In trying to rescue amphibians from a global fungus epidemic, researchers are finding that bacteria may be their best allies.
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Edited by Scott J. Hultgren, Washington University School of Medicine, St. Louis, MO, and approved July 8, 2013 (received for review April 11, 2013)
Abstract
Biofilms represent the predominant mode of microbial growth in the natural environment. Bacillus subtilis is a ubiquitous Gram-positive soil bacterium that functions as an effective plant growth-promoting agent. The biofilm matrix is composed of an exopolysaccharide and an amyloid fiber-forming protein, TasA, and assembles with the aid of a small secreted protein, BslA. Here we show that natively synthesized and secreted BslA forms surface layers around the biofilm. Biophysical analysis demonstrates that BslA can self-assemble at interfaces, forming an elastic film. Molecular function is revealed from analysis of the crystal structure of BslA, which consists of an Ig-type fold with the addition of an unusual, extremely hydrophobic “cap” region. A combination of in vivo biofilm formation and in vitro biophysical analysis demonstrates that the central hydrophobic residues of the cap are essential to allow a hydrophobic, nonwetting biofilm to form as they control the surface activity of the BslA protein. The hydrophobic cap exhibits physiochemical properties remarkably similar to the hydrophobic surface found in fungal hydrophobins; thus, BslA is a structurally defined bacterial hydrophobin. We suggest that biofilms formed by other species of bacteria may have evolved similar mechanisms to provide protection to the resident bacterial community.
Footnotes
↵1L.H., A.O., and F.V.R. contributed equally to this work.
- ↵2To whom correspondence should be addressed. E-mail: n.r.stanleywall{at}dundee.ac.uk.
Author contributions: L.H., A.O., F.V.R., K.M.B., M.P., C.E.M., D.M.F.v.A., and N.R.S.-W. designed research; L.H., A.O., F.V.R., K.M.B., and N.R.S.-W. performed research; L.H., A.O., F.V.R., K.M.B., M.P., and N.R.S.-W. contributed new reagents/analytic tools; L.H., A.O., F.V.R., K.M.B., A.R.P., C.E.M., D.M.F.v.A., and N.R.S.-W. analyzed data; and L.H., F.V.R., C.E.M., D.M.F.v.A., and N.R.S.-W. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Data deposition: Crystallography, atomic coordinates, and structure factors have been deposited in the Protein Data Bank, www.pdb.org (PDB ID code 4bhu).
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1306390110/-/DCSupplemental.
Freely available online through the PNAS open access option.
- Laura Hobleya,1,
- Adam Ostrowskia,1,
- Francesco V. Raoa,1,
- Keith M. Bromleyb,
- Michael Portera,c,
- Alan R. Prescottd,
- Cait E. MacPheeb,
- Daan M. F. van Aaltena,e, and
- Nicola R. Stanley-Walla,2
- aDivision of Molecular Microbiology,
- cCentre for Gene Regulation and Expression,
- dDivision of Cell Signalling and Immunology, and
- eMRC Protein Phosphorylation and Ubiquitylation Unit, College of Life Sciences, University of Dundee, Dundee DD1 5EH, United Kingdom; and
- bJames Clerk Maxwell Building, School of Physics, University of Edinburgh, Edinburgh EH9 3JZ, United Kingdom
Edited by Scott J. Hultgren, Washington University School of Medicine, St. Louis, MO, and approved July 8, 2013 (received for review April 11, 2013)
Abstract
Biofilms represent the predominant mode of microbial growth in the natural environment. Bacillus subtilis is a ubiquitous Gram-positive soil bacterium that functions as an effective plant growth-promoting agent. The biofilm matrix is composed of an exopolysaccharide and an amyloid fiber-forming protein, TasA, and assembles with the aid of a small secreted protein, BslA. Here we show that natively synthesized and secreted BslA forms surface layers around the biofilm. Biophysical analysis demonstrates that BslA can self-assemble at interfaces, forming an elastic film. Molecular function is revealed from analysis of the crystal structure of BslA, which consists of an Ig-type fold with the addition of an unusual, extremely hydrophobic “cap” region. A combination of in vivo biofilm formation and in vitro biophysical analysis demonstrates that the central hydrophobic residues of the cap are essential to allow a hydrophobic, nonwetting biofilm to form as they control the surface activity of the BslA protein. The hydrophobic cap exhibits physiochemical properties remarkably similar to the hydrophobic surface found in fungal hydrophobins; thus, BslA is a structurally defined bacterial hydrophobin. We suggest that biofilms formed by other species of bacteria may have evolved similar mechanisms to provide protection to the resident bacterial community.
- biofilm surface protein
- in situ immunofluorescence
- biofilm hydrophobicity
Footnotes
↵1L.H., A.O., and F.V.R. contributed equally to this work.
- ↵2To whom correspondence should be addressed. E-mail: n.r.stanleywall{at}dundee.ac.uk.
Author contributions: L.H., A.O., F.V.R., K.M.B., M.P., C.E.M., D.M.F.v.A., and N.R.S.-W. designed research; L.H., A.O., F.V.R., K.M.B., and N.R.S.-W. performed research; L.H., A.O., F.V.R., K.M.B., M.P., and N.R.S.-W. contributed new reagents/analytic tools; L.H., A.O., F.V.R., K.M.B., A.R.P., C.E.M., D.M.F.v.A., and N.R.S.-W. analyzed data; and L.H., F.V.R., C.E.M., D.M.F.v.A., and N.R.S.-W. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Data deposition: Crystallography, atomic coordinates, and structure factors have been deposited in the Protein Data Bank, www.pdb.org (PDB ID code 4bhu).
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1306390110/-/DCSupplemental.
Freely available online through the PNAS open access option.
Self-assembling hydrophobin coats biofilm
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