Becoming settlers: Elements and mechanisms for surface colonization by Pseudomonas putida.


Journal

Environmental microbiology
ISSN: 1462-2920
Titre abrégé: Environ Microbiol
Pays: England
ID NLM: 100883692

Informations de publication

Date de publication:
09 2023
Historique:
received: 13 01 2023
accepted: 31 03 2023
medline: 4 9 2023
pubmed: 13 4 2023
entrez: 12 4 2023
Statut: ppublish

Résumé

Pseudomonads are considered to be among the most widespread culturable bacteria in mesophilic environments. The evolutive success of Pseudomonas species can be attributed to their metabolic versatility, in combination with a set of additional functions that enhance their ability to colonize different niches. These include the production of secondary metabolites involved in iron acquisition or having a detrimental effect on potential competitors, different types of motility, and the capacity to establish and persist within biofilms. Although biofilm formation has been extensively studied using the opportunistic pathogen Pseudomonas aeruginosa as a model organism, a significant body of knowledge is also becoming available for non-pathogenic Pseudomonas. In this review, we focus on the mechanisms that allow Pseudomonas putida to colonize biotic and abiotic surfaces and adapt to sessile life, as a relevant persistence strategy in the environment. This species is of particular interest because it includes plant-beneficial strains, in which colonization of plant surfaces may be relevant, and strains used for environmental and biotechnological applications, where the design and functionality of biofilm-based bioreactors, for example, also have to take into account the efficiency of bacterial colonization of solid surfaces. This work reviews the current knowledge of mechanistic and regulatory aspects of biofilm formation by P. putida and pinpoints the prospects in this field.

Identifiants

pubmed: 37045787
doi: 10.1111/1462-2920.16385
doi:

Types de publication

Journal Article Review Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1575-1593

Informations de copyright

© 2023 The Authors. Environmental Microbiology published by Applied Microbiology International and John Wiley & Sons Ltd.

