Minor pilins are involved in motility and natural competence in the cyanobacterium Synechocystis sp. PCC 6803

. 2021 Sep ; 116 (3) : 743-765. [epub] 20210704

Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid34115422

Cyanobacteria synthesize type IV pili, which are known to be essential for motility, adhesion and natural competence. They consist of long flexible fibers that are primarily composed of the major pilin PilA1 in Synechocystis sp. PCC 6803. In addition, Synechocystis encodes less abundant pilin-like proteins, which are known as minor pilins. In this study, we show that the minor pilin PilA5 is essential for natural transformation but is dispensable for motility and flocculation. In contrast, a set of minor pilins encoded by the pilA9-slr2019 transcriptional unit are necessary for motility but are dispensable for natural transformation. Neither pilA5-pilA6 nor pilA9-slr2019 are essential for pilus assembly as mutant strains showed type IV pili on the cell surface. Three further gene products with similarity to PilX-like minor pilins have a function in flocculation of Synechocystis. The results of our study indicate that different minor pilins facilitate distinct pilus functions. Further, our microarray analysis demonstrated that the transcription levels of the minor pilin genes change in response to surface contact. A total of 122 genes were determined to have altered transcription between planktonic and surface growth, including several plasmid genes which are involved exopolysaccharide synthesis and the formation of bloom-like aggregates.

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Abramoff, M.D., Magalhaes, P.J. & Ram, S.J. (2004) Image processing with ImageJ. Biophotonics International, 11, 36-42.

Adams, D.W., Stutzmann, S., Stoudmann, C. & Blokesch, M. (2019) DNA-uptake pili of Vibrio cholerae are required for chitin colonization and capable of kin recognition via sequence-specific self-interaction. Nature Microbiology, 4, 1545-1557. https://doi.org/10.1038/s41564-019-0479-5

Agostoni, M., Koestler, B.J., Waters, C.M., Williams, B.L. & Montgomery, B.L. (2013) Occurrence of cyclic di-GMP-modulating output domains in cyanobacteria: an illuminating perspective. mBio, 4, 451-464. https://doi.org/10.1128/mBio.00451-13

Agostoni, M., Waters, C.M. & Montgomery, B.L. (2016) Regulation of biofilm formation and cellular buoyancy through modulating intracellular cyclic di-GMP levels in engineered cyanobacteria. Biotechnology and Bioengineering, 113, 311-319. https://doi.org/10.1002/bit.25712

Aldridge, C., Spence, E., Kirkilionis, M.A., Frigerio, L. & Robinson, C. (2008) Tat-dependent targeting of Rieske iron-sulphur proteins to both the plasma and thylakoid membranes in the cyanobacterium Synechocystis PCC 6803. Molecular Microbiology, 70, 140-150. https://doi.org/10.1111/j.1365-2958.2008.06401.x

Barten, R. & Lill, H. (1995) DNA-uptake in the naturally competent cyanobacterium, Synechocystis sp. PCC 6803. FEMS Microbiology Letters, 129, 83-87.

Belete, B., Lu, H. & Wozniak, D.J. (2008) Pseudomonas aeruginosa AlgR regulates type IV pilus biosynthesis by activating transcription of the fimU-pilVWXY1Y2E operon. Journal of Bacteriology, 190, 2023-2030.

Berry, J.L., Xu, Y., Ward, P.N., Lea, S.M., Matthews, S.J. & Pelicic, V. (2016) A comparative structure/function analysis of two type IV pilin DNA receptors defines a novel mode of DNA binding. Structure, 24, 926-934. https://doi.org/10.1016/j.str.2016.04.001

Beyer, H.M., Gonschorek, P., Samodelov, S.L., Meier, M., Weber, W. & Zurbriggen, M.D. (2015) AQUA cloning: a versatile and simple enzyme-free cloning approach. PLoS One, 10, e0137652. https://doi.org/10.1371/journal.pone.0137652

Bhaya, D., Bianco, N.R., Bryant, D. & Grossman, A. (2000) Type IV pilus biogenesis and motility in the cyanobacterium Synechocystis sp. PCC6803. Molecular Microbiology, 37, 941-951.

