Pseudomonas aeruginosa post-translational responses to elevated c-di-GMP levels.
Pseudomonas aeruginosa
RNA-seq
c-di-GMP
proteome
ribosome profiling
Journal
Molecular microbiology
ISSN: 1365-2958
Titre abrégé: Mol Microbiol
Pays: England
ID NLM: 8712028
Informations de publication
Date de publication:
05 2022
05 2022
Historique:
revised:
22
03
2022
received:
05
10
2021
accepted:
27
03
2022
pubmed:
2
4
2022
medline:
31
5
2022
entrez:
1
4
2022
Statut:
ppublish
Résumé
C-di-GMP signaling can directly influence bacterial behavior by affecting the functionality of c-di-GMP-binding proteins. In addition, c-di-GMP can exert a global effect on gene transcription or translation, for example, via riboswitches or by binding to transcription factors. In this study, we investigated the effects of changes in intracellular c-di-GMP levels on gene expression and protein production in the opportunistic pathogen Pseudomonas aeruginosa. We induced c-di-GMP production via an ectopically introduced diguanylate cyclase and recorded the transcriptional, translational as well as proteomic profile of the cells. We demonstrate that rising levels of c-di-GMP under growth conditions otherwise characterized by low c-di-GMP levels caused a switch to a non-motile, auto-aggregative P. aeruginosa phenotype. This phenotypic switch became apparent before any c-di-GMP-dependent role on transcription, translation, or protein abundance was observed. Our results suggest that rising global c-di-GMP pools first affects the motility phenotype of P. aeruginosa by altering protein functionality and only then global gene transcription.
Substances chimiques
Bacterial Proteins
0
Escherichia coli Proteins
0
bis(3',5')-cyclic diguanylic acid
61093-23-0
Cyclic GMP
H2D2X058MU
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1213-1226Informations de copyright
© 2022 The Authors. Molecular Microbiology published by John Wiley & Sons Ltd.
Références
Ahmad, I., Cimdins, A., Beske, T. & Römling, U. (2017) Detailed analysis of c-di-GMP mediated regulation of csgD expression in salmonella typhimurium. BMC Microbiology, 17(1), 1-12. https://doi.org/10.1186/s12866-017-0934-5
Aldridge, P., Paul, R., Goymer, P., Rainey, P. & Jenal, U. (2003) Role of the GGDEF regulator PleD in polar development of Caulobacter crescentus. Molecular Microbiology, 47(6), 1695-1708. https://doi.org/10.1046/j.1365-2958.2003.03401.x
Almblad, H., Harrison, J.J., Rybtke, M., Groizeleau, J., Givskov, M., Parsek, M.R. et al. (2015) The cyclic AMP-Vfr signaling pathway in Pseudomonas aeruginosa is inhibited by cyclic Di-GMP. Journal of Bacteriology, 197(13), 2190-2200. https://doi.org/10.1128/JB.00193-15
Arora, S.K., Ritchings, B.W., Almira, E.C., Lory, S. & Ramphal, R. (1997) A transcriptional activator, FleQ, regulates mucin adhesion and flagellar gene expression in Pseudomonas aeruginosa in a cascade manner. Journal of Bacteriology, 179(17), 5574-5581. https://doi.org/10.1128/JB.179.17.5574-5581.1997
Baker, A.E., Diepold, A., Kuchma, S.L., Scott, J.E., Ha, D.G., Orazi, G. et al. (2016) PilZ domain protein FlgZ mediates cyclic Di-GMP-dependent swarming motility control in Pseudomonas aeruginosa. Journal of Bacteriology, 198(13), 1837-1846. https://doi.org/10.1128/JB.00196-16
Baraquet, C., Murakami, K., Parsek, M.R. & Harwood, C.S. (2012) The FleQ protein from Pseudomonas aeruginosa functions as both a repressor and an activator to control gene expression from the Pel operon promoter in response to c-di-GMP. Nucleic Acids Research, 40(15), 7207-7218. https://doi.org/10.1093/nar/gks384