Références

Ainelo, H., Lahesaare, A., Teppo, A., Kivisaar, M. & Teras, R. (2017) The promoter region of lapA and its transcriptional regulation by Fis in Pseudomonas putida. PLoS One, 12, e0185482.
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, 2190-2200.
Amador, C.I., Canosa, I., Govantes, F. & Santero, E. (2010) Lack of CbrB in Pseudomonas putida affects not only amino acids metabolism but also different stress responses and biofilm development. Environmental Microbiology, 12, 1748-1761.
Arrizubieta, M.J., Toledo-Arana, A., Amorena, B., Penadés, J.R. & Lasa, I. (2004) Calcium inhibits bap-dependent multicellular behavior in Staphylococcus aureus. Journal of Bacteriology, 186, 7490-7498.
Barrientos-Moreno, L. & Espinosa-Urgel, M. (2018) Biofilm stress responses associated to aromatic hydrocarbons. In: Krell, T. (Ed.) Cellular ecophysiology of microbe: hydrocarbon and lipid interactions. Handbook of hydrocarbon and lipid microbiology. Cham: Springer, pp. 105-115.
Barrientos-Moreno, L., Molina-Henares, M.A., Pastor-García, M., Ramos-González, M.I. & Espinosa-Urgel, M. (2019) Arginine biosynthesis modulates pyoverdine production and release in Pseudomonas putida as part of the mechanism of adaptation to oxidative stress. Journal of Bacteriology, 201, e00454-19.
Barrientos-Moreno, L., Molina-Henares, M.A., Ramos-González, M.I. & Espinosa-Urgel, M. (2020) Arginine as an environmental and metabolic cue for cyclic diguanylate signalling and biofilm formation in Pseudomonas putida. Scientific Reports, 10, 13623.
Barrientos-Moreno, L., Molina-Henares, M.A., Ramos-González, M.I. & Espinosa-Urgel, M. (2022) Role of the transcriptional regulator ArgR in the connection between arginine metabolism and c-di-GMP signaling in Pseudomonas putida. Applied and Environmental Microbiology, 88, e0006422.
Bashan, Y. (1986) Alginate beads as synthetic inoculant carriers for slow release of bacteria that affect plant growth. Applied and Environmental Microbiology, 51, 1089-1098.
Benedetti, I., de Lorenzo, V. & Nikel, P.I. (2016) Genetic programming of catalytic Pseudomonas putida biofilms for boosting biodegradation of haloalkanes. Metabolic Engineering, 33, 109-118.
Bernier, S.P., Ha, D.G., Khan, W., Merritt, J.H. & O'Toole, G.A. (2011) Modulation of Pseudomonas aeruginosa surface-associated group behaviors by individual amino acids through c-di-GMP signaling. Research in Microbiology, 162, 680-688.
Blanco-Romero, E., Garrido-Sanz, D., Rivilla, R., Redondo-Nieto, M. & Martín, M. (2020) In silico characterization and phylogenetic distribution of extracellular matrix components in the model rhizobacteria Pseudomonas fluorescens f113 and other pseudomonads. Microorganisms, 8, 1740.
Blanco-Romero, E., Redondo-Nieto, M., Martínez-Granero, F., Garrido-Sanz, D., Ramos-González, M.I., Martín, M. et al. (2018) Genome-wide analysis of the FleQ direct regulon in Pseudomonas fluorescens F113 and Pseudomonas putida KT2440. Scientific Reports, 8, 13145.
Borlee, B.R., Goldman, A.D., Murakami, K., Samudrala, R., Wozniak, D.J. & Parsek, M.R. (2010) Pseudomonas aeruginosa uses a cyclic-di-GMP-regulated adhesin to reinforce the biofilm extracellular matrix. Molecular Microbiology, 75, 827-842.
Boyd, C.D., Smith, T.J., El-Kirat-Chatel, S., Newell, P.D., Dufrêne, Y.F. & O'Toole, G.A. (2014) Structural features of the Pseudomonas fluorescens biofilm adhesin LapA required for LapG-dependent cleavage, biofilm formation, and cell surface localization. Journal of Bacteriology, 196, 2775-2788.
Bridier, A., Piard, J.C., Briandet, R. & Bouchez, T. (2020) Emergence of a synergistic diversity as a response to competition in Pseudomonas putida biofilms. Microbial Ecology, 80, 47-59.
Chang, W.S., van de Mortel, M., Nielsen, L., Nino de Guzman, G., Li, X. & Halverson, L.J. (2007) Alginate production by Pseudomonas putida creates a hydrated microenvironment and contributes to biofilm architecture and stress tolerance under water-limiting conditions. Journal of Bacteriology, 189, 8290-8299.
Choy, W.K., Zhou, L., Syn, C.K., Zhang, L.H. & Swarup, S. (2004) MorA defines a new class of regulators affecting flagellar development and biofilm formation in diverse Pseudomonas species. Journal of Bacteriology, 186, 7221-7228.
Christensen, B.B., Haagensen, J.A., Heydorn, A. & Molin, S. (2002) Metabolic commensalism and competition in a two-species microbial consortium. Applied and Environmental Microbiology, 68, 2495-2502.
Collins, A.J., Pastora, A.B., Smith, T.J. & O'Toole, G.A. (2020) MapA, a second large RTX adhesin conserved across the pseudomonads, contributes to biofilm formation by Pseudomonas fluorescens. Journal of Bacteriology, 202, e00277-20.