Bhaya, D., Takahashi, A., Shahi, P. & Grossman, A.R. (2001) Novel motility mutants of Synechocystis strain PCC 6803 generated by in vitro transposon mutagenesis. Journal of Bacteriology, 183, 6140-6143.

Bhaya, D., Watanabe, N., Ogawa, T. & Grossman, A.R. (1999) The role of an alternative sigma factor in motility and pilus formation in the cyanobacterium Synechocystis sp. strain PCC 6803. Proceedings of the National Academy of Sciences of the United States of America, 96, 3188-3193. https://doi.org/10.1073/pnas.96.6.3188

Burhenne, H. & Kaever, V. (2013) Quantification of cyclic dinucleotides by reversed-phase LC-MS/MS. Methods in Molecular Biology, 1016, 27-37.

Cehovin, A., Simpson, P.J., McDowell, M.A., Brown, D.R., Noschese, R., Pallett, M. et al. (2013) Specific DNA recognition mediated by a type IV pilin. Proceedings of the National Academy of Sciences of the United States of America, 110, 3065-3070. https://doi.org/10.1073/pnas.1218832110

Cengic, I., Uhlén, M. & Hudson, E.P. (2018) Surface display of small affinity proteins on Synechocystis sp. strain PCC 6803 mediated by fusion to the major type IV pilin PilA1. Journal of Bacteriology, 200, e00270-18.

Chandra, A., Joubert, L.-M. & Bhaya, D. (2017) Modulation of type IV pili phenotypic plasticity through a novel chaperone-usher system in Synechocystis sp. bioRxiv, 130278.

Conradi, F.D., Zhou, R.Q., Oeser, S., Schuergers, N., Wilde, A. & Mullineaux, C.W. (2019) Factors controlling floc formation and structure in the cyanobacterium Synechocystis sp. strain PCC 6803. Journal of Bacteriology, 201, e00344-19.

DeFlaun, M.F., Paul, J.H. & Davis, D. (1986) Simplified method for dissolved DNA determination in aquatic environments. Applied and Environment Microbiology, 52, 654-659. https://doi.org/10.1128/aem.52.4.654-659.1986

Denise, R., Abby, S.S. & Rocha, E.P.C. (2019) Diversification of the type IV filament superfamily into machines for adhesion, protein secretion, DNA uptake, and motility. PLoS Biology, 17, e3000390. https://doi.org/10.1371/journal.pbio.3000390

Dienst, D., Dühring, U., Mollenkopf, H.-J., Vogel, J., Golecki, J., Hess, W.R. et al. (2008) The cyanobacterial homologue of the RNA chaperone Hfq is essential for motility of Synechocystis sp. PCC 6803. Microbiology, 154, 3134-3143. https://doi.org/10.1099/mic.0.2008/020222-0

Eisenhut, M., Wobeser, E.A.V., Jonas, L., Schubert, H., Ibelings, B.W., Bauwe, H. et al. (2007) Long-term response toward inorganic carbon limitation in wild type and glycolate turnover mutants of the cyanobacterium Synechocystis sp. strain PCC 6803. Plant Physiology, 144, 1946-1959.

Elhai, J. & Wolk, C.P.P. (1988) Conjugal transfer of DNA to cyanobacteria. Methods in Enzymology, 167, 747-754.

