Publication Cover
Biofouling
The Journal of Bioadhesion and Biofilm Research
Volume 33, 2017 - Issue 6
372
Views
8
CrossRef citations to date
0
Altmetric
Articles

Adaptation to copper stress influences biofilm formation in Alteromonas macleodii

, , , &
Pages 505-519 | Received 24 Feb 2017, Accepted 09 May 2017, Published online: 12 Jun 2017

References

  • Alice AF, Crosa JH. 2012. The TonB3 system in the human pathogen Vibrio vulnificus is under the control of the global regulators Lrp and cyclic AMP receptor protein. J Bacteriol. 194:1897–1911.10.1128/JB.06614-11
  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local aligment search tool. J Mol Biol. 215:403–410.10.1016/S0022-2836(05)80360-2
  • Belas R. 2014. Biofilms, flagella, and mechanosensing of surfaces by bacteria. Trends Microbiol. 22:517–527.10.1016/j.tim.2014.05.002
  • Bhaskar PV, Bhosle NB. 2006. Bacterial extracellular polymeric substance (EPS): a carrier of heavy metals in the marine food-chain. Environ Int. 32:191–198.10.1016/j.envint.2005.08.010
  • Bidwell JP, Spotte S. 1985. Artificial sea waters: formulas and methods. Boston, (MA): Jones and Bartlett.
  • Biémont C. 2010. A brief history of the status of transposable elements: from junk DNA to major players in evolution. Genetics. 186:1085–1093.10.1534/genetics.110.124180
  • Brinkman AB, Ettema TJG, de Vos WM, van der Oost J. 2003. The Lrp family of transcriptional regulators. Mol Microbiol. 48:287–294.10.1046/j.1365-2958.2003.03442.x
  • Bruland KW, Rue EL, Donat JR, Skrabal SA, Moffett JW. 2000. Intercomparison of voltammetric techniques to determine the chemical speciation of dissolved copper in a coastal seawater sample. Anal Chim Acta. 405:99–113.10.1016/S0003-2670(99)00675-3
  • Chen C-L, Maki JS, Rittschof D, Teo SL-M. 2013. Early marine bacterial biofilms on a copper-based antifouling paint. Int Biodeter Biodegrad. 83:71–76.10.1016/j.ibiod.2013.04.012
  • Chou S-H, Galperin MY. 2016. Diversity of the c-di-GMP binding proteins and mechanisms. J Bacteriol. 198:3–46.
  • Cusick KD, Dale JR, Little BJ, Biffinger JC. 2016. Draft genome sequences of four Alteromonas macleodii strains isolated from copper coupons and grown long-term at elevated copper levels. Genome A. 4:e01311–01316.
  • Dang H, Lovell CR. 2016. Microbial surface colonization and biofilm development in marine environments. Microbiol Mol Biol Rev. 80:91–138.10.1128/MMBR.00037-15
  • Darling AE, Mau B, Perna NT. 2010. ProgressiveMauve: multiple genome alignment with gene gain, loss, and rearrangement. PLoS ONE. 5:e11147.10.1371/journal.pone.0011147
  • Davey MA, O’Toole GA. 2000. Microbial biofilms: from ecology to molecular genetics. Microbiol Mol Biol Rev. 64:847–867.10.1128/MMBR.64.4.847-867.2000
  • Finnie AA. 2006. Improved estimates of environmental copper release rates from antifouling products. Biofouling. 22:279–291.10.1080/08927010600898862
  • Flemming HC, Neu TR, Wozniak DJ. 2007. The EPS matrix: the “House of Biofilm cells”. J Bacteriol. 189:7945–7947.10.1128/JB.00858-07
  • Flynn KM, Dowell G, Johnson TM, Koestler BJ, Waters CM, Cooper VS. 2016. Evolution of ecological diversity in biofilms of Pseudomonas aeruginosa by altered cyclic diguanylate signaling. J Bacteriol. 198:2608–2618.10.1128/JB.00048-16
  • Garcia CA, Alcaraz ES, Franco MA, Passerini de Rossi BN. 2015. Iron is a signal for Stenotrophomonas maltophilia biofilm formation, oxidative stress response, OMPs expression, and virulence. Front Microbiol. 6:926.
  • Gjermansen M, Ragas P, Tolker-Nielsen T. 2006. Proteins with GGDEF and EAL domains regulate Pseudomonas putida biofilm formation and dispersal. FEMS Microbiol Lett. 265:215–224.
  • Graveline R, Garneau P, Martin C, Mourez M, Hancock MA, Lavoie R, Harel J. 2014. Leucine-responsive regulatory protein Lrp and PapI homologues influence phase variation of CS31A fimbriae. J Bacteriol. 196:2944–2953.10.1128/JB.01622-14