Basu Roy, A. & Sauer, K. (2014) Diguanylate cyclase NicD-based signalling mechanism of nutrient-induced dispersion by Pseudomonas aeruginosa. Molecular Microbiology, 94(4), 771-793. https://doi.org/10.1111/mmi.12802
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(6), 2023-2030. https://doi.org/10.1128/JB.01623-07
Benjamini, Y. & Hochberg, Y. (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society: Series B (Methodological), 57(1), 289-300. https://doi.org/10.1111/j.2517-6161.1995.tb02031.x
Bense, S., Bruchmann, S., Steffen, A., Stradal, T.E.B., Häussler, S. & Düvel, J. (2019) Spatiotemporal control of FlgZ activity impacts Pseudomonas aeruginosa flagellar motility. Molecular Microbiology, 111(6), 1544-1557. https://doi.org/10.1111/mmi.14236
de Bentzmann, S. & Plésiat, P. (2011) The Pseudomonas aeruginosa opportunistic pathogen and human infections. Environmental Microbiology, 13(7), 1655-1665. https://doi.org/10.1111/J.1462-2920.2011.02469.X
Bhattacharyya, R.P., Bandyopadhyay, N., Ma, P., Son, S.S., Liu, J., He, L.L. et al. (2019) Simultaneous detection of genotype and phenotype enables rapid and accurate antibiotic susceptibility determination. Nature Medicine, 25(12), 1858-1864. https://doi.org/10.1038/s41591-019-0650-9
Blanka, A., Düvel, J., Dötsch, A., Klinkert, B., Abraham, W.R., Kaever, V. et al. (2015) Constitutive production of c-di-GMP is associated with mutations in a variant of Pseudomonas aeruginosa with altered membrane composition. Science Signaling, 8(372), ra36. https://doi.org/10.1126/scisignal.2005943
Boehm, A., Kaiser, M., Li, H., Spangler, C., Kasper, C.A., Ackermann, M. et al. (2010) Second messenger-mediated adjustment of bacterial swimming velocity. Cell, 141(1), 107-116. https://doi.org/10.1016/j.cell.2010.01.018
Borrero-de Acuña, J.M., Molinari, G., Rohde, M., Dammeyer, T., Wissing, J., Jänsch, L. et al. (2015) A periplasmic complex of the nitrite reductase NirS, the chaperone DnaK, and the flagellum protein FliC is essential for flagellum assembly and motility in Pseudomonas aeruginosa. Journal of Bacteriology, 197(19), 3066-3075. https://doi.org/10.1128/JB.00415-15
Brencic, A. & Lory, S. (2009) Determination of the regulon and identification of novel mRNA targets of Pseudomonas aeruginosa RsmA. Molecular Microbiology, 72(3), 612-632. https://doi.org/10.1111/j.1365-2958.2009.06670.x
Brencic, A., McFarland, K.A., McManus, H.R., Castang, S., Mogno, I., Dove, S.L. et al. (2009) The GacS/GacA signal transduction system of Pseudomonas aeruginosa acts exclusively through its control over the transcription of the RsmY and RsmZ regulatory small RNAs. Molecular Microbiology, 73(3), 434-445. https://doi.org/10.1111/j.1365-2958.2009.06782.x
Chambers, J.R., Liao, J., Schurr, M.J. & Sauer, K. (2014) BrlR from Pseudomonas aeruginosa is a c-di-GMP-responsive transcription factor. Molecular Microbiology, 92(3), 471-487. https://doi.org/10.1111/mmi.12562
Chambers, J.R. & Sauer, K. (2013) The MerR-like regulator BrlR impairs Pseudomonas aeruginosa biofilm tolerance to colistin by repressing PhoPQ. Journal of Bacteriology, 195(20), 4678-4688. https://doi.org/10.1128/JB.00834-13
Chan, C., Paul, R., Samoray, D., Amiot, N.C., Giese, B., Jenal, U. et al. (2004) Structural basis of activity and allosteric control of diguanylate cyclase. Proceedings of the National Academy of Sciences of the United States of America, 101(49), 17084-17089. https://doi.org/10.1073/pnas.0406134101
Chin, K.H., Lee, Y.C., Le Tu, Z., Chen, C.H., Tseng, Y.H., Yang, J.M. et al. (2010) The cAMP receptor-like protein CLP is a novel c-di-GMP receptor linking cell-cell signaling to virulence gene expression in Xanthomonas campestris. Journal of Molecular Biology, 396(3), 646-662. https://doi.org/10.1016/j.jmb.2009.11.076
