skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Unintended Laboratory-Driven Evolution Reveals Genetic Requirements for Biofilm Formation by Desulfovibrio vulgaris Hildenborough

Abstract

Biofilms of sulfate-reducing bacteria (SRB) are of particular interest as members of this group are culprits in corrosion of industrial metal and concrete pipelines as well as being key players in subsurface metal cycling. Yet the mechanism of biofilm formation by these bacteria has not been determined. Here in this paper, we show that two supposedly identical wild-type cultures of the SRBDesulfovibrio vulgarisHildenborough maintained in different laboratories have diverged in biofilm formation. From genome resequencing and subsequent mutant analyses, we discovered that a single nucleotide change within DVU1017, the ABC transporter of a type I secretion system (T1SS), was sufficient to eliminate biofilm formation inD. vulgarisHildenborough. Two T1SS cargo proteins were identified as likely biofilm structural proteins, and the presence of at least one (with either being sufficient) was shown to be required for biofilm formation. Antibodies specific to these biofilm structural proteins confirmed that DVU1017, and thus the T1SS, is essential for localization of these adhesion proteins on the cell surface. We propose that DVU1017 is a member of the lapB category of microbial surface proteins because of its phenotypic similarity to the adhesin export system described for biofilm formation in the environmental pseudomonads. These findings have led to themore » identification of two functions required for biofilm formation in D. vulgaris Hildenborough and focus attention on the importance of monitoring laboratory-driven evolution, as phenotypes as fundamental as biofilm formation can be altered. The growth of bacteria attached to a surface (i.e., biofilm), specifically biofilms of sulfate-reducing bacteria, has a profound impact on the economy of developed nations due to steel and concrete corrosion in industrial pipelines and processing facilities. Furthermore, the presence of sulfate-reducing bacteria in oil wells causes oil souring from sulfide production, resulting in product loss, a health hazard to workers, and ultimately abandonment of wells. Identification of the required genes is a critical step for determining the mechanism of biofilm formation by sulfate reducers. Here, the transporter by which putative biofilm structural proteins are exported from sulfate-reducing Desulfovibrio vulgaris Hildenborough cells was discovered, and a single nucleotide change within the gene coding for this transporter was found to be sufficient to completely stop formation of biofilm.« less

Authors:
ORCiD logo [1]; ORCiD logo [1];  [2];  [3];  [4];  [2]; ORCiD logo [5]; ORCiD logo [3];  [1]
  1. Univ. of Missouri, Columbia, MO (United States). Dept. of Biochemistry
  2. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Environmental Genomics and Systems Biology Division
  3. Montana State Univ., Bozeman, MT (United States). Dept. of Microbiology and Immunology; Montana State Univ., Bozeman, MT (United States). Center for Biofilm Engineering
  4. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Environmental Genomics and Systems Biology Division; Univ. of California, Berkeley, CA (United States). Dept. of Bioengineering
  5. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Molecular Biophysics and Integrated Bioimaging Division
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1417607
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
mBio (Online)
Additional Journal Information:
Journal Name: mBio (Online); Journal Volume: 8; Journal Issue: 5; Journal ID: ISSN 2150-7511
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Desulfovibrio vulgaris; biofilms; genetic polymorphisms; secretion systems; sulfate reduction