  • Hengge R. 2009. Principles of c-di-GMP signalling in bacteria. Nat Rev Microbiol. 7:263–273.10.1038/nrmicro2109
  • Huangyutitham V, Tüzün Güvener Z, Harwood CS. 2013. Subcellular clustering of the phosphorylated WspR response regulator protein stimulates its diguanylate cyclase activity. mBio. 4:e00242-00213.
  • Ivanova EP, Lopez-Perez M, Zabalos M, Nguyen SH, Webb HK, Ryan J, Lagutin K, Vyssotski M, Crawford RJ, Rodriguez-Valera F. 2015. Ecophysiological diversity of a novel member of the genus Alteromonas, and description of Alteromonas mediterranea sp. nov. Antonie Van Leeuwenhoek. 107:119–132.10.1007/s10482-014-0309-y
  • Koressaar T, Remm M. 2007. Enhancements and modifications of primer design program Primer3. Bioinformatics. 23:1289–1291.10.1093/bioinformatics/btm091
  • Kulesekara H, Lee V, Brencic A, Liberati N, Urbach J, Miyata S, Lee DG, Neely AN, Hyodo M, Hayakawa Y, et al. 2006. Analysis of Pseudomonas aeruginosa diguanylate cyclases and phosphodiesterases reveals a role for bis-(3′-5′)-cyclic-GMP in virulence. Proc Nat Acad Sci. 103:2839–2844.10.1073/pnas.0511090103
  • Little B, Wagner P, Angell P, White D. 1996. Correlation between localized anodic areas and Oceanospirillum biofilms on copper. Int Biodeter Biodegrad. 37:159–162.10.1016/S0964-8305(96)00014-5
  • Lopez-Lopez A, Bartual SG, Stal L, Onyshchenko O, Rodriguez-Valera F. 2005. Genetic analysis of housekeeping genes reveals a deep-sea ecotype of Alteromonas macleodii in the Mediterranean Sea. Environ Microbiol. 7:649–659.10.1111/emi.2005.7.issue-5
  • Lopez-Perez M, Gonzaga A, Martin-Cuadrado AB, Onyshchenko O, Ghavidel A, Ghai R, Rodriguez-Valera F 2012. Genomes of surface isolates of Alteromonas macleodii: the life of a widespread marine opportunistic copiotroph. Sci Rep. 2:696.
  • Lopez-Perez M, Gonzaga A, Rodriguez-Valera F. 2013. Genomic diversity of “Deep Ecotype” Alteromonas macleodii isolates: evidence for Pan-Mediterranean clonal frames. Genome Biol Evol. 5:1220–1232.10.1093/gbe/evt089
  • Mittleman MW, Geesey GG. 1985. Copper-binding characteristics of exopolymers from a fresh water-sediment bacterium. Appl Environ Microbiol. 49:846–851.
  • Nakao R, Senpuku H, Watanabe H. 2006. Porphyromonas gingivalis galE is involved in lipopolysaccharide O-antigen synthesis and biofilm formation. Infect Immun. 74:6145–6153.10.1128/IAI.00261-06
  • Nesper J, Lauriano CM, Klose KE, Kapfhammer D, Kraiss A, Reidl J. 2001. Characterization of Vibrio cholerae O1 El tor galU and galE mutants: influence on lipopolysaccharide structure, colonization, and biofilm formation. Infect Immun. 69:435–445.10.1128/IAI.69.1.435-445.2001
  • Newell PD, Yoshioka S, Hvorecny KL, Monds RD, O’Toole GA. 2011. Systematic analysis of diguanylate cyclases that promote biofilm formation by Pseudomonas fluorescens PF0-1. J Bacteriol. 193:4685–4698.10.1128/JB.05483-11
  • O’Toole GA. 2011. A microtiter dish biofilm formation assay. J Vis Exp. 47:2437.
  • Ozaki S, Schalch-Moser A, Zumthor L, Manfredi P, Ebbensgaard A, Schirmer T, Jenal U. 2014. Activation and polar sequestration of PopA, a c-di-GMP effector protein involved in Caulobacter crescentus cell cycle control. Mol Microbiol. 94:580–594.10.1111/mmi.2014.94.issue-3
  • Paul K, Nieto V, Carlquist WC, Blair DF, Harshey RM. 2010. The c-di-GMP binding protein YcgR controls flagellar motor direction and speed to affect chemotaxis by a “backstop brake” mechanism. Mol Cell. 38:128–139.10.1016/j.molcel.2010.03.001
  • Pfaffl MW, Tichopad A, Prgomet C, Neuvians TP. 2004. Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: bestKeeper – Excel-based tool using pair-wise correlations. Biotechnol Lett. 26:509–515.10.1023/B:BILE.0000019559.84305.47
  • Pruss BM, Besernann C, Denton A, Wolfe AJ. 2006. A complex transcription network controls the early stages of biofilm development by Escherichia coli. J Bacteriol. 188:3731–3739.10.1128/JB.01780-05