Choi, M., Chang, C.-Y., Clough, T., Broudy, D., Killeen, T., MacLean, B. et al. (2014) MSstats: an R package for statistical analysis of quantitative mass spectrometry-based proteomic experiments. Bioinformatics, 30(17), 2524-2526. https://doi.org/10.1093/bioinformatics/btu305
Chou, S.H. & Galperin, M.Y. (2016) Diversity of cyclic di-GMP-binding proteins and mechanisms. Journal of Bacteriology, 198, 32-46. https://doi.org/10.1128/JB.00333-15
Christen, B., Christen, M., Paul, R., Schmid, F., Folcher, M., Jenoe, P. et al. (2006) Allosteric control of cyclic di-GMP signaling. The Journal of Biological Chemistry, 281(42), 32015-32024. https://doi.org/10.1074/jbc.M603589200
Cox, J. & Mann, M. (2008) MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nature Biotechnology, 26(12), 1367-1372. https://doi.org/10.1038/nbt.1511
Cox, J., Neuhauser, N., Michalski, A., Scheltema, R.A., Olsen, J.V. & Mann, M. (2011) Andromeda: a peptide search engine integrated into the MaxQuant environment. Journal of Proteome Research, 10(4), 1794-1805. https://doi.org/10.1021/pr101065j
Cutruzzolà, F. & Frankenberg-Dinkel, N. (2016) Origin and impact of nitric oxide in Pseudomonas aeruginosa biofilms. Journal of Bacteriology, 198, 55-65. https://doi.org/10.1128/JB.00371-15
Deutsch, E.W., Bandeira, N., Sharma, V., Perez-Riverol, Y., Carver, J.J., Kundu, D.J. et al. (2020) The ProteomeXchange consortium in 2020: enabling “big data” approaches in proteomics. Nucleic Acids Research, 48(D1), D1145-D1152. https://doi.org/10.1093/nar/gkz984
Drake, H.L. (2015) PilZ domain proteins of the plant pathogen Xanthomonas oryzae pv. Oryzae function differentially in virulence. Applied and Environmental Microbiology, 81, 4233-4234. https://doi.org/10.1128/AEM.01322-15
Fang, X. & Gomelsky, M. (2010) A post-translational, c-di-GMP-dependent mechanism regulating flagellar motility. Molecular Microbiology, 76(5), 1295-1305. https://doi.org/10.1111/j.1365-2958.2010.07179.x
Fernandez, N.L., Hsueh, B.Y., Nhu, N.T.Q., Franklin, J.L., Dufour, Y.S. & Waters, C.M. (2020) Vibrio cholerae adapts to sessile and motile lifestyles by cyclic di-GMP regulation of cell shape. Proceedings of the National Academy of Sciences of the United States of America, 117(46), 29046-29054. https://doi.org/10.1073/pnas.2010199117
Frank, D.W. (1997) The exoenzyme S regulon of Pseudomonas aeruginosa. Molecular Microbiology, 26, 621-629. https://doi.org/10.1046/j.1365-2958.1997.6251991.x
Fulcher, N.B., Holliday, P.M., Klem, E., Cann, M.J. & Wolfgang, M.C. (2010) The Pseudomonas aeruginosa Chp chemosensory system regulates intracellular cAMP levels by modulating adenylate cyclase activity. Molecular Microbiology, 76(4), 889-904. https://doi.org/10.1111/j.1365-2958.2010.07135.x
Green, S.K., Schroth, M.N., Cho, J.J., Kominos, S.D. & Vitanza-Jack, V.B. (1974) Agricultural plants and soil as a reservoir for Pseudomonas aeruginosa. Applied Microbiology, 28(6), 987-991. https://doi.org/10.1128/am.28.6.987-991.1974
Guzzo, C.R., Dunger, G., Salinas, R.K. & Farah, C.S. (2013) Structure of the PilZ-FimXEAL-c-di-GMP complex responsible for the regulation of bacterial type IV pilus biogenesis. Journal of Molecular Biology, 425(12), 2174-2197. https://doi.org/10.1016/J.JMB.2013.03.021
Hammerschmidt, S. & Rohde, M. (2019) Electron microscopy to study the fine structure of the pneumococcal cell. Methods in Molecular Biology, 1968, 13-33. https://doi.org/10.1007/978-1-4939-9199-0_2
Hengge, R. (2009) Principles of c-di-GMP signalling in bacteria. Nature Reviews Microbiology, 7(4), 263-273. https://doi.org/10.1038/nrmicro2109
