r-forge.r-project.org/projects/circular/
2. Alam M, Oesterhelt D. 1984. Morphology, function and isolation of halobacterial flagella. Journal of Molecular Biology 176:459-475.
3. Berg HC, Brown DA. 1972. Chemotaxis in Escherichia coli analysed by three-dimensional tracking. Nature 239: 500-504.
4. Bhaya D, Bianco NR, Bryant D, Grossman A. 2000. Type IV pilus biogenesis and motility in the cyanobacterium Synechocystis sp. PCC6803. Molecular Microbiology 37:941-951.
5. Bhaya D, Nakasugi K, Fazeli F, Burriesci MS. 2006. Phototaxis and impaired motility in adenylyl cyclase and cyclase receptor protein mutants of Synechocystis sp. strain PCC 6803. Journal of Bacteriology 188:7306-7310. doi: 10.1128/JB.00573-06
6. Bhaya D, Takahashi A, Grossman AR. 2001. Light regulation of type IV pilus-dependent motility by chemosensor-like elements in Synechocystis PCC6803. Proceedings of the National Academy of Sciences of the United States of America 98:7540-7545. doi: 10.1073/pnas.131201098
7. Bhaya D. 2004. Light matters: phototaxis and signal transduction in unicellular cyanobacteria. Molecular Microbiology 53:745-754. doi: 10.1111/j.1365-2958.2004.04160.x
8. Bulyha I, Schmidt C, Lenz P, Jakovljevic V, Hone A, Maier B, Hoppert M, Søgaard-And ersen L. 2009. Regulation of the type IV pili molecular machine by dynamic localization of two motor proteins. Molecular Microbiology 74:691-706. doi: 10.1111/j.1365-2958.2009.06891.x
9. Chau RM, Ursell T, Wang S, Huang KC, Bhaya D. 2015. Maintenance of motility bias during cyanobacterial phototaxis. Biophysical Journal 108:1623-1632. doi: 10.1016/j.bpj.2015.01.042
10. Choi JS, Chung YH, Moon YJ, Kim C, Watanabe M, Song PS. 1999. Photomovement of the gliding cyanobacterium Synechocystis sp. PCC 6803. Photochemistry and Photobiology 70:95-102.
11. Duysens LN. 1956. The flattening of the absorption spectrum of suspensions, as compared to that of solutions. Biochimica et Biophysica Acta 19:12.
12. Ehlers K, Oster G. 2012. On the mysterious propulsion of Synechococcus. PloS One 7:e36081. doi: 10.1371/journal.pone.0036081
13. Engelmann TW. 1883. Bacterium photometricum. Ein Beitrag zur vergleichenden Physiologie des Licht-und Farbensinnes. Pfluegers Arch. Gesamte Physiol. Menschen Tiere 30:95-124.
14. Esteves T, Oliveira MJ, Quelhas P. 2013a. Cancer cell detection and tracking based on local interest point detectors. In: Kamel M, Campilho A, eds. Image Analysis and Recognition SE - 49. Berlin, Heidelberg: Springer. 434-441. doi: 10.1007/978-3-642-39094-4_49
15. Esteves T, Oliveira MJ, Quelhas P. 2013b. Cancer cell detection and morphology analysis based on local interest point detectors. In: Sanches J, Mico L, Cardoso J, eds. Pattern Recognition and Image Analysis SE - 74. Berlin, Heidelberg: Springer. 624-631. doi: 10.1007/978-3-642-38628-2_74
16. FerrandP, Wenger J, Devilez A, Pianta M, Stout B, Bonod N, Popov E, Rigneault H. 2008. Direct imaging of photonic nanojets. Optics Express 16:6930-6940. doi: 10.1364/OE.16.006930
17. Fiedler B, Borner T, Wilde A. 2005. Phototaxis in the cyanobacterium Synechocystis sp. PCC 6803: role of different photoreceptors. Photochemistry and Photobiology 81:1481-1488. doi: 10.1562/2005-06-28-RA-592
18. Gal. 1994. US Patent 5,310,623.
19. Heifetz A, Kong SC, Sahakian AV, Taflove A, Backman V. 2009. Photonic nanojets. Journal of Computational and Theoretical Nanoscience 6:1979-1992. doi: 10.1166/jctn.2009.1254
20. HildebrandE, Dencher N. 1975. Two photosystems controlling behavioural responses of halobacterium halobium. Nature 257:46-48. doi: 10.1038/257046a0
21. Hader D-P, Burkart U. 1983. Optical properties of Dictyostelium discoideum pseudoplasmodia responsible for phototactic orientation. Experimental Mycology 7:8. doi: 10.1016/0147-5975(83)90069-5
