Role of Caulobacter Cell Surface Structures in Colonization of the Air-Liquid Interface
Abstract
In aquatic environments,Caulobacterspp. can be found at the boundary between liquid and air known as the neuston. I report an approach to study temporal features ofCaulobacter crescentuscolonization and pellicle biofilm development at the air-liquid interface and have defined the role of cell surface structures in this process. At this interface,C. crescentusinitially forms a monolayer of cells bearing a surface adhesin known as the holdfast. When excised from the liquid surface, this monolayer strongly adheres to glass. The monolayer subsequently develops into a three-dimensional structure that is highly enriched in clusters of stalked cells known as rosettes. As this pellicle film matures, it becomes more cohesive and less adherent to a glass surface. A mutant strain lacking a flagellum does not efficiently reach the surface, and strains lacking type IV pili exhibit defects in organization of the three-dimensional pellicle. Strains unable to synthesize the holdfast fail to accumulate at the boundary between air and liquid and do not form a pellicle. Phase-contrast images support a model whereby the holdfast functions to trapC. crescentuscells at the air-liquid boundary. Unlike the holdfast, neither the flagellum nor type IV pili are required forC. crescentusto partition to the air-liquid interface. While it is well establishedmore »
- Authors:
-
- Univ. of Chicago, IL (United States); Michigan State Univ., East Lansing, MI (United States)
- Publication Date:
- Research Org.:
- Marine Biological Laboratory, Woods Hole, MA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institutes of Health (NIH)
- OSTI Identifier:
- 1623331
- Grant/Contract Number:
- SC0016127
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Journal of Bacteriology
- Additional Journal Information:
- Journal Volume: 201; Journal Issue: 18; Related Information: Role of Caulobacter Cell Surface Structures in Colonization of the Air-Liquid InterfaceAretha Fiebig, J Bacteriol, 2019Dynamics and Control of Biofilms of the Oligotrophic Bacterium Caulobacter crescentusJ Bacteriol, 2004Holdfast Formation in Motile Swarmer Cells Optimizes Surface Attachment during Caulobacter crescentus DevelopmentJ Bacteriol, 2005Genomic characteristics of Dickeya fangzhongdai isolates from pear and the function of type IV pili in the chromosomeCHEN et al., Journal of Integrative Agriculture, 2020Direct observation of ultrafast plasmonic hot electron transfer in the strong coupling regimeHangyong Shan et al., Light: Science & Applications, 2019Monitoring work well-being, job confidence and care provided by care home staff using a self-report surveyTim Benson et al., BMJ Open Quality, 2019; Journal ID: ISSN 0021-9193
- Publisher:
- American Society for Microbiology
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; 54 ENVIRONMENTAL SCIENCES; Alphaproteobacteria; Caulobacter; biofilm; flagellum; holdfast; neuston pellicle type 4 pilus unipolar polysaccharide
Citation Formats
Fiebig, Aretha. Role of Caulobacter Cell Surface Structures in Colonization of the Air-Liquid Interface. United States: N. p., 2019.
Web. doi:10.1128/JB.00064-19.
Fiebig, Aretha. Role of Caulobacter Cell Surface Structures in Colonization of the Air-Liquid Interface. United States. https://doi.org/10.1128/JB.00064-19
Fiebig, Aretha. Thu .
"Role of Caulobacter Cell Surface Structures in Colonization of the Air-Liquid Interface". United States. https://doi.org/10.1128/JB.00064-19. https://www.osti.gov/servlets/purl/1623331.