Hickman, J.W. & Harwood, C.S. (2008) Identification of FleQ from Pseudomonas aeruginosa as a c-di-GMP-responsive transcription factor. Molecular Microbiology, 69(2), 376-389. https://doi.org/10.1111/j.1365-2958.2008.06281.x
Ingolia, N.T., Brar, G.A., Rouskin, S., McGeachy, A.M. & Weissman, J.S. (2012) The ribosome profiling strategy for monitoring translation in vivo by deep sequencing of ribosome-protected mRNA fragments. Nature Protocols, 7(8), 1534-1550. https://doi.org/10.1038/nprot.2012.086
Ingolia, N.T., Ghaemmaghami, S., Newman, J.R.S. & Weissman, J.S. (2009) Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science, 324(5924), 218-223. https://doi.org/10.1126/science.1168978
Jenal, U. & Malone, J. (2006) Mechanisms of cyclic-di-GMP signaling in bacteria. Annual Review of Genetics, 40, 385-407. https://doi.org/10.1146/annurev.genet.40.110405.090423
Jones, A.K., Fulcher, N.B., Balzer, G.J., Urbanowski, M.L., Pritchett, C.L., Schurr, M.J. et al. (2010) Activation of the Pseudomonas aeruginosa AlgU regulon through mucA mutation inhibits cyclic AMP/Vfr signaling. Journal of Bacteriology, 192(21), 5709-5717. https://doi.org/10.1128/JB.00526-10
Jones, C.J., Utada, A., Davis, K.R., Thongsomboon, W., Zamorano Sanchez, D., Banakar, V. et al. (2015) C-di-GMP regulates motile to sessile transition by modulating MshA pili biogenesis and near-surface motility behavior in vibrio cholerae. PLoS Pathogens, 11(10), e1005068. https://doi.org/10.1371/journal.ppat.1005068
Kong, W., Zhao, J., Kang, H., Zhu, M., Zhou, T., Deng, X. et al. (2015) ChIP-seq reveals the global regulator AlgR mediating cyclic di-GMP synthesis in Pseudomonas aeruginosa. Nucleic Acids Research, 43(17), 8268-8282. https://doi.org/10.1093/nar/gkv747
Krasteva, P.V., Fong, J.C.N., Shikuma, N.J., Beyhan, S., Navarro, M.V.A.S., Yildiz, F.H. et al. (2010) Vibrio cholerae VpsT regulates matrix production and motility by directly sensing cyclic di-GMP. Science (New York, N.Y.), 327(5967), 866-868. https://doi.org/10.1126/science.1181185
Kuchma, S.L., Ballok, A.E., Merritt, J.H., Hammond, J.H., Lu, W., Rabinowitz, J.D. et al. (2010) Cyclic-di-GMP-mediated repression of swarming motility by Pseudomonas aeruginosa: the pilY1 gene and its impact on surface-associated behaviors. Journal of Bacteriology, 192(12), 2950-2964. https://doi.org/10.1128/JB.01642-09
Kulasakara, H., Lee, V., Brencic, A., Liberati, N., Urbach, J., Miyata, S. et al. (2006) Analysis of Pseudomonas aeruginosa diguanylate cyclases and phosphodiesterases reveals a role for bis-(3′-5′)-cyclic-GMP in virulence. Proceedings of the National Academy of Sciences of the United States of America, 103(8), 2839-2844. https://doi.org/10.1073/pnas.0511090103
Langmead, B. & Salzberg, S.L. (2012) Fast gapped-read alignment with bowtie 2. Nature Methods, 9(4), 357-359. https://doi.org/10.1038/nmeth.1923
Langmead, B., Trapnell, C., Pop, M. & Salzberg, S.L. (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biology, 10(3), R25. https://doi.org/10.1186/gb-2009-10-3-r25
Lee, E.R., Baker, J.L., Weinberg, Z., Sudarsan, N. & Breaker, R.R. (2010) An allosteric self-splicing ribozyme triggered by a bacterial second messenger. Science, 329(5993), 845-848. https://doi.org/10.1126/science.1190713
Liao, J., Schurr, M.J. & Sauera, K. (2013) The MerR-like regulator BrlR confers biofilm tolerance by activating multidrug efflux pumps in Pseudomonas aeruginosa biofilms. Journal of Bacteriology, 195(15), 3352-3363. https://doi.org/10.1128/JB.00318-13