22. Hader DP. 1987. Photosensory behavior in procaryotes. Microbiological Reviews 51:1-21.
23. Khayatan B, Meeks JC, Risser DD. 2015. Evidence that a modified type IV pilus-like system powers gliding motility and polysaccharide secretion in filamentous cyanobacteria. Molecular Microbiology 98:1021-1036. doi: 10.1111/mmi.13205
24. Kondou Y, Mogami N, Hoshi F, Kutsuna S, Nakazawa M, Sakurai T, Matsui M, Kaneko T, Tabata S, Tanaka I, Manabe K. 2002. Bipolar localization of putative photoreceptor protein for phototaxis in thermophilic cyanobacterium synechococcus elongatus. Plant and Cell Physiology 43:1585-1588. doi: 10.1093/pcp/pcf176
25. Kondou Y, Nakazawa M, Higashi Sho-ichi, Watanabe M, Manabe K. 2001. Equal-quantum action spectra indicate fluence-rate-selective action of multiple photoreceptors for photomovement of the thermophilic cyanobacterium synechococcus elongatus. Photochemistry and Photobiology 73:90-95. doi: 10.1562/0031-8655(2001)073<0090:EQASIF>2.0.CO;2
26. Kreimer G. 2009. The green algal eyespot apparatus: a primordial visual system and more? Current Genetics 55: 19-43. doi: 10.1007/s00294-008-0224-8
27. LaBianca NC, Gelorme JD. 1995. High-aspect-ratio resist for thick-film applications. In: Allen RD, ed, SPIEs 1995 Symposium on Microlithography. pp 846-852.
28. Lindeberg T. 1994. Scale-space theory: a basic tool for analyzing structures at different scales. Journal of Applied Statistics 21:225-270. doi: 10.1080/757582976
29. Lowe AR, Tang JH, Yassif J, Graf M, Huang WYC, Groves JT, Weis K, Liphardt JT. 2015. Importin-b modulates the permeability of the nuclear pore complex in a ran-dependent manner. eLife 4:e04052. doi: 10.7554/eLife.04052
30. Mann NH, Novac N, Mullineaux CW, Newman J, Bailey S, Robinson C. 2000. Involvement of an FtsH homologue in the assembly of functional photosystem I in the cyanobacterium Synechocystis sp. PCC 6803. FEBS Letters 479:72-77. doi: 10.1016/S0014-5793(00)01871-8
31. Merz AJ, So M, Sheetz MP. 2000. Pilus retraction powers bacterial twitching motility. Nature 407:98-102. doi: 10.1038/35024105
32. Myers J, Graham J-R, Wang RT 1980. Light harvesting in anacystis nidulans studied in pigment mutants. Plant Physiology 66:1144-1149. doi: 10.1104/pp 66.6.1144
33. Ng W-O, Grossman AR, Bhaya D. 2003. Multiple light inputs control phototaxis in synechocystis sp. Strain PCC6803. Journal of Bacteriology 185:1599-1607. doi: 10.1128/JB.185.5.1599-1607.2003
34. Pisareva T, Shumskaya M, Maddalo G, Ilag L, Norling B. 2007. Proteomics of synechocystis sp. PCC 6803. FEBS Journal 274:791-804. doi: 10.1111/j.1742-4658.2006.05624.x
35. Pringsheim EG. 1968. Cyanophyceen-Studien. Archives of Microbiology 63:331-355. doi: 10.1007/BF00412120
36. R Core Team. 2013. R: a language and environment for statistical computing. R Found Stat Comput:Vienna, Austria. https://www.r-project.org/.
37. Ragatz L, Jiang Z-Y, Bauer CE, Gest H. 1995. Macroscopic phototactic behavior of the purple photosynthetic bacterium rhodospirillum centenum. Archives of Microbiology 163:6. doi: 10.1007/BF00262196
38. Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY. 1979. Generic assignments, strain histories and properties of pure cultures of cyanobacteria. Journal of General Microbiology 111:61. doi: 10.1099/00221287-111-1-1
39. Samuel ADT, Petersen JD, Reese TS. 2001. Envelope structure of synechococcus sp. WH8113, a nonflagellated swimming cyanobacterium. BMC Microbiology 1:4. doi: 10.1186/1471-2180-1-4
40. Savakis P, De Causmaecker S, Angerer V, Ruppert U, and ers K, Essen L-O, Wilde A. 2012. Light-induced alteration of c-di-GMP level controls motility of Synechocystis sp. PCC 6803. Molecular Microbiology 85:239-251. doi: 10.1111/j.1365-2958.2012.08106.x
41. Schmidt S. 2013. The interactive FTDT toolbox (iFTDT). http://www.problemsinelectrodynamics.com/tools/interactive-fdtd-toolbox.