Ellison, C.K., Dalia, T.N., Vidal Ceballos, A., Wang, J.-C.-Y.-Y., Biais, N., Brun, Y.V. et al. (2018) Retraction of DNA-bound type IV competence pili initiates DNA uptake during natural transformation in Vibrio cholerae. Nature Microbiology, 3, 773-780. https://doi.org/10.1038/s41564-018-0174-y

Georg, J., Dienst, D., Schürgers, N., Wallner, T., Kopp, D., Stazic, D. et al. (2014) The small regulatory RNA SyR1/PsrR1 controls photosynthetic functions in cyanobacteria. The Plant Cell, 26, 3661-3679. https://doi.org/10.1105/tpc.114.129767

Giltner, C.L., Habash, M. & Burrows, L.L. (2010) Pseudomonas aeruginosa minor pilins are incorporated into type IV pili. Journal of Molecular Biology, 398, 444-461. https://doi.org/10.1016/j.jmb.2010.03.028

Giltner, C.L., Nguyen, Y. & Burrows, L.L. (2012) Type IV pilin proteins: versatile molecular modules. Microbiology and Molecular Biology Reviews, 76, 740-772. https://doi.org/10.1128/MMBR.00035-12

Giner-Lamia, J., Robles-Rengel, R., Hernández-Prieto, M.A., Isabel Muro-Pastor, M., Florencio, F.J. & Futschik, M.E. (2017) Identification of the direct regulon of NtcA during early acclimation to nitrogen starvation in the cyanobacterium Synechocystis sp. PCC 6803. Nucleic Acids Research, 45, 11800-11820. https://doi.org/10.1093/nar/gkx860

Gordon, V.D. & Wang, L. (2019) Bacterial mechanosensing: the force will be with you, always. Journal of Cell Science, 132, jcs227694. https://doi.org/10.1242/jcs.227694

Grigorieva, G. & Shestakov, S. (1982) Transformation in the cyanobacterium Synechocystis sp. 6803. FEMS Microbiology Letters, 13, 367-370.

Harris, J.R. (1997) Negative staining and cryo-electron microscopy: the thin film techniques. In RMS, Microscopy Handbook. BIOS Scientific Publishers Ltd.

Hengge, R. (2021) High-specificity local and global c-di-GMP signaling. Trends in Microbiology, 24, S0966-842X(21)00037-8. Epub ahead of print.

Hernández-Prieto, M.A., Semeniuk, T.A., Giner-Lamia, J. & Futschik, M.E. (2016) The transcriptional landscape of the photosynthetic model cyanobacterium Synechocystis sp. PCC 6803. Scientific Reports, 6, 1-15. https://doi.org/10.1038/srep22168

Hu, J., Zhan, J., Chen, H., He, C., Cang, H. & Wang, Q. (2018) The small regulatory antisense RNA PilR affects pilus formation and cell motility by negatively regulating pilA11 in Synechocystis sp. PCC 6803. Frontiers in Microbiology, 9, 786. https://doi.org/10.3389/fmicb.2018.00786

Ibáñez de Aldecoa, A.L., Zafra, O. & González-Pastor, J.E. (2017) Mechanisms and regulation of extracellular DNA release and its biological roles in microbial communities. Frontiers in Microbiology, 8, 1390. https://doi.org/10.3389/fmicb.2017.01390

Jacobsen, T., Bardiaux, B., Francetic, O., Izadi-Pruneyre, N. & Nilges, M. (2020) Structure and function of minor pilins of type IV pili. Medical Microbiology and Immunology, 209, 301-308. https://doi.org/10.1007/s00430-019-00642-5

Jakob, A., Schuergers, N. & Wilde, A. (2017) Phototaxis assays of Synechocystis sp. PCC 6803 at macroscopic and microscopic scales. Bio-Protocol, 7, e2328.