Collins, A.J., Smith, T.J., Sondermann, H. & O'Toole, G.A. (2020) From input to output: the lap/c-di-GMP biofilm regulatory circuit. Annual Review of Microbiology, 74, 607-631.
Corral-Lugo, A., De la Torre, J., Matilla, M.A., Fernández, M., Morel, B., Espinosa-Urgel, M. et al. (2016) Assessment of the contribution of chemoreceptor-based signalling to biofilm formation. Environmental Microbiology, 18, 3355-3372.
Costerton, J. (1999) Introduction to biofilm. International Journal of Antimicrobial Agents, 11, 217-221.
Costerton, J.W., Lewandowski, Z., Caldwell, D.E., Korber, D.R. & Lappin-Scott, H.M. (1995) Microbial biofilms. Annual Review of Microbiology, 49, 711-745.
Craven, S.E. & Williams, D.D. (1998) In vitro attachment of Salmonella typhimurium to chicken cecal mucus: effect of cations and pretreatment with Lactobacillus spp. isolated from the intestinal tracts of chickens. Journal of Food Protection, 61, 265-271.
D'Alvise, P.W., Sjøholm, O.R., Yankelevich, T., Jin, Y., Wuertz, S. & Smets, B.F. (2010) TOL plasmid carriage enhances biofilm formation and increases extracellular DNA content in Pseudomonas putida KT2440. FEMS Microbiological Letters, 312, 84-92.
Davey, M.E. & O'Toole, G.A. (2000) Microbial biofilms: from ecology to molecular genetics. Microbiology and Molecular Biology Reviews, 64, 847-867.
de Weger, L.A., van der Vlugt, C.I., Wijfjes, A.H., Bakker, P.A., Schippers, B. & Lugtenberg, B. (1987) Flagella of a plant-growth-stimulating Pseudomonas fluorescens strain are required for colonization of potato roots. Journal of Bacteriology, 169, 2769-2773.
Díaz-Salazar, C., Calero, P., Espinosa-Portero, R., Jiménez-Fernández, A., Wirebrand, L., Velasco-Domínguez, M.G. et al. (2017) The stringent response promotes biofilm dispersal in Pseudomonas putida. Scientific Reports, 7, 18055.
Dueholm, M.S., Søndergaard, M.T., Nilsson, M., Christiansen, G., Stensballe, A., Overgaard, M.T. et al. (2013) Expression of Fap amyloids in Pseudomonas aeruginosa, P. fluorescens, and P. putida results in aggregation and increased biofilm formation. Microbiology, 2, 365-382.
Duque, E., de la Torre, J., Bernal, P., Molina-Henares, M.A., Alaminos, M., Espinosa-Urgel, M. et al. (2013) Identification of reciprocal adhesion genes in pathogenic and non-pathogenic Pseudomonas. Environmental Microbiology, 15, 36-48.
Eilers, K., Kuok Hoong Yam, J., Morton, R., Mei Hui Yong, A., Brizuela, J., Hadjicharalambous, C. et al. (2022) Phenotypic and integrated analysis of a comprehensive Pseudomonas aeruginosa PAO1 library of mutants lacking cyclic-di-GMP-related genes. Frontiers Microbiology, 13, 949597.
Espinosa-Urgel, M., Kolter, R. & Ramos, J.L. (2002) Root colonization by Pseudomonas putida: love at first sight. Microbiology (Reading), 148, 341-343.
Espinosa-Urgel, M., Salido, A. & Ramos, J.L. (2000) Genetic analysis of functions involved in adhesion of Pseudomonas putida to seeds. Journal of Bacteriology, 182, 2363-2369.
Fazli, M., Almblad, H., Rybtke, M.L., Givskov, M., Eberl, L. & Tolker-Nielsen, T. (2014) Regulation of biofilm formation in Pseudomonas and Burkholderia species. Environmental Microbiology, 16, 1961-1981.
Feng, H., Fu, R., Hou, X., Lv, Y., Zhang, N., Liu, Y. et al. (2021) Chemotaxis of beneficial rhizobacteria to root exudates: the first step towards root-microbe rhizosphere interactions. International Journal of Molecular Sciences, 22, 6655.
Fong, J.N.C. & Yildiz, F.H. (2015) Biofilm matrix proteins. Microbiology Spectrum, 3. Available from: https://doi.org/10.1128/microbiolspec.MB-0004-2014
Fraile, S., Briones, M., Revenga-Parra, M., de Lorenzo, V., Lorenzo, E. & Martínez-García, E. (2021) Engineering tropism of Pseudomonas putida toward target surfaces through ectopic display of recombinant nanobodies. ACS Synthetic Biology, 10, 2049-2059.
Fuqua, C. (2010) Passing the baton between laps: adhesion and cohesion in Pseudomonas putida biofilms. Molecular Microbiology, 77, 533-566.
García-Fontana, C., Reyes-Darias, J.A., Muñoz-Martínez, F., Alfonso, C., Morel, B., Ramos, J.L. et al. (2013) High specificity in CheR methyltransferase function: CheR2 of Pseudomonas putida is essential for chemotaxis, whereas CheR1 is involved in biofilm formation. Journal of Biological Chemistry, 288, 18987-18999.
Gazzola, G., Habimana, O., Quinn, L., Casey, E. & Murphy, C.D. (2019) Population dynamics of a dual Pseudomonas putida-Pseudomonas fluorescens biofilm in a capillary bioreactor. Biofouling, 35, 299-307.