42. Schuergers N, Nurnberg DJ, Wallner T, Mullineaux CW, Wilde A. 2015. PilB localization correlates with the direction of twitching motility in the cyanobacterium Synechocystis sp. PCC 6803. Microbiology 161:960-966. doi: 10.1099/mic.0.000064
43. Shropshire W. 1962. The lens effect and phototropism of phycomyces. The Journal of General Physiology 45: 949-958. doi: 10.1085/jgp.45.5.949
44. Sourjik V, Wingreen NS. 2012. Responding to chemical gradients: bacterial chemotaxis. Current Opinion in Cell Biology 24:262-268. doi: 10.1016/j.ceb.2011.11.008
45. Spence E, Sarcina M, Ray N, Møller SG, Mullineaux CW, Robinson C. 2003. Membrane-specific targeting of green fluorescent protein by the tat pathway in the cyanobacterium synechocystis PCC6803. Molecular Microbiology 48:1481-1489. doi: 10.1046/j.1365-2958.2003.03519.x
46. Stanier RY, Kunisawa R, Mand el M, Cohen-Bazire G. 1971. Purification and properties of unicellular blue-green algae (order chroococcales). Bacteriological Reviews 35:171-205.
47. Sugiura K, Itoh S. 2012. Single-cell confocal spectrometry of a filamentous cyanobacterium Nostoc at room and cryogenic temperature. Diversity and differentiation of pigment systems in 311 cells. Plant and Cell Physiology 53:1492-1506. doi: 10.1093/pcp/pcs093
48. Terauchi K, Ohmori M. 1999. An adenylate cyclase, cyal, regulates cell motility in the cyanobacterium Synechocystis sp. PCC 6803. Plant and Cell Physiology 40:248-251. doi: 10.1093/oxfordjournals.pcp.a029534
49. Trautmann D, Voss B, Wilde A, Al-Babili S, Hess WR. 2012. Microevolution in cyanobacteria: re-sequencing a motile substrain of Synechocystis sp. PCC 6803. DNA Research 19:435-448. doi: 10.1093/dnares/dss024
50. Wadhams GH, Armitage JP. 2004. Making sense of it all: bacterial chemotaxis. Nature Reviews. Molecular Cell Biology 5:1024-1037. doi: 10.1038/nrm1524
51. Wilde A, Mullineaux CW. 2015. Motility in cyanobacteria: polysaccharide tracks and type IV pilus motors. Molecular Microbiology 98:998-1001. doi: 10.1111/mmi.13242
52. Willey JM, Waterbury JB 1989. Chemotaxis toward nitrogenous compounds by swimming strains of marine synechococcus spp. Applied and Environmental Microbiology 55:1888-1894
53. Wuichet K, Zhulin IB. 2010. Origins and diversification of a complex signal transduction system in prokaryotes. Science Signaling 3:ra50. doi: 10.1126/scisignal.2000724
54. Yee SK. 1966. Numerical solution of initial boundary value problems involving Maxwell’s equations in isotropic media. IEEE Transactions on Antennas and Propagation 14:302-307.
55. Yoshihara S, Geng XX, Okamoto S, Yura K, Murata T, Go M, Ohmori M, Ikeuchi M. 2001. Mutational analysis of genes involved in pilus structure, motility and transformation competency in the unicellular motile Cyanobacterium Synechocystis sp. PCC 6803. Plant and Cell Physiology 42:63-73. doi: 10.1093/pcp/pce007
56. Yoshihara S, Ikeuchi M. 2004. Phototactic motility in the unicellular cyanobacterium Synechocystis sp. PCC 6803. Photochemical and Photobiological Sciences 3:512-518. doi: 10.1039/b402320j
57. Yoshihara S, Suzuki F, Fujita H, Geng XX, 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 and Cell Physiology 41:1299-1304. doi: 10.1093/pcp/pce010