Litschko, C., Budde, I., Berger, M., & Fiebig, T. (2021). Exploitation of capsule polymerases for enzymatic synthesis of polysaccharide antigens used in glycoconjugate vaccines. In Methods in molecular biology (vol. 2183, pp. 313-330). https://doi.org/10.1007/978-1-0716-0795-4_16
Luo, Y., Zhao, K., Baker, A.E., Kuchma, S.L., Coggan, K.A., Wolfgang, M.C. et al. (2015) A hierarchical cascade of second messengers regulates Pseudomonas aeruginosa surface behaviors. MBio, 6(1), 1-11. https://doi.org/10.1128/mBio.02456-14
Malone, J.G., Williams, R., Christen, M., Jenal, U., Spiers, A.J. & Rainey, P.B. (2007) The structure-function relationship of WspR, a Pseudomonas fluorescens response regulator with a GGDEF output domain. Microbiology, 153(4), 980-994. https://doi.org/10.1099/mic.0.2006/002824-0
Marko, V.A., Kilmury, S.L.N., MacNeil, L.T. & Burrows, L.L. (2018) Pseudomonas aeruginosa type IV minor pilins and PilY1 regulate virulence by modulating FimS-AlgR activity. PLoS Pathogens, 14(5), e1007074. https://doi.org/10.1371/journal.ppat.1007074
Marsden, A.E., Intile, P.J., Schulmeyer, K.H., Simmons-Patterson, E.R., Urbanowski, M.L., Wolfgang, M.C. et al. (2016) Vfr directly activates exsA transcription to regulate expression of the Pseudomonas aeruginosa type III secretion system. Journal of Bacteriology, 198(9), 1442-1450. https://doi.org/10.1128/JB.00049-16
Martin, M. (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet Journal, 17(1), 10. https://doi.org/10.14806/ej.17.1.200
de Matos Simoes, R. & Emmert-Streib, F. (2012) Bagging statistical network inference from large-scale gene expression data. PLoS One, 7(3), 33624. https://doi.org/10.1371/journal.pone.0033624
Merighi, M., Lee, V.T., Hyodo, M., Hayakawa, Y. & Lory, S. (2007) The second messenger bis-(3′-5′)-cyclic-GMP and its PilZ domain-containing receptor Alg44 are required for alginate biosynthesis in Pseudomonas aeruginosa. Molecular Microbiology, 65(4), 876-895. https://doi.org/10.1111/j.1365-2958.2007.05817.x
Morgan, J.L.W., McNamara, J.T. & Zimmer, J. (2014) Mechanism of activation of bacterial cellulose synthase by cyclic di-GMP. Nature Structural and Molecular Biology, 21(5), 489-496. https://doi.org/10.1038/nsmb.2803
Morici, L.A., Carterson, A.J., Wagner, V.E., Frisk, A., Schurr, J.R., Höner zu Bentrup, K. et al. (2007) Pseudomonas aeruginosa AlgR represses the Rhl quorum-sensing system in a biofilm-specific manner. Journal of Bacteriology, 189(21), 7752-7764. https://doi.org/10.1128/JB.01797-06
Moscoso, J.A., Jaeger, T., Valentini, M., Hui, K., Jenal, U. & Filloux, A. (2014) The diguanylate cyclase SadC is a central player in Gac/Rsm-mediated biofilm formation in Pseudomonas aeruginosa. Journal of Bacteriology, 196(23), 4081-4088. https://doi.org/10.1128/JB.01850-14
Moscoso, J.A., Mikkelsen, H., Heeb, S., Williams, P. & Filloux, A. (2011) The Pseudomonas aeruginosa sensor RetS switches type III and type VI secretion via c-di-GMP signalling. Environmental Microbiology, 13(12), 3128-3138. https://doi.org/10.1111/j.1462-2920.2011.02595.x
Mulcahy, H., O’Callaghan, J., O’Grady, E.P., Adams, C. & O’Gara, F. (2006) The posttranscriptional regulator RsmA plays a role in the interaction between Pseudomonas aeruginosa and human airway epithelial cells by positively regulating the type III secretion system. Infection and Immunity, 74(5), 3012-3015. https://doi.org/10.1128/IAI.74.5.3012-3015.2006
Nguyen, Y., Harvey, H., Sugiman-Marangos, S., Bell, S.D., Buensuceso, R.N.C., Junop, M.S. et al. (2015) Structural and functional studies of the Pseudomonas aeruginosa minor pilin, PilE. Journal of Biological Chemistry, 290(44), 26856-26865. https://doi.org/10.1074/jbc.M115.683334