Gjermansen, M., Nilsson, M., Yang, L. & Tolker-Nielsen, T. (2010) Characterization of starvation-induced dispersion in Pseudomonas putida biofilms: genetic elements and molecular mechanisms. Molecular Microbiology, 75, 815-826.
Gjermansen, M., Ragas, P., Sternberg, C., Molin, S. & Tolker-Nielsen, T. (2005) Characterization of starvation-induced dispersion in Pseudomonas putida biofilms. Environmental Microbiology, 7, 894-906.
Gjermansen, M., Ragas, P. & Tolker-Nielsen, T. (2006) Proteins with GGDEF and EAL domains regulate Pseudomonas putida biofilm formation and dispersal. FEMS Microbiological Letters, 265, 215-224.
Gumerov, V.M., Ortega, D.R., Adebali, O., Ulrich, L.E. & Zhulin, I.B. (2020) MiST 3.0: an updated microbial signal transduction database with an emphasis on chemosensory systems. Nucleic Acids Research, 48, D459-D464.
Güvener, Z.T. & Harwood, C.S. (2007) Subcellular location characteristics of the Pseudomonas aeruginosa GGDEF protein, WspR, indicate that it produces cyclic-di-GMP in response to growth on surfaces. Molecular Microbiology, 66, 1459-1473.
Hansen, S.K., Haagensen, J.A., Gjermansen, M., Jørgensen, T.M., Tolker-Nielsen, T. & Molin, S. (2007) Characterization of a Pseudomonas putida rough variant evolved in a mixed-species biofilm with Acinetobacter sp. strain C6. Journal of Bacteriology, 189, 4932-4943.
Hansen, S.K., Rainey, P.B., Haagensen, J.A. & Molin, S. (2007) Evolution of species interactions in a biofilm community. Nature, 445, 533-536.
Harber, M.J., Mackenzie, R. & Asscher, A.W. (1983) A rapid bioluminescence method for quantifying bacterial adhesion to polystyrene. Journal of General Microbiology, 129, 621-632.
Heilmann, C., Gerke, C., Perdreau-Remington, F. & Götz, F. (1996) Characterization of Tn917 insertion mutants of Staphylococcus epidermidis affected in biofilm formation. Infection and Immunity, 64, 277-282.
Henrici, A.T. (1933) Studies of freshwater bacteria: I. A direct microscopic technique. Journal of Bacteriology, 25, 277-286.
Hinsa, S.M., Espinosa-Urgel, M., Ramos, J.L. & O'Toole, G.A. (2003) Transition from reversible to irreversible attachment during biofilm formation by Pseudomonas fluorescens WCS365 requires an ABC transporter and a large secreted protein. Molecular Microbiology, 49, 905-918.
Hinsa, S.M. & O'Toole, G.A. (2006) Biofilm formation by Pseudomonas fluorescens WCS365: a role for LapD. Microbiology (Reading), 152, 1375-1383.
Huertas-Rosales, Ó., Ramos-González, M.I. & Espinosa-Urgel, M. (2016) Self-regulation and interplay of Rsm family proteins modulate the lifestyle of Pseudomonas putida. Applied and Environmental Microbiology, 82, 5673-5686.
Huertas-Rosales, Ó., Romero, M., Heeb, S., Espinosa-Urgel, M., Cámara, M. & Ramos-González, M.I. (2017) The pseudomonas putida CsrA/RsmA homologues negatively affect c-di-GMP pools and biofilm formation through the GGDEF/EAL response regulator CfcR. Environmental Microbiology, 19, 3551-3566.
Hueso-Gil, Á., Calles, B. & de Lorenzo, V. (2020) The Wsp intermembrane complex mediates metabolic control of the swim-attach decision of pseudomonas putida. Environmental Microbiology, 22, 3535-3547.
Hueso-Gil, Á., Calles, B., O'Toole, G.A. & de Lorenzo, V. (2020) Gross transcriptomic analysis of Pseudomonas putida for diagnosing environmental shifts. Microbial Biotechnology, 13, 263-273.
Ivanov, I.E., Boyd, C.D., Newell, P.D., Schwartz, M.E., Turnbull, L., Johnson, M.S. et al. (2012) Atomic force and super-resolution microscopy support a role for LapA as a cell-surface biofilm adhesin of Pseudomonas fluorescens. Research in Microbiology, 163, 685-691.
Jenal, U., Reinders, A. & Lori, C. (2017) Cyclic di-GMP: second messenger extraordinaire. Nature Reviews Microbiology, 15, 271-284.
Jiménez-Fernández, A., López-Sánchez, A., Calero, P. & Govantes, F. (2015) The c-di-GMP phosphodiesterase BifA regulates biofilm development in pseudomonas putida. Environmental Microbiology Reports, 7, 78-84.
Jiménez-Fernández, A., López-Sánchez, A., Jiménez-Díaz, L., Navarrete, B., Calero, P., Platero, A.I. et al. (2016) Complex interplay between FleQ, cyclic diguanylate and multiple σ factors coordinately regulates flagellar motility and biofilm development in Pseudomonas putida. PLoS One, 11, e0163142.
Katharios-Lanwermeyer, S., Whitfield, G.B., Howell, P.L. & O'Toole, G.A. (2021) Pseudomonas aeruginosa uses c-di-GMP phosphodiesterases RmcA and MorA to regulate biofilm maintenance. MBio, 12, e03384-20.
Kessler, C., Mhatre, E., Cooper, V. & Kim, W. (2021) Evolutionary divergence of the Wsp signal transduction systems in Beta- and Gammaproteobacteria. Applied and Environmental Microbiology, 87, e0130621.