Kaneko, T., Nakamura, Y., Sasamoto, S., Watanabe, A., Kohara, M., Matsumoto, M. et al. (2003) Structural analysis of four large plasmids harboring in a unicellular cyanobacterium, Synechocystis sp. PCC 6803. DNA Research, 10, 221-228. https://doi.org/10.1093/dnares/10.5.221

Kizawa, A., Kawahara, A., Takimura, Y., Nishiyama, Y. & Hihara, Y. (2016) RNA-seq profiling reveals novel target genes of LexA in the cyanobacterium Synechocystis sp. PCC 6803. Frontiers in Microbiology, 7, 193. https://doi.org/10.3389/fmicb.2016.00193

Klotz, A., Georg, J., Bučinská, L., Watanabe, S., Reimann, V., Januszewski, W. et al. (2016) Awakening of a dormant cyanobacterium from nitrogen chlorosis reveals a genetically determined program. Current Biology, 26, 2862-2872. https://doi.org/10.1016/j.cub.2016.08.054

Kopf, M., Klähn, S., Scholz, I., Matthiessen, J.K.F., Hess, W.R. & Voß, B. (2014) Comparative analysis of the primary transcriptome of Synechocystis sp. PCC 6803. DNA Research, 21, 527-539. https://doi.org/10.1093/dnares/dsu018

Korotkov, K.V. & Hol, W.G.J. (2008) Structure of the GspK-GspI-GspJ complex from the enterotoxigenic Escherichia coli type 2 secretion system. Nature Structural & Molecular Biology, 15, 462-468. https://doi.org/10.1038/nsmb.1426

Laventie, B.-J.-J. & Jenal, U. (2020) Surface sensing and adaptation in bacteria. Annual Review of Microbiology, 74, 735-760. https://doi.org/10.1146/annurev-micro-012120-063427

Laventie, B.-J., Sangermani, M., Estermann, F., Manfredi, P., Planes, R., Hug, I. et al. (2019) A surface-induced asymmetric program promotes tissue colonization by Pseudomonas aeruginosa. Cell Host & Microbe, 25, 140-152.e6. https://doi.org/10.1016/j.chom.2018.11.008

Linhartová, M., Bučinská, L., Halada, P., Ječmen, T., Šetlík, J., Komenda, J. et al. (2014) Accumulation of the type IV prepilin triggers degradation of SecY and YidC and inhibits synthesis of photosystem II proteins in the cyanobacterium Synechocystis PCC 6803. Molecular Microbiology, 93, 1207-1223.

Luscombe, N.M., Austin, S.E., Berman, H.M. & Thornton, J.M. (2000) An overview of the structures of protein-DNA complexes. Genome Biology, 1(reviews001), 1.

Maeda K., Okuda Y., Enomoto G., Watanabe S., Ikeuchi M. (2021) Biosynthesis of a sulfated exopolysaccharide, synechan, and bloom formation in the model cyanobacterium Synechocystis sp. strain PCC 6803. eLife, 10. http://dx.doi.org/10.7554/elife.66538

Mattick, J.S. (2002) Type IV pili and twitching motility. Annual Review of Microbiology, 56, 289-314. https://doi.org/10.1146/annurev.micro.56.012302.160938

Mitschke, J., Georg, J., Scholz, I., Sharma, C.M., Dienst, D., Bantscheff, J. et al. (2011) An experimentally anchored map of transcriptional start sites in the model cyanobacterium Synechocystis sp. PCC 6803. Proceedings of the National Academy of Sciences of the United States of America, 108, 2124-2129.

Nakane, D. & Nishizaka, T. (2017) Asymmetric distribution of type IV pili triggered by directional light in unicellular cyanobacteria. Proceedings of the National Academy of Sciences of the United States of America, 114, 6593-6598. https://doi.org/10.1073/pnas.1702395114

Nakasugi, K., Svenson, C.J. & Neilan, B.A. (2006) The competence gene, comF, from Synechocystis sp. strain PCC 6803 is involved in natural transformation, phototactic motility and piliation. Microbiology, 152, 3623-3631. https://doi.org/10.1099/mic.0.29189-0

Neuhaus, A., Selvaraj, M., Salzer, R., Langer, J.D., Kruse, K., Kirchner, L. et al. (2020) Cryo-electron microscopy reveals two distinct type IV pili assembled by the same bacterium. Nature Communications, 11, 1-13.