Citation Formats

De León, Kara B., Zane, Grant M., Trotter, Valentine V., Krantz, Gregory P., Arkin, Adam P., Butland, Gareth P., Walian, Peter J., Fields, Matthew W., and Wall, Judy D. Unintended Laboratory-Driven Evolution Reveals Genetic Requirements for Biofilm Formation by Desulfovibrio vulgaris Hildenborough. United States: N. p., 2017. Web. doi:10.1128/mBio.01696-17.
De León, Kara B., Zane, Grant M., Trotter, Valentine V., Krantz, Gregory P., Arkin, Adam P., Butland, Gareth P., Walian, Peter J., Fields, Matthew W., & Wall, Judy D. Unintended Laboratory-Driven Evolution Reveals Genetic Requirements for Biofilm Formation by Desulfovibrio vulgaris Hildenborough. United States. doi:10.1128/mBio.01696-17.
De León, Kara B., Zane, Grant M., Trotter, Valentine V., Krantz, Gregory P., Arkin, Adam P., Butland, Gareth P., Walian, Peter J., Fields, Matthew W., and Wall, Judy D. Tue . "Unintended Laboratory-Driven Evolution Reveals Genetic Requirements for Biofilm Formation by Desulfovibrio vulgaris Hildenborough". United States. doi:10.1128/mBio.01696-17. https://www.osti.gov/servlets/purl/1417607.
@article{osti_1417607,
title = {Unintended Laboratory-Driven Evolution Reveals Genetic Requirements for Biofilm Formation by Desulfovibrio vulgaris Hildenborough},
author = {De León, Kara B. and Zane, Grant M. and Trotter, Valentine V. and Krantz, Gregory P. and Arkin, Adam P. and Butland, Gareth P. and Walian, Peter J. and Fields, Matthew W. and Wall, Judy D.},
abstractNote = {Biofilms of sulfate-reducing bacteria (SRB) are of particular interest as members of this group are culprits in corrosion of industrial metal and concrete pipelines as well as being key players in subsurface metal cycling. Yet the mechanism of biofilm formation by these bacteria has not been determined. Here in this paper, we show that two supposedly identical wild-type cultures of the SRBDesulfovibrio vulgarisHildenborough maintained in different laboratories have diverged in biofilm formation. From genome resequencing and subsequent mutant analyses, we discovered that a single nucleotide change within DVU1017, the ABC transporter of a type I secretion system (T1SS), was sufficient to eliminate biofilm formation inD. vulgarisHildenborough. Two T1SS cargo proteins were identified as likely biofilm structural proteins, and the presence of at least one (with either being sufficient) was shown to be required for biofilm formation. Antibodies specific to these biofilm structural proteins confirmed that DVU1017, and thus the T1SS, is essential for localization of these adhesion proteins on the cell surface. We propose that DVU1017 is a member of the lapB category of microbial surface proteins because of its phenotypic similarity to the adhesin export system described for biofilm formation in the environmental pseudomonads. These findings have led to the identification of two functions required for biofilm formation in D. vulgaris Hildenborough and focus attention on the importance of monitoring laboratory-driven evolution, as phenotypes as fundamental as biofilm formation can be altered. The growth of bacteria attached to a surface (i.e., biofilm), specifically biofilms of sulfate-reducing bacteria, has a profound impact on the economy of developed nations due to steel and concrete corrosion in industrial pipelines and processing facilities. Furthermore, the presence of sulfate-reducing bacteria in oil wells causes oil souring from sulfide production, resulting in product loss, a health hazard to workers, and ultimately abandonment of wells. Identification of the required genes is a critical step for determining the mechanism of biofilm formation by sulfate reducers. Here, the transporter by which putative biofilm structural proteins are exported from sulfate-reducing Desulfovibrio vulgaris Hildenborough cells was discovered, and a single nucleotide change within the gene coding for this transporter was found to be sufficient to completely stop formation of biofilm.},
doi = {10.1128/mBio.01696-17},
journal = {mBio (Online)},
number = 5,
volume = 8,
place = {United States},
year = {2017},
month = {10}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 2 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Development of a Markerless Genetic Exchange System for Desulfovibrio vulgaris Hildenborough and Its Use in Generating a Strain with Increased Transformation Efficiency
journal, October 2009

  • Keller, K. L.; Bender, K. S.; Wall, J. D.
  • Applied and Environmental Microbiology, Vol. 75, Issue 24, p. 7682-7691
  • DOI: 10.1128/AEM.01839-09

Bioremediation of chromate: thermodynamic analysis of the effects of Cr(VI) on sulfate-reducing bacteria
journal, November 2002

  • B., Chardin; A., Dolla; F., Chaspoul
  • Applied Microbiology and Biotechnology, Vol. 60, Issue 3
  • DOI: 10.1007/s00253-002-1091-8

Systems biology approach to bioremediation
journal, June 2012


Physiologic studies with the sulfate-reducing bacterium Desulfovibrio desulfuricans: Evaluation for use in a biofuel cell
journal, April 1996


Impact of sulphate-reducing bacteria on the performance of engineering materials
journal, July 2011


Comparative transcriptome analysis of Desulfovibrio vulgaris grown in planktonic culture and mature biofilm on a steel surface
journal, June 2007

  • Zhang, Weiwen; Culley, David E.; Nie, Lei
  • Applied Microbiology and Biotechnology, Vol. 76, Issue 2
  • DOI: 10.1007/s00253-007-1014-9

Biofilm formation in Desulfovibrio vulgaris Hildenborough is dependent upon protein filaments
journal, November 2007


Distribution and Evolution of von Willebrand/Integrin A Domains: Widely Dispersed Domains with Roles in Cell Adhesion and Elsewhere
journal, October 2002

  • Whittaker, Charles A.; Hynes, Richard O.
  • Molecular Biology of the Cell, Vol. 13, Issue 10
  • DOI: 10.1091/mbc.E02-05-0259

High-throughput Isolation and Characterization of Untagged Membrane Protein Complexes: Outer Membrane Complexes of Desulfovibrio vulgaris
journal, October 2012

  • Walian, Peter J.; Allen, Simon; Shatsky, Maxim
  • Journal of Proteome Research, Vol. 11, Issue 12
  • DOI: 10.1021/pr300548d

Survey of large protein complexes in D. vulgaris reveals great structural diversity
journal, September 2009

  • Han, B. -G.; Dong, M.; Liu, H.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 39
  • DOI: 10.1073/pnas.0813068106

The genome sequence of the anaerobic, sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough
journal, April 2004

  • Heidelberg, John F.; Seshadri, Rekha; Haveman, Shelley A.
  • Nature Biotechnology, Vol. 22, Issue 5
  • DOI: 10.1038/nbt959