Kierek, K. & Watnick, P.I. (2003) The Vibrio cholerae O139 O-antigen polysaccharide is essential for Ca2+-dependent biofilm development in sea water. Proceedings of the National Academy of Sciences United States of America, 100, 14357-14362.
Kuchma, S.L., Brothers, K.M., Merritt, J.H., Liberati, N.T., Ausubel, F.M. & O'Toole, G.A. (2007) BifA, a cyclic-Di-GMP phosphodiesterase, inversely regulates biofilm formation and swarming motility by Pseudomonas aeruginosa PA14. Journal of Bacteriology, 189, 8165-8178.
Kuiper, I., Lagendijk, E.L., Pickford, R., Derrick, J.P., Lamers, G.E., Thomas-Oates, J.E. et al. (2004) Characterization of two Pseudomonas putida lipopeptide biosurfactants, putisolvin I and II, which inhibit biofilm formation and break down existing biofilms. Molecular Microbiology, 51, 97-113.
Lahesaare, A., Moor, H., Kivisaar, M. & Teras, R. (2014) Pseudomonas putida Fis binds to the lapF promoter in vitro and represses the expression of LapF. PLoS One, 9, e115901.
Lasa, I. (2006) Towards the identification of the common features of bacterial biofilm development. International Microbiology, 9, 21-28.
Lee, C.K., Vachier, J., de Anda, J., Zhao, K., Baker, A.E., Bennett, R.R. et al. (2020) Social cooperativity of bacteria during reversible surface attachment in young biofilms: a quantitative comparison of Pseudomonas aeruginosa PA14 and PAO1. MBio, 11, e02644-19.
Li, G., Brown, P.J.B., Tang, J.X., Xu, J., Quardokus, E.M., Fuqua, C. et al. (2012) Surface contact stimulates the just-in-time deployment of bacterial adhesins. Molecular Microbiology, 83, 41-51.
Liu, C., Sun, D., Zhu, J., Liu, J. & Liu, W. (2020) The regulation of bacterial biofilm formation by cAMP-CRP: a mini-review. Frontiers Microbiology, 11, 802.
Liu, H., Li, S., Xie, X. & Shi, Q. (2021) Pseudomonas putida actively forms biofilms to protect the population under antibiotic stress. Environmental Pollution, 270, 116261.
Liu, H., Xiao, Y., Nie, H., Huang, Q. & Chen, W. (2017) Influence of (p)ppGpp on biofilm regulation in pseudomonas putida KT2440. Microbiological Research, 204, 1-8.
Liu, H., Yan, H., Xiao, Y., Nie, H., Huang, Q. & Chen, W. (2019) The exopolysaccharide gene cluster pea is transcriptionally controlled by RpoS and repressed by AmrZ in Pseudomonas putida KT2440. Microbiological Research, 218, 1-11.
López-Sánchez, A., Jiménez-Fernández, A., Calero, P., Gallego, L.D. & Govantes, F. (2013) New methods for the isolation and characterization of biofilm-persistent mutants in Pseudomonas putida. Environmental Microbiology Reports, 5, 679-685.
López-Sánchez, A., Leal-Morales, A., Jiménez-Díaz, L., Platero, A.I., Bardallo-Pérez, J., Díaz-Romero, A. et al. (2016) Biofilm formation-defective mutants in pseudomonas putida. FEMS Microbiological Letters, 363, fnw127.
Martínez-Bueno, M.A., Tobes, R., Rey, M. & Ramos, J.L. (2002) Detection of multiple extracytoplasmic function (ECF) sigma factors in the genome of Pseudomonas putida KT2440 and their counterparts in Pseudomonas aeruginosa PA01. Environmental Microbiology, 4, 842-855.
Martínez-Gil, M., Quesada, J.M., Ramos-González, M.I., Soriano, M.I., de Cristóbal, R.E. & Espinosa-Urgel, M. (2013) Interplay between extracellular matrix components of Pseudomonas putida biofilms. Research in Microbiology, 164, 382-389.
Martínez-Gil, M., Ramos-González, M.I. & Espinosa-Urgel, M. (2014) Roles of cyclic di-GMP and the Gac system in transcriptional control of the genes coding for the Pseudomonas putida adhesins LapA and LapF. Journal of Bacteriology, 196, 1484-1495.
Martínez-Gil, M., Romero, D., Kolter, R. & Espinosa-Urgel, M. (2012) Calcium causes multimerization of the large adhesin LapF and modulates biofilm formation by Pseudomonas putida. Journal of Bacteriology, 194, 6782-6789.
Martínez-Gil, M., Yousef-Coronado, F. & Espinosa-Urgel, M. (2010) LapF, the second largest Pseudomonas putida protein, contributes to plant root colonization and determines biofilm architecture. Molecular Microbiology, 77, 549-561.
Matilla, M.A., Espinosa-Urgel, M., Rodriguez-Herva, J.J., Ramos, J.L. & Ramos-González, M.I. (2007) Genomic analysis reveals the major driving forces of bacterial life in the rhizosphere. Genome Biology, 8, R179.
Matilla, M.A., Ramos, J.L., Duque, E., de Dios Alché, J., Espinosa-Urgel, M. & Ramos-González, M.I. (2007) Temperature and pyoverdine-mediated iron acquisition control surface motility of Pseudomonas putida. Environmental Microbiology, 9, 1842-1850.
Matilla, M.A., Travieso, M.L., Ramos, J.L. & Ramos-González, M.I. (2011) Cyclic diguanylate (c-di-GMP) turnover mediated by the sole GGDEF/EAL response regulator in Pseudomonas putida: its role in the rhizosphere and an analysis of its target processes. Environmental Microbiology, 13, 1745-1766.