@article{osti_1623331,
title = {Role of Caulobacter Cell Surface Structures in Colonization of the Air-Liquid Interface},
author = {Fiebig, Aretha},
abstractNote = {In aquatic environments,Caulobacterspp. can be found at the boundary between liquid and air known as the neuston. I report an approach to study temporal features ofCaulobacter crescentuscolonization and pellicle biofilm development at the air-liquid interface and have defined the role of cell surface structures in this process. At this interface,C. crescentusinitially forms a monolayer of cells bearing a surface adhesin known as the holdfast. When excised from the liquid surface, this monolayer strongly adheres to glass. The monolayer subsequently develops into a three-dimensional structure that is highly enriched in clusters of stalked cells known as rosettes. As this pellicle film matures, it becomes more cohesive and less adherent to a glass surface. A mutant strain lacking a flagellum does not efficiently reach the surface, and strains lacking type IV pili exhibit defects in organization of the three-dimensional pellicle. Strains unable to synthesize the holdfast fail to accumulate at the boundary between air and liquid and do not form a pellicle. Phase-contrast images support a model whereby the holdfast functions to trapC. crescentuscells at the air-liquid boundary. Unlike the holdfast, neither the flagellum nor type IV pili are required forC. crescentusto partition to the air-liquid interface. While it is well established that the holdfast enables adherence to solid surfaces, this study provides evidence that the holdfast has physicochemical properties that allow partitioning of nonmotile mother cells to the air-liquid interface and facilitate colonization of this microenvironment. In aquatic environments, the boundary at the air interface is often highly enriched with nutrients and oxygen. Colonization of this niche likely confers a significant fitness advantage in many cases. This study provides evidence that the cell surface adhesin known as a holdfast enablesCaulobacter crescentusto partition to and colonize the air-liquid interface. Additional surface structures, including the flagellum and type IV pili, are important determinants of colonization and biofilm formation at this boundary. Considering that holdfast-like adhesins are broadly conserved inCaulobacterspp. and other members of the diverse classAlphaproteobacteria, these surface structures may function broadly to facilitate colonization of air-liquid boundaries in a range of ecological contexts, including freshwater, marine, and soil ecosystems},
doi = {10.1128/JB.00064-19},
journal = {Journal of Bacteriology},
number = 18,
volume = 201,
place = {United States},
year = {Thu Aug 22 00:00:00 EDT 2019},
month = {Thu Aug 22 00:00:00 EDT 2019}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 8 works
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Sea surface microlayers: A unified physicochemical and biological perspective of the air–ocean interface
journal, February 2013
- Cunliffe, Michael; Engel, Anja; Frka, Sanja
- Progress in Oceanography, Vol. 109
Microbiology of aquatic surface microlayers
journal, March 2011
- Cunliffe, Michael; Upstill-Goddard, Robert C.; Murrell, J. Colin
- FEMS Microbiology Reviews, Vol. 35, Issue 2
Surface Films: Areas of Water Bodies That Are Often Overlooked
journal, January 2005
- Wotton, Roger S.; Preston, Terence M.
- BioScience, Vol. 55, Issue 2
Bacterial adhesion at the single-cell level
journal, July 2018
- Berne, Cecile; Ellison, Courtney K.; Ducret, Adrien
- Nature Reviews Microbiology, Vol. 16, Issue 10
Microbial Biofilms: from Ecology to Molecular Genetics
journal, December 2000
- Davey, M. E.; O'toole, G. A.
- Microbiology and Molecular Biology Reviews, Vol. 64, Issue 4
Biofilms: an emergent form of bacterial life
journal, August 2016
- Flemming, Hans-Curt; Wingender, Jost; Szewzyk, Ulrich
- Nature Reviews Microbiology, Vol. 14, Issue 9
Films of bacteria at interfaces
journal, September 2017
- Vaccari, Liana; Molaei, Mehdi; Niepa, Tagbo H. R.
- Advances in Colloid and Interface Science, Vol. 247
Gram-negative bacteria can also form pellicles: Floating biofilm in Gram-negative bacteria
journal, May 2014
- Armitano, Joshua; Méjean, Vincent; Jourlin-Castelli, Cécile
- Environmental Microbiology Reports, Vol. 6, Issue 6
The role of extracellular DNA in the establishment, maintenance and perpetuation of bacterial biofilms
journal, October 2013
- Okshevsky, Mira; Meyer, Rikke Louise
- Critical Reviews in Microbiology, Vol. 41, Issue 3
Following the terrestrial tracks of Caulobacter - redefining the ecology of a reputed aquatic oligotroph
journal, August 2018
- Wilhelm, Roland C.