Type I secretion in gram-negative bacteria
journal, November 2004


Scalable web services for the PSIPRED Protein Analysis Workbench
journal, June 2013

  • Buchan, Daniel W. A.; Minneci, Federico; Nugent, Tim C. O.
  • Nucleic Acids Research, Vol. 41, Issue W1
  • DOI: 10.1093/nar/gkt381

Proline-induced Distortions of Transmembrane Helices
journal, November 2002


Characterization of sulfate transport in Desulfovibrio desulfuricans
journal, August 1989


A constant rate of spontaneous mutation in DNA-based microbes.
journal, August 1991


Comparative genome sequencing of Escherichia coli allows observation of bacterial evolution on a laboratory timescale
journal, November 2006

  • Herring, Christopher D.; Raghunathan, Anu; Honisch, Christiane
  • Nature Genetics, Vol. 38, Issue 12
  • DOI: 10.1038/ng1906

Evolution of microbial diversity during prolonged starvation
journal, March 1999

  • Finkel, S. E.; Kolter, R.
  • Proceedings of the National Academy of Sciences, Vol. 96, Issue 7
  • DOI: 10.1073/pnas.96.7.4023

In silico analysis of large microbial surface proteins
journal, July 2007


MicrobesOnline: an integrated portal for comparative and functional genomics
journal, November 2009

  • Dehal, P. S.; Joachimiak, M. P.; Price, M. N.
  • Nucleic Acids Research, Vol. 38, Issue suppl_1, p. D396-D400
  • DOI: 10.1093/nar/gkp919

LapD is a bis-(3',5')-cyclic dimeric GMP-binding protein that regulates surface attachment by Pseudomonas fluorescens Pf0-1
journal, February 2009

  • Newell, P. D.; Monds, R. D.; O'Toole, G. A.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 9
  • DOI: 10.1073/pnas.0808933106

Characterization of starvation-induced dispersion in Pseudomonas putida biofilms: genetic elements and molecular mechanisms
journal, February 2010


A c-di-GMP Effector System Controls Cell Adhesion by Inside-Out Signaling and Surface Protein Cleavage
journal, February 2011


Genetic Analysis of Functions Involved in Adhesion of Pseudomonas putida to Seeds
journal, January 2000


LapF, the second largest Pseudomonas putida protein, contributes to plant root colonization and determines biofilm architecture: Role of LapF in surface colonization by P. putida
journal, June 2010


Identification of a cyclic-di-GMP-modulating response regulator that impacts biofilm formation in a model sulfate reducing bacterium
journal, July 2014


Biofilm growth mode promotes maximum carrying capacity and community stability during product inhibition syntrophy
journal, December 2014

  • Brileya, Kristen A.; Camilleri, Laura B.; Zane, Grant M.
  • Frontiers in Microbiology, Vol. 5
  • DOI: 10.3389/fmicb.2014.00693

Effect of the Deletion of qmoABC and the Promoter-Distal Gene Encoding a Hypothetical Protein on Sulfate Reduction in Desulfovibrio vulgaris Hildenborough
journal, June 2010

  • Zane, G. M.; Yen, H. -c. B.; Wall, J. D.
  • Applied and Environmental Microbiology, Vol. 76, Issue 16
  • DOI: 10.1128/AEM.00691-10

Rex (Encoded by DVU_0916) in Desulfovibrio vulgaris Hildenborough Is a Repressor of Sulfate Adenylyl Transferase and Is Regulated by NADH
journal, October 2014

  • Christensen, G. A.; Zane, G. M.; Kazakov, A. E.
  • Journal of Bacteriology, Vol. 197, Issue 1
  • DOI: 10.1128/JB.02083-14

Overcoming the anaerobic hurdle in phenotypic microarrays: Generation and visualization of growth curve data for Desulfovibrio vulgaris Hildenborough
journal, February 2009

  • Borglin, Sharon; Joyner, Dominique; Jacobsen, Janet
  • Journal of Microbiological Methods, Vol. 76, Issue 2
  • DOI: 10.1016/j.mimet.2008.10.003

Draft Genome Sequence of Pelosinus fermentans JBW45, Isolated during In Situ Stimulation for Cr(VI) Reduction
journal, September 2012

  • Bowen De Leon, K.; Young, M. L.; Camilleri, L. B.
  • Journal of Bacteriology, Vol. 194, Issue 19
  • DOI: 10.1128/JB.01224-12

Fast gapped-read alignment with Bowtie 2
journal, March 2012

  • Langmead, Ben; Salzberg, Steven L.
  • Nature Methods, Vol. 9, Issue 4
  • DOI: 10.1038/nmeth.1923

Harnessing homologous recombination in vitro to generate recombinant DNA via SLIC
journal, February 2007

  • Li, Mamie Z.; Elledge, Stephen J.
  • Nature Methods, Vol. 4, Issue 3
  • DOI: 10.1038/nmeth1010

The Genetic Basis for Bacterial Mercury Methylation
journal, February 2013


Complete genome sequence and comparative analysis of the metabolically versatile Pseudomonas putida KT2440
journal, December 2002