Meadows, P.S. (1971) The attachment of bacteria to solid surfaces. Archiv für Mikrobiologie, 75, 374-381.
Mendrygal, K.E. & González, J.E. (2000) Environmental regulation of exopolysaccharide production in Sinorhizobium meliloti. Journal of Bacteriology, 182, 599-606.
Mills, E., Petersen, E., Kulasekara, B.R. & Miller, S.I. (2015) A direct screen for c-di-GMP modulators reveals a Salmonella typhimurium periplasmic ʟ-arginine-sensing pathway. Science Signaling, 8, ra57.
Molina, M.A., Godoy, P., Ramos-González, M.I., Muñoz, N., Ramos, J.L. & Espinosa-Urgel, M. (2005) Role of iron and the TonB system in colonization of corn seeds and roots by pseudomonas putida KT2440. Environmental Microbiology, 7, 443-449.
Molina-Henares, M.A., Ramos-González, M.I., Daddaoua, A., Fernández-Escamilla, A.M. & Espinosa-Urgel, M. (2017) FleQ of Pseudomonas putida KT2440 is a multimeric cyclic diguanylate binding protein that differentially regulates expression of biofilm matrix components. Research in Microbiology, 168, 36-45.
Monds, R.D., Newell, P.D., Gross, R.H. & O'Toole, G.A. (2007) Phosphate-dependent modulation of c-di-GMP levels regulates Pseudomonas fluorescens Pf0-1 biofilm formation by controlling secretion of the adhesin LapA. Molecular Microbiology, 63, 656-679.
Monds, R.D., Silby, M.W. & Mahanty, H.K. (2001) Expression of the Pho regulon negatively regulates biofilm formation by Pseudomonas aureofaciens PA147-2. Molecular Microbiology, 42, 415-426.
Navarrete, B., Leal-Morales, A., Serrano-Ron, L., Sarrió, M., Jiménez-Fernández, A., Jiménez-Díaz, L. et al. (2019) Transcriptional organization, regulation and functional analysis of flhF and fleN in pseudomonas putida. PLoS One, 14, e0214166.
Newell, P.D., Boyd, C.D., Sondermann, H. & O'Toole, G.A. (2011) A c-di-GMP effector system controls cell adhesion by inside-out signaling and surface protein cleavage. PLoS Biology, 9, e1000587.
Nie, H., Xiao, Y., He, J., Lium, H., Nie, L., Chen, W. et al. (2020) Phenotypic-genotypic analysis of GGDEF/EAL/HD-GYP domain-encoding genes in Pseudomonas putida. Environmental Microbiology Reports, 12, 38-48.
Nie, H., Xiao, Y., Liu, H., He, J., Chen, W. & Huang, Q. (2017) FleN and FleQ play a synergistic role in regulating lapA and bcs operons in Pseudomonas putida KT2440. Environmental Microbiology Reports, 9, 571-580.
Nie, H., Xiao, Y., Song, M., Wu, N., Peng, Q., Duan, W. et al. (2022) Wsp system oppositely modulates antibacterial activity and biofilm formation via FleQ-FleN complex in Pseudomonas putida. Environmental Microbiology, 24, 1543-1559.
Nielsen, L., Li, X. & Halverson, L.J. (2011) Cell-cell and cell-surface interactions mediated by cellulose and a novel exopolysaccharide contribute to Pseudomonas putida biofilm formation and fitness under water-limiting conditions. Environmental Microbiology, 13, 1342-1356.
Nilsson, M., Chiang, W.C., Fazli, M., Gjermansen, M., Givskov, M. & Tolker-Nielsen, T. (2011) Influence of putative exopolysaccharide genes on Pseudomonas putida KT2440 biofilm stability. Environmental Microbiology, 13, 1357-1369.
O'Neal, L., Baraquet, C., Suo, Z., Dreifus, J.E., Peng, Y., Raivio, T.L. et al. (2022) The Wsp system of Pseudomonas aeruginosa links surface sensing and cell envelope stress. Proceedings of the National Academy of Sciences of the United States of America, 119, e2117633119.
Österberg, S., Åberg, A., Herrera Seitz, M.K., Wolf-Watz, M. & Shingler, V. (2013) Genetic dissection of a motility-associated c-di-GMP signalling protein of Pseudomonas putida. Environmental Microbiology Reports, 5, 556-565.
O'Toole, G.A. & Kolter, R. (1998a) Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Molecular Microbiology, 30, 295-304.
O'Toole, G.A. & Kolter, R. (1998b) Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Molecular Microbiology, 28, 449-461.
Otto, K. & Silhavy, T.J. (2002) Surface sensing and adhesion of Escherichia coli controlled by the Cpx-signaling pathway. Proceedings of the National Academy of Sciences of the United States of America, 99, 2287-2292.
Paiardini, A., Mantoni, F., Giardina, G., Paone, A., Janson, G., Leoni, L. et al. (2018) A novel bacterial L-arginine sensor controlling c-di-GMP levels in Pseudomonas aeruginosa. Proteins, 86, 1088-1096.
Palmer, J., Flint, S. & Brooks, J. (2007) Bacterial cell attachment, the beginning of a biofilm. Journal of Industrial Microbiology and Biotechnology, 34, 577-588.