- The ISME Journal, Vol. 12, Issue 12
Cellular Differentiation in Stalked Bacteria
journal, December 1962
- Stove, J. L.; Stanier, R. Y.
- Nature, Vol. 196, Issue 4860
Development of Surface Adhesion in Caulobacter crescentus
journal, March 2004
- Bodenmiller, Diane; Toh, Evelyn; Brun, Yves V.
- Journal of Bacteriology, Vol. 186, Issue 5
Holdfast Formation in Motile Swarmer Cells Optimizes Surface Attachment during Caulobacter crescentus Development
journal, July 2006
- Levi, Assaf; Jenal, Urs
- Journal of Bacteriology, Vol. 188, Issue 14
Surface contact stimulates the just-in-time deployment of bacterial adhesins: Surface stimulation of bacterial adhesins
journal, November 2011
- Li, Guanglai; Brown, Pamela J. B.; Tang, Jay X.
- Molecular Microbiology, Vol. 83, Issue 1
Dynamics and Control of Biofilms of the Oligotrophic Bacterium Caulobacter crescentus
journal, December 2004
- Entcheva-Dimitrov, P.; Spormann, A. M.
- Journal of Bacteriology, Vol. 186, Issue 24
Identification of Genes Required for Synthesis of the Adhesive Holdfast in Caulobacter crescentus
journal, February 2003
- Smith, Chris S.; Hinz, Aaron; Bodenmiller, Diane
- Journal of Bacteriology, Vol. 185, Issue 4
Characterization of the Caulobacter crescentus Holdfast Polysaccharide Biosynthesis Pathway Reveals Significant Redundancy in the Initiating Glycosyltransferase and Polymerase Steps
journal, August 2008
- Toh, Evelyn; Kurtz, Harry D.; Brun, Yves V.
- Journal of Bacteriology, Vol. 190, Issue 21
A Genome-Wide Analysis of Adhesion in Caulobacter crescentus Identifies New Regulatory and Biosynthetic Components for Holdfast Assembly
journal, February 2019
- Hershey, David M.; Fiebig, Aretha; Crosson, Sean
- mBio, Vol. 10, Issue 1
Composition of the Holdfast Polysaccharide from Caulobacter crescentus
journal, June 2019
- Hershey, David M.; Porfírio, Sara; Black, Ian
- Journal of Bacteriology, Vol. 201, Issue 17
Layered Structure and Complex Mechanochemistry Underlie Strength and Versatility in a Bacterial Adhesive
journal, February 2018
- Hernando-Pérez, Mercedes; Setayeshgar, Sima; Hou, Yifeng
- mBio, Vol. 9, Issue 1
Genome-scale fitness profile of Caulobacter crescentus grown in natural freshwater
journal, October 2018
- Hentchel, Kristy L.; Reyes Ruiz, Leila M.; Curtis, Patrick D.
- The ISME Journal, Vol. 13, Issue 2
Insight into the microbial multicellular lifestyle via flow-cell technology and confocal microscopy
journal, February 2009
- Pamp, Sünje Johanna; Sternberg, Claus; Tolker-Nielsen, Tim
- Cytometry Part A, Vol. 75A, Issue 2
A Cell Cycle and Nutritional Checkpoint Controlling Bacterial Surface Adhesion
journal, January 2014
- Fiebig, Aretha; Herrou, Julien; Fumeaux, Coralie
- PLoS Genetics, Vol. 10, Issue 1
Type IV Pilin Proteins: Versatile Molecular Modules
journal, November 2012
- Giltner, Carmen L.; Nguyen, Ylan; Burrows, Lori L.
- Microbiology and Molecular Biology Reviews, Vol. 76, Issue 4
The flagellum in bacterial pathogens: For motility and a whole lot more
journal, October 2015
- Chaban, Bonnie; Hughes, H. Velocity; Beeby, Morgan
- Seminars in Cell & Developmental Biology, Vol. 46
Vibrio biofilms: so much the same yet so different
journal, March 2009
- Yildiz, Fitnat H.; Visick, Karen L.