O’Toole, G. A., & Kolter, R. (1998). Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Molecular Microbiology, 28(3), 449-461. Available from: http://www.ncbi.nlm.nih.gov/pubmed/9632250
Oh, E., Becker, A.H., Sandikci, A., Huber, D., Chaba, R., Gloge, F. et al. (2011) Selective ribosome profiling reveals the cotranslational chaperone action of trigger factor in vivo. Cell, 147(6), 1295-1308. https://doi.org/10.1016/j.cell.2011.10.044
Overhage, J., Bains, M., Brazas, M.D. & Hancock, R.E.W. (2008) Swarming of Pseudomonas aeruginosa is a complex adaptation leading to increased production of virulence factors and antibiotic resistance. Journal of Bacteriology, 190(8), 2671-2679. https://doi.org/10.1128/JB.01659-07
Paul, K., Nieto, V., Carlquist, W.C., Blair, D.F. & Harshey, R.M. (2010) The c-di-GMP binding protein YcgR controls flagellar motor direction and speed to affect chemotaxis by a “backstop brake” mechanism. Molecular Cell, 38(1), 128-139. https://doi.org/10.1016/j.molcel.2010.03.001
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(24), 7563-7568. https://doi.org/10.1073/pnas.1502025112
Pratt, J.T., Tamayo, R., Tischler, A.D. & Camilli, A. (2007) PilZ domain proteins bind cyclic diguanylate and regulate diverse processes in vibrio cholerae. Journal of Biological Chemistry, 282(17), 12860-12870. https://doi.org/10.1074/jbc.M611593200
Revelle, W. (2021). psych: procedures for psychological, psychometric, and personality research. Available from https://cran.r-project.org/package=psych
Richter, A.M., Possling, A., Malysheva, N., Yousef, K.P., Herbst, S., von Kleist, M. et al. (2020) Local c-di-GMP signaling in the control of synthesis of the E. coli biofilm exopolysaccharide pEtN-cellulose. Journal of Molecular Biology, 432(16), 4576-4595. https://doi.org/10.1016/j.jmb.2020.06.006
Rinaldo, S., Giardina, G., Mantoni, F., Paone, A. & Cutruzzolà, F. (2018) Beyond nitrogen metabolism: nitric oxide, cyclic-di-GMP and bacterial biofilms. FEMS Microbiology Letters, 365(6), 1-9. https://doi.org/10.1093/FEMSLE/FNY029
Robinson, M.D., McCarthy, D.J. & Smyth, G.K. (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics, 26(1), 139-140. https://doi.org/10.1093/bioinformatics/btp616
Römling, U., Galperin, M.Y. & Gomelsky, M. (2013) Cyclic di-GMP: the first 25 years of a universal bacterial second messenger. Microbiology and Molecular Biology Reviews, 77(1), 1-52. https://doi.org/10.1128/MMBR.00043-12
Ross, P., Weinhouse, H., Aloni, Y., Michaeli, D., Weinberger-Ohana, P., Mayer, R. et al. (1987) Regulation of cellulose synthesis in acetobacter xylinum by cyclic diguanylic acid. Nature, 325(6101), 279-281. https://doi.org/10.1038/325279a0
Ryan, R.P., Lucey, J., O’Donovan, K., McCarthy, Y., Yang, L., Tolker-Nielsen, T. et al. (2009) HD-GYP domain proteins regulate biofilm formation and virulence in Pseudomonas aeruginosa. Environmental Microbiology, 11(5), 1126-1136. https://doi.org/10.1111/j.1462-2920.2008.01842.x
Ryjenkov, D.A., Simm, R., Römling, U. & Gomelsky, M. (2006) The PilZ domain is a receptor for the second messenger c-di-GMP: the PilZ domain protein YcgR controls motility in enterobacteria. The Journal of Biological Chemistry, 281(41), 30310-30314. https://doi.org/10.1074/jbc.C600179200
Schmidt, A.J., Ryjenkov, D.A. & Gomelsky, M. (2005) The ubiquitous protein domain EAL is a cyclic diguanylate-specific phosphodiesterase: enzymatically active and inactive EAL domains. Journal of Bacteriology, 187(14), 4774-4781. https://doi.org/10.1128/JB.187.14.4774-4781.2005