Ng, D., Harn, T., Altindal, T., Kolappan, S., Marles, J.M., Lala, R. et al. (2016) The Vibrio cholerae minor pilin TcpB initiates assembly and retraction of the toxin-coregulated pilus. PLoS Pathogens, 12, e1006109. https://doi.org/10.1371/journal.ppat.1006109

Nguyen, Y., Sugiman-Marangos, S., Harvey, H., Bell, S.D., Charlton, C.L., Junop, M.S. et al. (2015) Pseudomonas aeruginosa minor pilins prime type IVa pilus assembly and promote surface display of the PilY1 adhesin. Journal of Biological Chemistry, 290, 601-611. https://doi.org/10.1074/jbc.M114.616904

Niemeyer, J. & Gessler, F. (2002) Determination of free DNA in soils. Journal of Plant Nutrition and Soil Science, 165, 121. https://doi.org/10.1002/1522-2624(200204)165:2<121:AID-JPLN1111121>3.0.CO;2-X

Ohmori, M. & Okamoto, S. (2004) Photoresponsive cAMP signal transduction in cyanobacteria. Photochemical & Photobiological Sciences, 3, 503-511. https://doi.org/10.1039/b401623h

Omagari, K., Yoshimura, H., Suzuki, T., Takano, M., Ohmori, M. & Sarai, A. (2008) ΔG-based prediction and experimental confirmation of SyCRP1-binding sites on the Synechocystis genome. FEBS Journal, 275, 4786-4795. https://doi.org/10.1111/j.1742-4658.2008.06618.x

Orf, I., Schwarz, D., Kaplan, A., Kopka, J., Hess, W.R., Hagemann, M. et al. (2016) CyAbrB2 contributes to the transcriptional regulation of low CO2 acclimation in Synechocystis sp. PCC 6803. Plant and Cell Physiology, 57, 2232-2243.

Paul, J.H., Jeffrey, W.H., David, A.W., DeFlaun, M.F. & Cazares, L.H. (1989) Turnover of extracellular DNA in eutrophic and oligotrophic freshwater environments of Southwest Florida. Applied and Environment Microbiology, 55, 1823-1828. https://doi.org/10.1128/aem.55.7.1823-1828.1989

Pelicic, V. (2008) Type IV pili: E pluribus unum? Molecular Microbiology, 68, 827-837. https://doi.org/10.1111/j.1365-2958.2008.06197.x

Persat, A., Inclan, Y.F., Engel, J.N., Stone, H.A. & Gitai, Z. (2015) Type IV pili mechanochemically regulate virulence factors in Pseudomonas aeruginosa. Proceedings of the National Academy of Sciences of the United States of America, 112, 7563-7568.

Piepenbrink, K.H. (2019) DNA uptake by type IV filaments. Frontiers in Molecular Biosciences, 6, 1. https://doi.org/10.3389/fmolb.2019.00001

Pinto, F.L., Thapper, A., Sontheim, W. & Lindblad, P. (2009) Analysis of current and alternative phenol based RNA extraction methodologies for cyanobacteria. BMC Molecular Biology, 10, 79. https://doi.org/10.1186/1471-2199-10-79

Porcellinis, A.J.D., Klähn, S., Rosgaard, L., Kirsch, R., Gutekunst, K., Georg, J. et al. (2016) The non-coding RNA Ncr0700/PmgR1 is required for photomixotrophic growth and the regulation of glycogen accumulation in the cyanobacterium Synechocystis sp. PCC 6803. Plant and Cell Physiology, 57, 2091-2103.

Rodesney, C.A., Roman, B., Dhamani, N., Cooley, B.J., Katira, P., Touhami, A. et al. (2017) Mechanosensing of shear by Pseudomonas aeruginosa leads to increased levels of the cyclic-di-GMP signal initiating biofilm development. Proceedings of the National Academy of Sciences of the United States of America, 114, 5906-5911.