Phippen, C.W., Mikolajek, H., Schlaefli, H.G., Keevil, C.W., Webb, J.S. & Tews, I. (2014) Formation and dimerization of the phosphodiesterase active site of the Pseudomonas aeruginosa MorA, a bi-functional c-di-GMP regulator. FEBS Letters, 588, 4631-4636.
Pliego, C., Cazorla, F.M., González-Sánchez, M.A., Pérez-Jiménez, R.M., de Vicente, A. & Ramos, C. (2007) Selection for biocontrol bacteria antagonistic toward Rosellinia necatrix by enrichment of competitive avocado root tip colonizers. Research in Microbiology, 158, 463-470.
Pratt, L.A. & Kolter, R. (1998) Genetic analysis of Escherichia coli biofilm formation: roles of flagella, motility, chemotaxis and type I pili. Molecular Microbiology, 30, 285-293.
Puhm, M., Hendrikson, J., Kivisaar, M. & Teras, R. (2022) Pseudomonas putida biofilm depends on the vWFa-domain of LapA in peptides-containing growth medium. International Journal of Molecular Sciences, 23, 5898.
Purtschert-Montenegro, G., Cárcamo-Oyarce, G., Pinto-Carbó, M., Agnoli, K., Bailly, A. & Eberl, L. (2022) Pseudomonas putida mediates bacterial killing, biofilm invasion and biocontrol with a type IVB secretion system. Nature Microbiology, 7, 1547-1557.
Ramos- González, M.I., Travieso, M.L., Soriano, M.I., Matilla, M.A., Huertas-Rosales, O., Barrientos-Moreno, L. et al. (2016) Genetic dissection of the regulatory network associated with high c-di-GMP levels in Pseudomonas putida KT2440. Frontiers in Microbiology, 7, 1093.
Ramos-González, M.I., Campos, M.J. & Ramos, J.L. (2005) Analysis of pseudomonas putida KT2440 gene expression in the maize rhizosphere: in vivo expression technology capture and identification of root activated promoters. Journal of Bacteriology, 187, 4033-4041.
Ramos-González, M.I., Matilla, M.A., Quesada, J.M., Ramos, J.L. & Espinosa-Urgel, M. (2013) Using genomics to unveil bacterial determinants of rhizosphere life style. In: de Bruijn, F.J. (Ed.) Molecular microbial ecology of the rhizosphere, Vol. 1. Hoboken, NJ, USA: John Wiley & Sons Inc., pp. 7-16.
Rodríguez-Herva, J.J., Duque, E., Molina-Henares, M.A., Navarro-Avilés, G., Van Dillewijn, P., De La Torre, J. et al. (2010) Physiological and transcriptomic characterization of a fliA mutant of Pseudomonas putida KT2440. Enviromnmental Microbiology Reports, 2(3), 373-380.
Rouse, S.L., Matthews, S.J. & Dueholm, M.S. (2018) Ecology and biogenesis of functional amyloids in pseudomonas. Journal of Molecular Biology, 430, 3685-3695.
Santamaría-Hernando, S., De Bruyne, L., Höfte, M. & Ramos-González, M.I. (2022) Improvement of fitness and biocontrol properties of Pseudomonas putida via an extracellular heme peroxidase. Microbial Biotechnology, 15, 2652-2666.
Sarand, I., Osterberg, S., Holmqvist, S., Holmfeldt, P., Skärfstad, E., Parales, R.E. et al. (2008) Metabolism-dependent taxis towards (methyl)phenols is coupled through the most abundant of three polar localized Aer-like proteins of Pseudomonas putida. Environmental Microbiology, 10, 1320-1334.
Sarkisova, S., Patrauchan, M.A., Berglund, D., Nivens, D.E. & Franklin, M.J. (2005) Calcium-induced virulence factors associated with the extracellular matrix of mucoid Pseudomonas aeruginosa biofilms. Journal of Bacteriology, 187, 4327-4337.
Sauer, K. & Camper, A.K. (2001) Characterization of phenotypic changes in Pseudomonas putida in response to surface-associated growth. Journal of Bacteriology, 183, 6579-6589.
Sauer, K., Camper, A.K., Ehrlich, G.D., Costerton, J.W. & Davies, D.G. (2002) Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm. Journal of Bacteriology, 184, 1140-1154.
Schmidt, J., Müsken, M., Becker, T., Magnowska, Z., Bertinetti, D., Möller, S. et al. (2011) The Pseudomonas aeruginosa chemotaxis methyltransferase CheR1 impacts on bacterial surface sampling. PLoS One, 6, e18184.
Shamim, S., Rehman, A. & Qazi, M.H. (2014) Swimming, swarming, twitching, and chemotactic responses of Cupriavidus metallidurans CH34 and Pseudomonas putida mt2 in the presence of cadmium. Archives of Environmental Contamination and Toxicology, 66, 407-414.
Spiers, A.J., Kahn, S.G., Bohannon, J., Travisano, M. & Rainey, P.B. (2002) Adaptive divergence in experimental populations of Pseudomonas fluorescens. I. Genetic and phenotypic bases of wrinkly spreader fitness. Genetics, 161, 33-46.
Svenningsen, N.B., Martínez-García, E., Nicolaisen, M.H., de Lorenzo, V. & Nybroe, O. (2018) The biofilm matrix polysaccharides cellulose and alginate both protect Pseudomonas putida mt-2 against reactive oxygen species generated under matric stress and copper exposure. Microbiology (Reading), 164, 883-888.