  • Ramakers C, Ruijter JM, Deprez RHL, Moorman AFM. 2003. Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett. 339:62–66.10.1016/S0304-3940(02)01423-4
  • Ritter A, Com E, Bazire A, Goncalves Mdos S, Delage L, Le Pennec G, Pineau C, Dreanno C, Compere C, Dufour A. 2012. Proteomic studies highlight outer-membrane proteins related to biofilm development in the marine bacterium Pseudoalteromonas sp. D41. Proteomics. 12:3180–3192.10.1002/pmic.v12.21
  • Romling U, Galperin MY, Gomelsky M. 2013. Cyclic di-GMP: the first 25 years of a universal bacterial second messenger. Microbiol Mol Biol Rev. 77:1–52.10.1128/MMBR.00043-12
  • Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, Rajandream MA, Barrell B. 2000. Artemis: sequence visualization and annotation. Bioinformatics. 16:944–945.10.1093/bioinformatics/16.10.944
  • Ryjenkov DA, Tarutina M, Moskvin OV, Gomelsky M. 2005. Cyclic diguanylate is a ubiquitous signaling molecule in bacteria: insights into biochemistry of the GGDEF protein domain. J Bacteriol. 187:1792–1798.10.1128/JB.187.5.1792-1798.2005
  • Schmidt AJ, Ryjenkov DA, Gomelsky M. 2005. The ubiquitous protein domain EAL is a cyclic diguanylate-specific phosphodiesterase: enzymatically active and inactive EAL domains. J Bacteriol. 187:4774–4781.10.1128/JB.187.14.4774-4781.2005
  • Schmittgen TD, Livak KJ. 2008. Analyzing real-time PCR data by the comparative CT method. Nat Prot. 3:1101–1108.10.1038/nprot.2008.73
  • Simm R, Morr M, Kader A, Nimtz M, Romling U. 2004. GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility. Mol Microbiol. Aug; 53:1123–1134.10.1111/j.1365-2958.2004.04206.x
  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. 30:2725–2729.10.1093/molbev/mst197
  • Tang K, Jiao N, Liu K, Zhang Y, Li SW. 2012. Distribution and functions of TonB-dependent transporters in marine bacteria and environments: implications for dissolved organic matter utilization. PLoS ONE. 7:E41204.10.1371/journal.pone.0041204
  • Taylor BL, Zhulin IB, Johnson MS. 1999. Aerotaxis and other energy-sensing behavior in bacteria. Annu Rev Microbiol. 53:103–128.10.1146/annurev.micro.53.1.103
  • Tischler AD, Camilli A. 2004. Cyclic diguanylate (c-di-GMP) regulates Vibrio cholerae biofilm formation. Mol Microbiol. 53:857–869.10.1111/j.1365-2958.2004.04155.x
  • Untergrasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG. 2012. Primer3 – new capabilities and interfaces. Nucleic Acids Res. 40:e115.10.1093/nar/gks596
  • Valentini M, Filloux A. 2016. Biofilms and cyclic di-GMP (c-di-GMP) signaling: lessons from Pseudomonas aeruginosa and other bacteria. J Biol Chem. 291:12547–12555.10.1074/jbc.R115.711507
  • Williams CL, Neu HM, Gilbreath JJ, Michel SLJ, Zurawski DV, Merrell DS. 2016. Copper resistance of the emerging pathogen Acinetobacter baumannii. Appl Environ Microbiol. 82:6174–6188.10.1128/AEM.01813-16
  • Yan Q, Hu X, Wang N. 2012. The novel virulence-related gene nlxA in the lipopolysaccharide cluster of Xanthomonas citri ssp. citri is involved in the production of lipopolysaccharide and extracellular polysaccharide, motility, biofilm formation and stress resistance. Mol Plant Pathol. 13:923–934.10.1111/mpp.2012.13.issue-8
  • Yebra DM, Kiil S, Dam-Johansen K. 2004. Antifouling technology - past, present and future steps towards efficient and environmentally friendly antifouling coatings. Prog Org Coat. 50:75–104.10.1016/j.porgcoat.2003.06.001
  • Zhou J, Fries MR, Sanford RA, Tiedje JM. 1995. Phylogenetic analysis of a new group of denitrifiers capable of anaerobic growth on toluene and description of Azoarcus tolulyticus sp. nov. Int J Syst Bacteriol. 45:500–506.10.1099/00207713-45-3-500
  • Zuker M. 2003. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31:3406–3415.10.1093/nar/gkg595

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.