Shishkin, A.A., Giannoukos, G., Kucukural, A., Ciulla, D., Busby, M., Surka, C. et al. (2015) Simultaneous generation of many RNA-seq libraries in a single reaction. Nature Methods, 12(4), 323-325. https://doi.org/10.1038/nmeth.3313
Simm, R., Morr, M., Kader, A., Nimtz, M. & Römling, U. (2004) GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility. Molecular Microbiology, 53(4), 1123-1134. https://doi.org/10.1111/j.1365-2958.2004.04206.x
Siryaporn, A., Kuchma, S.L., O’Toole, G.A., Gitai, Z. & Ausubel, F.M. (2014) Surface attachment induces Pseudomonas aeruginosa virulence. Proceedings of the National Academy of Sciences of the United States of America, 111(47), 16860-16865. https://doi.org/10.1073/pnas.1415712111
Solano, C., García, B., Latasa, C., Toledo-Arana, A., Zorraquino, V., Valle, J. et al. (2009) Genetic reductionist approach for dissecting individual roles of GGDEF proteins within the c-di-GMP signaling network in salmonella. Proceedings of the National Academy of Sciences of the United States of America, 106(19), 7997-8002. https://doi.org/10.1073/pnas.0812573106
Spangler, C., Böhm, A., Jenal, U., Seifert, R. & Kaever, V. (2010) A liquid chromatography-coupled tandem mass spectrometry method for quantitation of cyclic di-guanosine monophosphate. Journal of Microbiological Methods, 81(3), 226-231. https://doi.org/10.1016/j.mimet.2010.03.020
Sudarsan, N., Lee, E.R., Weinberg, Z., Moy, R.H., Kim, J.N., Link, K.H. et al. (2008) Riboswitches in eubacteria sense the second messenger cyclic di-GMP. Science, 321(5887), 411-413. https://doi.org/10.1126/science.1159519
Valentini, M. & Filloux, A. (2016) Biofilms and cyclic di-GMP (c-di-GMP) signaling: lessons from Pseudomonas aeruginosa and other bacteria. Journal of Biological Chemistry, 291(24), 12547-12555. https://doi.org/10.1074/jbc.R115.711507
Van Alst, N.E., Picardo, K.F., Iglewski, B.H. & Haidaris, C.G. (2007) Nitrate sensing and metabolism modulate motility, biofilm formation, and virulence in Pseudomonas aeruginosa. Infection and Immunity, 75(8), 3780-3790. https://doi.org/10.1128/IAI.00201-07
Vizcaíno, J.A., Csordas, A., del-Toro, N., Dianes, J.A., Griss, J., Lavidas, I. et al. (2016) 2016 update of the PRIDE database and its related tools. Nucleic Acids Research, 44(D1), D447-D456. https://doi.org/10.1093/nar/gkv1145
Whitchurch, C.B., Alm, R.A. & Mattick, J.S. (1996) The alginate regulator AlgR and an associated sensor FimS are required for twitching motility in Pseudomonas aeruginosa. Proceedings of the National Academy of Sciences of the United States of America, 93(18), 9839-9843. https://doi.org/10.1073/pnas.93.18.9839
Winsor, G.L., Lo, R., Ho Sui, S.J., Ung, K.S., Huang, S., Cheng, D. et al. (2005) Pseudomonas aeruginosa genome database and PseudoCAP: facilitating community-based, continually updated, genome annotation. Nucleic Acids Research, 33, D338-D343. https://doi.org/10.1093/nar/gki047
Yahr, T.L. & Wolfgang, M.C. (2006) Transcriptional regulation of the Pseudomonas aeruginosa type III secretion system. Molecular Microbiology, 62, 631-640. https://doi.org/10.1111/j.1365-2958.2006.05412.x
Yu, H., Mudd, M., Boucher, J.C., Schurr, M.J. & Deretic, V. (1997) Identification of the algZ gene upstream of the response regulator algR and its participation in control of alginate production in Pseudomonas aeruginosa. Journal of Bacteriology, 179(1), 187-193. https://doi.org/10.1128/jb.179.1.187-193.1997
Zorraquino, V., García, B., Latasa, C., Echeverz, M., Toledo-Arana, A., Valle, J. et al. (2013) Coordinated cyclic-di-GMP repression of salmonella motility through YcgR and cellulose. Journal of Bacteriology, 195(3), 417-428. https://doi.org/10.1128/JB.01789-12