Rübsam, H., Kirsch, F., Reimann, V., Erban, A., Kopka, J., Hagemann, M. et al. (2018) The iron-stress activated RNA 1 (IsaR1) coordinates osmotic acclimation and iron starvation responses in the cyanobacterium Synechocystis sp. PCC 6803. Environmental Microbiology, 20, 2757-2768.

Saha, C.K., Sanches Pires, R., Brolin, H., Delannoy, M., Atkinson, G.C., Pires, R.S. et al. (2020) FlaGs and webFlaGs: Discovering novel biology through the analysis of gene neighbourhood conservation. Bioinformatics, 37, 1312-1314. btaa788.

Salleh, M.Z., Karuppiah, V., Snee, M., Thistlethwaite, A., Levy, C.W., Knight, D. et al. (2019) Structure and properties of a natural competence-associated pilin suggest a unique pilus tip-associated DNA receptor. mBio, 10, e00614-19. https://doi.org/10.1128/mBio.00614-19

Savakis, P., Causmaecker, S.D., Angerer, V., Ruppert, U., Anders, K., Essen, L.-O. et al. (2012) Light-induced alteration of c-di-GMP level controls motility of Synechocystis sp. PCC 6803. Molecular Microbiology, 85, 239-251. https://doi.org/10.1111/j.1365-2958.2012.08106.x

Schirmacher, A.M., Hanamghar, S.S. & Zedler, J.A.Z. (2020) Function and benefits of natural competence in cyanobacteria: From ecology to targeted manipulation. Life, 10, 249. https://doi.org/10.3390/life10110249

Schlebusch, M. & Forchhammer, K. (2010) Requirement of the nitrogen starvation-induced protein Sll0783 for polyhydroxybutyrate accumulation in Synechocystis sp. strain PCC 6803. Applied and Environment Microbiology, 76, 6101-6107.

Schuergers, N., Ruppert, U., Watanabe, S., Nürnberg, D.J., Lochnit, G., Dienst, D. et al. (2014) Binding of the RNA chaperone Hfq to the type IV pilus base is crucial for its function in Synechocystis sp. PCC 6803. Molecular Microbiology, 92, 840-852.

Schuergers, N. & Wilde, A. (2015) Appendages of the cyanobacterial cell. Life, 5, 700-715. https://doi.org/10.3390/life5010700

Sergeyenko, T.V. & Los, D.A. (2000) Identification of secreted proteins of the cyanobacterium Synechocystis sp. strain PCC 6803. FEMS Microbiology Letters, 193, 213-216.

Shibata, M., Ohkawa, H., Katoh, H., Shimoyama, M. & Ogawa, T. (2002) Two CO2 uptake systems in cyanobacteria: Four systems for inorganic carbon acquisition in Synechocystis sp. strain PCC 6803. Functional Plant Biology, 29, 123-129. https://doi.org/10.1071/PP01188

Song, W.Y., Zang, S.S., Li, Z.K., Dai, G.Z., Liu, K., Chen, M. et al. (2018) SyCRP2 is essential for twitching motility in the cyanobacterium Synechocystis sp. strain PCC 6803. Journal of Bacteriology, 200, e00436-18.