Tagua, V.G., Molina-Henares, M.A., Travieso, M.L., Nisa-Martínez, R., Quesada, J.M., Espinosa-Urgel, M. et al. (2022) C-di-GMP and biofilm are regulated in Pseudomonas putida by the CfcA/CfcR two-component system in response to salts. Environmental Microbiology, 24, 158-178.
Toutain, C.M., Caizza, N.C., Zegans, M.E. & O'Toole, G.A. (2007) Roles for flagellar stators in biofilm formation by Pseudomonas aeruginosa. Research in Microbiology, 158, 471-477.
Tremaroli, V., Fedi, S., Tamburini, S., Viti, C., Tatti, E., Ceri, H. et al. (2011) A histidine-kinase cheA gene of Pseudomonas pseudoalcaligens KF707 not only has a key role in chemotaxis but also affects biofilm formation and cell metabolism. Biofouling, 27, 33-46.
Vander Wauven, C., Piérard, A., Kley-Raymann, M. & Haas, D. (1984) Pseudomonas aeruginosa mutants affected in anaerobic growth on arginine: evidence for a four-gene cluster encoding the arginine deiminase pathway. Journal of Bacteriology, 16, 928-934.
Wang, J., Ma, W., Wang, Y., Lin, L., Wang, T., Wang, Y. et al. (2018) Deletion of 76 genes relevant to flagella and pili formation to facilitate polyhydroxyalkanoate production in Pseudomonas putida. Applied Microbiology and Biotechnology, 102, 10523-10539.
Webster, S.S., Mathelié-Guinlet, M., Verissimo, A.F., Schultz, D., Viljoen, A., Lee, C.K. et al. (2022) Force-induced changes of PilY1 drive surface sensing by Pseudomonas aeruginosa. MBio, 13, e0375421.
Winsor, G.L., Griffiths, E.J., Lo, R., Dhillon, B.K., Shay, J.A. & Brinkman, F.S. (2016) Enhanced annotations and features for comparing thousands of Pseudomonas genomes in the pseudomonas genome database. Nucleic Acids Research, 44, D646-D653.
Xiao, Y., Chen, H., Nie, L., He, M., Peng, Q., Zhu, W. et al. (2021) Identification of c-di-GMP/FleQ-regulated new target genes, including cyaA, encoding adenylate cyclase, in Pseudomonas putida. mSystems, 6, e00295-21.
Xiao, Y., Liang, Q., He, M., Wu, N., Nie, L., Chen, W. et al. (2022) Second messenger c-di-GMP modulates exopolysaccharide Pea-dependent phenotypes via regulation of eppA expression in Pseudomonas putida. Applied and Environmental Microbiology, 88, e0227021.
Xiao, Y., Liu, H., He, M., Nie, L., Nie, H., Chen, W. et al. (2020) A crosstalk between c-di-GMP and cAMP in regulating transcription of GcsA, a diguanylate cyclase involved in swimming motility in Pseudomonas putida. Environmental Microbiology, 22, 142-157.
Xiao, Y., Nie, H., Liu, H., Chen, W. & Huang, Q. (2016) Expression of the diguanylate cyclase GcbA is regulated by FleQ in response to cyclic di-GMP in Pseudomonas putida KT2440. Environmental Microbiology Reports, 8, 993-1002.
Xiao, Y., Nie, H., Liu, H., Luo, X., Chen, W. & Huang, Q. (2016) C-di-GMP regulates the expression of lapA and bcs operons via FleQ in Pseudomonas putida KT2440. Environmental Microbiology Reports, 8, 659-666.
Yousef-Coronado, F., Soriano, M.I., Yang, L., Molin, S. & Espinosa-Urgel, M. (2011) Selection of hyperadherent mutants in Pseudomonas putida biofilms. Microbiology (Reading), 157, 2257-2265.
Yousef-Coronado, F., Travieso, M.L. & Espinosa-Urgel, M. (2008) Different, overlapping mechanisms for colonization of abiotic and plant surfaces by Pseudomonas putida. FEMS Microbiological Letters, 288, 118-124.
Zhan, H.J., Lee, C.C. & Leigh, J.A. (1991) Induction of the second exopolysaccharide (EPSb) in Rhizobium meliloti SU47 by low phosphate concentrations. Journal of Bacteriology, 173, 7391-7394.
Zhang, L. & Mah, T.F. (2008) Involvement of a novel efflux system in biofilm-specific resistance to antibiotics. Journal of Bacteriology, 190, 4447-4452.
Zheng, Y., Li, Y., Long, H., Zhao, X., Jia, K., Li, J. et al. (2018) bifA regulates biofilm development of Pseudomonas putida MnB1 as a primary response to H2O2 and Mn2. Frontiers in Microbiology, 9, 1490.
Zobell, C.E. & Allen, E.C. (1935) The significance of marine bacteria in the fouling of submerged surfaces. Journal of Bacteriology, 29, 239-251.

Auteurs

Manuel Espinosa-Urgel (M)

Department of Biotechnology and Environmental Protection, Estación Experimental del Zaidín, Granada, Spain.

María Isabel Ramos-González (MI)

Department of Biotechnology and Environmental Protection, Estación Experimental del Zaidín, Granada, Spain.

Articles similaires

Biofilms Candida albicans Quorum Sensing Candida glabrata Menthol
Female Biofilms Animals Lactobacillus Mice

Naturally derived 3-aminoquinuclidine salts as new promising therapeutic agents.

Doris Crnčević, Alma Ramić, Andreja Radman Kastelic et al.
1.00
Humans Microbial Sensitivity Tests Anti-Bacterial Agents Biofilms Quinuclidines
Biofilms Horses Animals Escherichia coli Mesenchymal Stem Cells

Classifications MeSH