Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.

Subscribe

Logo for

Science 328 (5978): 627-629

Copyright © 2010 by the American Association for the Advancement of Science

D-Amino Acids Trigger Biofilm Disassembly

Ilana Kolodkin-Gal,1 Diego Romero,2 Shugeng Cao,3 Jon Clardy,3 Roberto Kolter,2 Richard Losick1,*

Abstract: Bacteria form communities known as biofilms, which disassemble over time. In our studies outlined here, we found that, before biofilm disassembly, Bacillus subtilis produced a factor that prevented biofilm formation and could break down existing biofilms. The factor was shown to be a mixture of D-leucine, D-methionine, D-tyrosine, and D-tryptophan that could act at nanomolar concentrations. D-Amino acid treatment caused the release of amyloid fibers that linked cells in the biofilm together. Mutants able to form biofilms in the presence of D-Amino acids contained alterations in a protein (YqxM) required for the formation and anchoring of the fibers to the cell. D-Amino acids also prevented biofilm formation by Staphylococcus aureus and Pseudomonas aeruginosa. D-amino acids are produced by many bacteria and, thus, may be a widespread signal for biofilm disassembly.

1 Department of Molecular and Cellular Biology, Harvard University, Cambridge, MA 02138, USA.
2 Department of Microbiology and Molecular Genetics, Harvard Medical School, Boston, MA 02115, USA.
3 Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, MA 02115, USA.