- Trends in Microbiology, Vol. 17, Issue 3
Second messenger–mediated tactile response by a bacterial rotary motor
journal, October 2017
- Hug, Isabelle; Deshpande, Siddharth; Sprecher, Kathrin S.
- Science, Vol. 358, Issue 6362
Obstruction of pilus retraction stimulates bacterial surface sensing
journal, October 2017
- Ellison, Courtney K.; Kan, Jingbo; Dillard, Rebecca S.
- Science, Vol. 358, Issue 6362
Feedback regulation of Caulobacter crescentus holdfast synthesis by flagellum assembly via the holdfast inhibitor HfiA: Caulobacter holdfast regulation by flagellum assembly
journal, October 2018
- Berne, Cécile; Ellison, Courtney K.; Agarwal, Radhika
- Molecular Microbiology, Vol. 110, Issue 2
Flagellar Mutants Have Reduced Pilus Synthesis in Caulobacter crescentus
journal, March 2019
- Ellison, Courtney K.; Rusch, Douglas B.; Brun, Yves V.
- Journal of Bacteriology, Vol. 201, Issue 18
Synchronization of Caulobacter Crescentus for Investigation of the Bacterial Cell Cycle
journal, January 2015
- Schrader, Jared M.; Shapiro, Lucy
- Journal of Visualized Experiments, Issue 98
Cell cycle constraints on capsulation and bacteriophage susceptibility
journal, November 2014
- Ardissone, Silvia; Fumeaux, Coralie; Bergé, Matthieu
- eLife, Vol. 3
Negative staining of freshwater bacterioneuston sampled directly with electron microscope specimen support grids
journal, May 1987
- Fuerst, J. A.; McGregor, A.; Dickson, M. R.
- Microbial Ecology, Vol. 13, Issue 3
Adhesion of single bacterial cells in the micronewton range
journal, April 2006
- Tsang, P. H.; Li, G.; Brun, Y. V.
- Proceedings of the National Academy of Sciences, Vol. 103, Issue 15
Motility, Chemotaxis and Aerotaxis Contribute to Competitiveness during Bacterial Pellicle Biofilm Development
journal, November 2015
- Hölscher, Theresa; Bartels, Benjamin; Lin, Yu-Cheng
- Journal of Molecular Biology, Vol. 427, Issue 23
Aerotaxis governs floating biofilm formation in Shewanella oneidensis: Aerotaxis and pellicle formation in S. oneidensis
journal, June 2013
- Armitano, Joshua; Méjean, Vincent; Jourlin-Castelli, Cécile
- Environmental Microbiology
Involvement of Flagella-Driven Motility and Pili in Pseudomonas aeruginosa Colonization at the Air-Liquid Interface
journal, January 2012
- Yamamoto, Kyosuke; Arai, Hiroyuki; Ishii, Masaharu
- Microbes and Environments, Vol. 27, Issue 3
Identification of genes essential for pellicle formation in Acinetobacter baumannii
journal, June 2015
- Giles, Sarah K.; Stroeher, Uwe H.; Eijkelkamp, Bart A.
- BMC Microbiology, Vol. 15, Issue 1
The Aerotactic Response of Caulobacter crescentus
journal, May 2016
- Morse, Michael; Colin, Remy; Wilson, Laurence G.
- Biophysical Journal, Vol. 110, Issue 9
Conserved modular design of an oxygen sensory/signaling network with species-specific output
journal, May 2005
- Crosson, S.; McGrath, P. T.; Stephens, C.
- Proceedings of the National Academy of Sciences, Vol. 102, Issue 22
Cell surface hydrophobicity and the orientation of certain bacteria at interfaces
journal, January 1973
- Marshall, K. C.; Cruickshank, R. H.