Stanier, R.Y., Deruelles, J., Rippka, R., Herdman, M. & Waterbury, J.B. (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. Journal of General Microbiology, 111, 1-61. https://doi.org/10.1099/00221287-111-1-1

Strom, M.S. & Lory, S. (1991) Amino acid substitutions in pilin of Pseudomonas aeruginosa. Effect on leader peptide cleavage, amino-terminal methylation, and pilus assembly. Journal of Biological Chemistry, 266, 1656-1664. https://doi.org/10.1016/S0021-9258(18)52345-0

Taton, A., Erikson, C., Yang, Y., Rubin, B.E., Rifkin, S.A., Golden, J.W. et al (2020) The circadian clock and darkness control natural competence in cyanobacteria. Nature Communications, 11, 1688. https://doi.org/10.1038/s41467-020-15384-9

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. https://doi.org/10.1093/oxfordjournals.pcp.a029534

Torsvik, V.L. & Goksoyr, J. (1978) Determination of bacterial DNA in soil. Soil Biology & Biochemistry, 10, 7-12. https://doi.org/10.1016/0038-0717(78)90003-2

Trautmann, D., Voß, B., Wilde, A., Al-Babili, S. & Hess, W.R. (2012) Microevolution in cyanobacteria: re-sequencing a motile substrain of Synechocystis sp. PCC 6803. DNA Research, 19, 435-448. https://doi.org/10.1093/dnares/dss024

Treuner-Lange, A., Chang, Y.-W., Glatter, T., Herfurth, M., Lindow, S., Chreifi, G. et al. (2020) PilY1 and minor pilins form a complex priming the type IVa pilus in Myxococcus xanthus. Nature Communications, 11, 1-14. https://doi.org/10.1038/s41467-020-18803-z

Trunk, T., Khalil, S.H. & Leo, J.C. (2018) Bacterial autoaggregation. AIMS Microbiology, 4, 140-164.

van Wolferen, M., Shajahan, A., Heinrich, K., Brenzinger, S., Black, I.M., Wagner, A. et al. (2020) Species-specific recognition of Sulfolobales mediated by UV-inducible pili and S-layer glycosylation patterns. mBio, 11, e03014-19.

Vorkapic, D., Pressler, K. & Schild, S. (2016) Multifaceted roles of extracellular DNA in bacterial physiology. Current Genetics, 62, 71-79. https://doi.org/10.1007/s00294-015-0514-x

Wallner, T., Pedroza, L., Voigt, K., Kaever, V. & Wilde, A. (2020) The cyanobacterial phytochrome 2 regulates the expression of phototaxis-related genes through the second messenger cyclic di-GMP. Photochemical & Photobiological Sciences, 19, 631-643.

Winther-Larsen, H.C., Hegge, F.T., Wolfgang, M., Hayes, S.F., Putten, J.P.M.V. & Koomey, M. (2001) Neisseria gonorrhoeae PilV, a type IV pilus-associated protein essential to human epithelial cell adherence. Proceedings of the National Academy of Sciences of the United States of America, 98, 15276-15281. https://doi.org/10.1073/pnas.261574998

Wolfgang, M., Putten, J.P.M.V., Hayes, S.F. & Koomey, M. (1999) The comP locus of Neisseria gonorrhoeae encodes a type IV prepilin that is dispensable for pilus biogenesis but essential for natural transformation. Molecular Microbiology, 31, 1345-1357. https://doi.org/10.1046/j.1365-2958.1999.01269.x

Yoshihara, S., Geng, XiaoXing, Okamoto, S., Yura, K., Murata, T., Go, M. et al. (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. https://doi.org/10.1093/pcp/pce007

Yoshimura, H., Yanagisawa, S., Kanehisa, M. & Ohmori, M. (2002) Screening for the target gene of cyanobacterial cAMP receptor protein SyCRP1. Molecular Microbiology, 43, 843-853. https://doi.org/10.1046/j.1365-2958.2002.02790.x

Yoshimura, H., Yoshihara, S., Okamoto, S., Ikeuchi, M. & Ohmori, M. (2002) A cAMP receptor protein, SyYCRP1, is responsible for the cell motility of Synechocystis sp. PCC 6803. Plant and Cell Physiology, 43, 460-463.

Yura, K., Toh, H. & Go, M. (1999) Putative mechanism of natural transformation as deduced from genome data. DNA Research, 6, 75-82. https://doi.org/10.1093/dnares/6.2.75

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