* To whom correspondence should be addressed. E-mail: losick{at}mcb.harvard.edu


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Functional Analysis of the Accessory Protein TapA in Bacillus subtilis Amyloid Fiber Assembly.
D. Romero, H. Vlamakis, R. Losick, and R. Kolter (2014)
J. Bacteriol. 196, 1505-1513
   Abstract »    Full Text »    PDF »
Roles of Cyclic Di-GMP and the Gac System in Transcriptional Control of the Genes Coding for the Pseudomonas putida Adhesins LapA and LapF.
M. Martinez-Gil, M. I. Ramos-Gonzalez, and M. Espinosa-Urgel (2014)
J. Bacteriol. 196, 1484-1495
   Abstract »    Full Text »    PDF »
Streptococcus pneumoniae detects and responds to foreign bacterial peptide fragments in its environment.
L. J. Hathaway, P. Battig, S. Reber, J. U. Rotzetter, S. Aebi, C. Hauser, M. Heller, A. Kadioglu, and K. Muhlemann (2014)
Open Bio 4, 130224
   Abstract »    Full Text »    PDF »
Conserved Pyridoxal Protein That Regulates Ile and Val Metabolism.
T. Ito, J. Iimori, S. Takayama, A. Moriyama, A. Yamauchi, H. Hemmi, and T. Yoshimura (2013)
J. Bacteriol. 195, 5439-5449
   Abstract »    Full Text »    PDF »
D-Amino Acids Indirectly Inhibit Biofilm Formation in Bacillus subtilis by Interfering with Protein Synthesis.
S. A. Leiman, J. M. May, M. D. Lebar, D. Kahne, R. Kolter, and R. Losick (2013)
J. Bacteriol. 195, 5391-5395
   Abstract »    Full Text »    PDF »
Amino Acid Racemization in Pseudomonas putida KT2440.
A. D. Radkov and L. A. Moe (2013)
J. Bacteriol. 195, 5016-5024
   Abstract »    Full Text »    PDF »
Identification, Purification, and Characterization of a Novel Amino Acid Racemase, Isoleucine 2-Epimerase, from Lactobacillus Species.
Y. Mutaguchi, T. Ohmori, T. Wakamatsu, K. Doi, and T. Ohshima (2013)
J. Bacteriol. 195, 5207-5215
   Abstract »    Full Text »    PDF »
Amino acids in the rhizosphere: From plants to microbes.
L. A. Moe (2013)
Am. J. Botany 100, 1692-1705
   Abstract »    Full Text »    PDF »
Biofilms 2012: New Discoveries and Significant Wrinkles in a Dynamic Field.
S. Haussler and C. Fuqua (2013)
J. Bacteriol. 195, 2947-2958
   Abstract »    Full Text »    PDF »
Staphylococcus epidermidis Esp Degrades Specific Proteins Associated with Staphylococcus aureus Biofilm Formation and Host-Pathogen Interaction.
S. Sugimoto, T. Iwamoto, K. Takada, K.-i. Okuda, A. Tajima, T. Iwase, and Y. Mizunoe (2013)
J. Bacteriol. 195, 1645-1655
   Abstract »    Full Text »    PDF »
Staphylococcus aureus Biofilms Promote Horizontal Transfer of Antibiotic Resistance.
V. J. Savage, I. Chopra, and A. J. O'Neill (2013)
Antimicrob. Agents Chemother. 57, 1968-1970
   Abstract »    Full Text »    PDF »
Tryptophan Inhibits Biofilm Formation by Pseudomonas aeruginosa.
K. S. Brandenburg, K. J. Rodriguez, J. F. McAnulty, C. J. Murphy, N. L. Abbott, M. J. Schurr, and C. J. Czuprynski (2013)
Antimicrob. Agents Chemother. 57, 1921-1925
   Abstract »    Full Text »    PDF »
Bacterial Biofilms: Development, Dispersal, and Therapeutic Strategies in the Dawn of the Postantibiotic Era.
M. Kostakioti, M. Hadjifrangiskou, and S. J. Hultgren (2013)
Cold Spring Harb Perspect Med 3, a010306
   Abstract »    Full Text »    PDF »
Extensive Reduction of Cell Viability and Enhanced Matrix Production in Pseudomonas aeruginosa PAO1 Flow Biofilms Treated with a D-Amino Acid Mixture.
Z. Sanchez, A. Tani, and K. Kimbara (2013)
Appl. Envir. Microbiol. 79, 1396-1399
   Abstract »    Full Text »    PDF »
Exposure to a Cutinase-like Serine Esterase Triggers Rapid Lysis of Multiple Mycobacterial Species.
Y. Yang, A. Bhatti, D. Ke, M. Gonzalez-Juarrero, A. Lenaerts, L. Kremer, Y. Guerardel, P. Zhang, and A. K. Ojha (2013)
J. Biol. Chem. 288, 382-392
   Abstract »    Full Text »    PDF »
Functional amyloid formation by Streptococcus mutans.
M. W. Oli, H. N. Otoo, P. J. Crowley, K. P. Heim, M. M. Nascimento, C. B. Ramsook, P. N. Lipke, and L. J. Brady (2012)
Microbiology 158, 2903-2916