- Archiv f�r Mikrobiologie, Vol. 91, Issue 1
The hydrophobicity of bacteria ? An important factor in their initial adhesion at the air-water inteface
journal, January 1981
- Dahlb�ck, Bj�rn; Hermansson, Malte; Kjelleberg, Staffan
- Archives of Microbiology, Vol. 128, Issue 3
Molecular Adsorption Steers Bacterial Swimming at the Air/Water Interface
journal, July 2013
- Morse, Michael; Huang, Athena; Li, Guanglai
- Biophysical Journal, Vol. 105, Issue 1
Holdfast spreading and thickening during Caulobacter crescentus attachment to surfaces
journal, January 2013
- Li, Guanglai; Brun, Yves V.; Tang, Jay X.
- BMC Microbiology, Vol. 13, Issue 1
Sequential regulation of developmental events during polar morphogenesis in Caulobacter crescentus: assembly of pili on swarmer cells requires cell separation.
journal, January 1988
- Sommer, J. M.; Newton, A.
- Journal of Bacteriology, Vol. 170, Issue 1
Molecular Motors Govern Liquidlike Ordering and Fusion Dynamics of Bacterial Colonies
journal, September 2018
- Welker, Anton; Cronenberg, Tom; Zöllner, Robert
- Physical Review Letters, Vol. 121, Issue 11
Pili-Induced Clustering of N. gonorrhoeae Bacteria
journal, September 2015
- Taktikos, Johannes; Lin, Yen Ting; Stark, Holger
- PLOS ONE, Vol. 10, Issue 9
Dynamics of Neisseria gonorrhoeae Attachment: Microcolony Development, Cortical Plaque Formation, and Cytoprotection
journal, August 2007
- Higashi, Dustin L.; Lee, Shaun W.; Snyder, Aurelie
- Infection and Immunity, Vol. 75, Issue 10
Characterization of the holdfast region of wild-type cells and holdfast mutants of Asticcacaulis biprosthecum
journal, January 1978
- Umbreit, Thomas H.; Pate, Jack L.
- Archives of Microbiology, Vol. 118, Issue 2
How Bacteria Use Type IV Pili Machinery on Surfaces
journal, December 2015
- Maier, Berenike; Wong, Gerard C. L.
- Trends in Microbiology, Vol. 23, Issue 12
The curved shape of Caulobacter crescentus enhances surface colonization in flow
journal, May 2014
- Persat, Alexandre; Stone, Howard A.; Gitai, Zemer
- Nature Communications, Vol. 5, Issue 1
Function and Regulation of Agrobacterium tumefaciens Cell Surface Structures that Promote Attachment
book, January 2018
- Thompson, Melene A.; Onyeziri, Maureen C.; Fuqua, Clay
- Current Topics in Microbiology and Immunology
A bacterial extracellular DNA inhibits settling of motile progeny cells within a biofilm: Biofilm inhibition by extracellular DNA
journal, July 2010
- Berne, Cécile; Kysela, David T.; Brun, Yves V.
- Molecular Microbiology
A Rhizobiales-Specific Unipolar Polysaccharide Adhesin Contributes to Rhodopseudomonas palustris Biofilm Formation across Diverse Photoheterotrophic Conditions
journal, December 2016
- Fritts, Ryan K.; LaSarre, Breah; Stoner, Ari M.
- Applied and Environmental Microbiology, Vol. 83, Issue 4
Short-Stalked Prosthecomicrobium hirschii Cells Have a Caulobacter-Like Cell Cycle
journal, February 2016
- Williams, Michelle; Hoffman, Michelle D.; Daniel, Jeremy J.
- Journal of Bacteriology, Vol. 198, Issue 7
A novel polar surface polysaccharide from Rhizobium leguminosarum binds host plant lectin
journal, March 2006
- Laus, Marc C.; Logman, Trudy J.; Lamers, Gerda E.