   Abstract »    Full Text »    PDF »
Evidence for Cyclic Di-GMP-Mediated Signaling in Bacillus subtilis.
Y. Chen, Y. Chai, J.-h. Guo, and R. Losick (2012)
J. Bacteriol. 194, 5080-5090
   Abstract »    Full Text »    PDF »
Bacterial swimmers that infiltrate and take over the biofilm matrix.
A. Houry, M. Gohar, J. Deschamps, E. Tischenko, S. Aymerich, A. Gruss, and R. Briandet (2012)
PNAS 109, 13088-13093
   Abstract »    Full Text »    PDF »
Fresh Approaches to Anti-Infective Therapies.
C. Nathan (2012)
Science Translational Medicine 4, 140sr2
   Full Text »    PDF »
Microbiota-Targeted Therapies: An Ecological Perspective.
K. P. Lemon, G. C. Armitage, D. A. Relman, and M. A. Fischbach (2012)
Science Translational Medicine 4, 137rv5
   Full Text »    PDF »
Identification of Bacillus subtilis SipW as a Bifunctional Signal Peptidase That Controls Surface-Adhered Biofilm Formation.
R. Terra, N. R. Stanley-Wall, G. Cao, and B. A. Lazazzera (2012)
J. Bacteriol. 194, 2781-2790
   Abstract »    Full Text »    PDF »
Inhibition of Bacterial Biofilm Formation and Swarming Motility by a Small Synthetic Cationic Peptide.
C. de la Fuente-Nunez, V. Korolik, M. Bains, U. Nguyen, E. B. M. Breidenstein, S. Horsman, S. Lewenza, L. Burrows, and R. E. W. Hancock (2012)
Antimicrob. Agents Chemother. 56, 2696-2704
   Abstract »    Full Text »    PDF »
Dimethyl Sulfoxide and Ethanol Elicit Increased Amyloid Biogenesis and Amyloid-Integrated Biofilm Formation in Escherichia coli.
J. Y. Lim, J. M. May, and L. Cegelski (2012)
Appl. Envir. Microbiol. 78, 3369-3378
   Abstract »    Full Text »    PDF »
Small-Molecule Modulators of Listeria monocytogenes Biofilm Development.
U. T. Nguyen, I. B. Wenderska, M. A. Chong, K. Koteva, G. D. Wright, and L. L. Burrows (2012)
Appl. Envir. Microbiol. 78, 1454-1465
   Abstract »    Full Text »    PDF »
Stenotrophomonas maltophilia: an Emerging Global Opportunistic Pathogen.
J. S. Brooke (2012)
Clin. Microbiol. Rev. 25, 2-41
   Abstract »    Full Text »    PDF »
Apple Flavonoid Phloretin Inhibits Escherichia coli O157:H7 Biofilm Formation and Ameliorates Colon Inflammation in Rats.
J.-H. Lee, S. C. Regmi, J.-A. Kim, M. H. Cho, H. Yun, C.-S. Lee, and J. Lee (2011)
Infect. Immun. 79, 4819-4827
   Abstract »    Full Text »    PDF »
Inhibitory Effects of D-Amino Acids on Staphylococcus aureus Biofilm Development.
A. I. Hochbaum, I. Kolodkin-Gal, L. Foulston, R. Kolter, J. Aizenberg, and R. Losick (2011)
J. Bacteriol. 193, 5616-5622
   Abstract »    Full Text »    PDF »
Pharmacokinetics/Pharmacodynamics of Colistin and Imipenem on Mucoid and Nonmucoid Pseudomonas aeruginosa Biofilms.
W. Hengzhuang, H. Wu, O. Ciofu, Z. Song, and N. Hoiby (2011)
Antimicrob. Agents Chemother. 55, 4469-4474
   Abstract »    Full Text »    PDF »
Distinct pathways for modification of the bacterial cell wall by non-canonical D-amino acids.
F. Cava, M. A. de Pedro, H. Lam, B. M. Davis, and M. K. Waldor (2011)
EMBO J. 30, 3442-3453
   Abstract »    Full Text »    PDF »
Screening of Escherichia coli Species Biodiversity Reveals New Biofilm-Associated Antiadhesion Polysaccharides.
O. Rendueles, L. Travier, P. Latour-Lambert, T. Fontaine, J. Magnus, E. Denamur, and J.-M. Ghigo (2011)
mBio 2, e00043-11
   Abstract »    Full Text »    PDF »
Intestine may be a major site of action for the apoA-I mimetic peptide 4F whether administered subcutaneously or orally.
M. Navab, S. T. Reddy, G. M. Anantharamaiah, S. Imaizumi, G. Hough, S. Hama, and A. M. Fogelman (2011)
J. Lipid Res. 52, 1200-1210
   Abstract »    Full Text »    PDF »
Regulation and Characterization of the dadRAX Locus for D-Amino Acid Catabolism in Pseudomonas aeruginosa PAO1.
W. He, C. Li, and C.-D. Lu (2011)
J. Bacteriol. 193, 2107-2115
   Abstract »    Full Text »    PDF »

To Advertise     Find Products


Science Signaling. ISSN 1937-9145 (online), 1945-0877 (print). Pre-2008: Science's STKE. ISSN 1525-8882