- Molecular Microbiology, Vol. 59, Issue 6
Glucomannan-Mediated Attachment of Rhizobium leguminosarum to Pea Root Hairs Is Required for Competitive Nodule Infection
journal, April 2008
- Williams, Alan; Wilkinson, Adam; Krehenbrink, Martin
- Journal of Bacteriology, Vol. 190, Issue 13
A Plant Arabinogalactan-Like Glycoprotein Promotes a Novel Type of Polar Surface Attachment by Rhizobium leguminosarum
journal, February 2012
- Xie, Fang; Williams, Alan; Edwards, Anne
- Molecular Plant-Microbe Interactions, Vol. 25, Issue 2
Mechanisms and regulation of polar surface attachment in Agrobacterium tumefaciens
journal, December 2009
- Tomlinson, Amelia D.; Fuqua, Clay
- Current Opinion in Microbiology, Vol. 12, Issue 6
Genetic analysis of Agrobacterium tumefaciens unipolar polysaccharide production reveals complex integrated control of the motile-to-sessile switch: Agrobacterium tumefaciens unipolar polysaccharide control
journal, July 2013
- Xu, Jing; Kim, Jinwoo; Koestler, Benjamin J.
- Molecular Microbiology, Vol. 89, Issue 5
Carbohydrate binding activities of Bradyrhizobium japonicum: unipolar localization of the lectin BJ38 on the bacterial cell surface.
journal, April 1993
- Loh, J. T.; Ho, S. C.; de Feijter, A. W.
- Proceedings of the National Academy of Sciences, Vol. 90, Issue 7
Cyclic Di-GMP Regulates Multiple Cellular Functions in the Symbiotic Alphaproteobacterium Sinorhizobium meliloti
journal, November 2015
- Schäper, Simon; Krol, Elizaveta; Skotnicka, Dorota
- Journal of Bacteriology, Vol. 198, Issue 3
Complete genome sequence of Hirschia baltica type strain (IFAM 1418T)
journal, December 2011
- Chertkov, Olga; Brown, Pamela J. B.; Kysela, David T.
- Standards in Genomic Sciences, Vol. 5, Issue 3
Stalk formation of Brevundimonas and how it compares to Caulobacter crescentus
journal, September 2017
- Curtis, Patrick D.
- PLOS ONE, Vol. 12, Issue 9
Ecology, Inhibitory Activity, and Morphogenesis of a Marine Antagonistic Bacterium Belonging to the Roseobacter Clade
journal, November 2005
- Bruhn, Jesper Bartholin; Nielsen, Kristian Fog; Hjelm, Mette
- Applied and Environmental Microbiology, Vol. 71, Issue 11
Plasmid curing and the loss of grip – The 65-kb replicon of Phaeobacter inhibens DSM 17395 is required for biofilm formation, motility and the colonization of marine algae
journal, March 2015
- Frank, Oliver; Michael, Victoria; Päuker, Orsola
- Systematic and Applied Microbiology, Vol. 38, Issue 2
Morphological Heterogeneity and Attachment of Phaeobacter inhibens
journal, November 2015
- Segev, Einat; Tellez, Adèle; Vlamakis, Hera
- PLOS ONE, Vol. 10, Issue 11
Prosthecate sphingomonads: proposal of Sphingomonas canadensis sp. nov.
journal, March 2013
- Abraham, W. -R.; Estrela, A. B.; Rohde, M.
- INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 63, Issue Pt 9
Coaggregation by the Freshwater Bacterium Sphingomonas natatoria Alters Dual-Species Biofilm Formation
journal, April 2009
- Min, K. R.; Rickard, A. H.
- Applied and Environmental Microbiology, Vol. 75, Issue 12
Phylogenomics and signature proteins for the alpha Proteobacteria and its main groups
journal, January 2007
- Gupta, Radhey S.; Mok, Amy
- BMC Microbiology, Vol. 7, Issue 1
Phosphorus limitation increases attachment in Agrobacterium tumefaciens and reveals a conditional functional redundancy in adhesin biosynthesis
journal, November 2012
- Xu, Jing; Kim, Jinwoo; Danhorn, Thomas
- Research in Microbiology, Vol. 163, Issue 9-10
Complete genome sequence of Caulobacter crescentus
journal, March 2001
- Nierman, W. C.; Feldblyum, T. V.; Laub, M. T.
- Proceedings of the National Academy of Sciences, Vol. 98, Issue 7