Function of a Chemotaxis-Like Signal Transduction Pathway in Modulating Motility, Cell Clumping, and Cell Length in the Alphaproteobacterium Azospirillum brasilense

Bible, Amber N.; Stephens, Bonnie B.; Ortega, Davi R.; Xie, Zhihong; Alexandre, Gladys

doi:10.1128/jb.00734-08

Cited by 79Bacterial Genetics and BiotechnologyEscherichia coli research studiesLegume Nitrogen Fixing Symbiosis

The DOI matches its Crossref record; 49 of the 49 references it cites were found in a registry or an index.

Function of a Chemotaxis-Like Signal Transduction Pathway in Modulating Motility, Cell Clumping, and Cell Length in the Alphaproteobacterium Azospirillum brasilense

Open access

Bible, Amber N., Stephens, Bonnie B., Ortega, Davi R., Xie, Zhihong, Alexandre, Gladys·2008·Journal of Bacteriology

DOI 10.1128/jb.00734-08PMC PMC2565992

Open this paper in CoChat — free account Open PDF

Abstract

A chemotaxis signal transduction pathway (hereafter called Che1) has been previously identified in the alphaproteobacterium Azospirillum brasilense. Previous experiments have demonstrated that although mutants lacking CheB and/or CheR homologs from this pathway are defective in chemotaxis, a mutant in which the entire chemotaxis pathway has been mutated displayed a chemotaxis phenotype mostly similar to that of the parent strain, suggesting that the primary function of this Che1 pathway is not the control of motility behavior. Here, we report that mutants carrying defined mutations in the cheA1 (strain AB101) and the cheY1 (strain AB102) genes and a newly constructed mutant lacking the entire operon [Delta(cheA1-cheR1)::Cm] (strain AB103) were defective, but not null, for chemotaxis and aerotaxis and had a minor defect in swimming pattern. We found that mutations in genes of the Che1 pathway affected the cell length of actively growing cells but not their growth rate. Cells of a mutant lacking functional cheB1 and cheR1 genes (strain BS104) were significantly longer than wild-type cells, whereas cells of mutants impaired in the cheA1 or cheY1 genes, as well as a mutant lacking a functional Che1 pathway, were significantly shorter than wild-type cells. Both the modest chemotaxis defects and the observed differences in cell length could be complemented by expressing the wild-type genes from a plasmid. In addition, under conditions of high aeration, cells of mutants lacking functional cheA1 or cheY1 genes or the Che1 operon formed clumps due to cell-to-cell aggregation, whereas the mutant lacking functional CheB1 and CheR1 (BS104) clumped poorly, if at all. Further analysis suggested that the nature of the exopolysaccharide produced, rather than the amount, may be involved in this behavior. Interestingly, mutants that displayed clumping behavior (lacking cheA1 or cheY1 genes or the Che1 operon) also flocculated earlier and quantitatively more than the wild-type cells, whereas the mutant lacking both CheB1 and CheR1 was delayed in flocculation. We propose that the Che1 chemotaxis-like pathway modulates the cell length as well as clumping behavior, suggesting a link between these two processes. Our data are consistent with a model in which the function of the Che1 pathway in regulating these cellular functions directly affects flocculation, a cellular differentiation process initiated under conditions of nutritional imbalance.

Integrity signals

Registry

Crossref · 10.1128/jb.00734-08

Cites

49 of 49 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

We couldn’t retrieve this paper’s full text, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Chemotaxis plays a role in the autoaggregation of Azospirillum brasiliense; the Che1 chemotactic signal transduction pathway increases swimming velocity with changes in aeration conditions, and mutants defective in Che1 do not alter their swimming speed and do not detach from early, reversibly formed clumps, leading to formation of larger flocs stabilised by exopolysaccharides.
“Chemotaxis also plays a role in the autoaggregation of Azospirillum brasiliense, a plant-associated soil bacterium [99]. Here, the chemotactic signal transduction pathway Che1 increases swimming velocity with changes in aeration conditions; mutants defective in Che1 do not alter their swimming speed and do not detach from early, reversibly formed clumps. This in turn leads to formation of larger ﬂ”
From Bacterial autoaggregation (2018) · cites this paper as [99]

A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding
Bradford, M. M. (1976) · Analytical Biochemistry · doi:10.1016/0003-2697(76)90527-3 · Cited by 255,302
Molecular Cloning: A Laboratory Manual
Sambrook, J., Fritsch, E., & Maniatis, T. (1989) · UCLA - Biblioteca de Ciencias de la Salud · Cited by 133,589
Colorimetric Method for Determination of Sugars and Related Substances
DuBois, M., Gilles, K. A., Hamilton, J. K., Rebers, P. A., & Smith, F. (1956) · Analytical Chemistry · doi:10.1021/ac60111a017 · Cited by 52,269
Molecular Cloning. A Laboratory Manual
Wood, E. (1983) · Biochemical Education · doi:10.1016/0307-4412(83)90068-7 · Cited by 29,534
Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes
Kovach, M. E., Elzer, P. H., Hill, D. S., Robertson, G. T., Farris, M. A., Roop, R. M., & Peterson, K. M. (1995) · Gene · doi:10.1016/0378-1119(95)00584-1 · Cited by 3,355
Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans
Figurski, D. H., & Helinski, D. R. (1979) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.76.4.1648 · Cited by 3,277
Chemotaxis in Escherichia coli analysed by Three-dimensional Tracking
Berg, H. C., & Brown, D. A. (1972) · Nature · doi:10.1038/239500a0 · Cited by 2,239
Physics of chemoreception
Berg, H. C., & Purcell, E. M. (1977) · Biophysical Journal · doi:10.1016/s0006-3495(77)85544-6 · Cited by 1,758
Improved broad-host-range plasmids for DNA cloning in Gram-negative bacteria
Keen, N. T., Tamaki, S. J., Kobayashi, D., et al. (1988) · Gene · doi:10.1016/0378-1119(88)90117-5 · Cited by 1,509
Making sense of it all: bacterial chemotaxis
Wadhams, G. H., & Armitage, J. P. (2004) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1524 · Cited by 1,480
Histidine kinases and response regulator proteins in two-component signaling systems
West, A. H., & Stock, A. (2001) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(01)01852-7 · Cited by 956
A chemosensory system that regulates biofilm formation through modulation of cyclic diguanylate levels
Hickman, J. W., Tifrea, D. F., & Harwood, C. S. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0507170102 · Cited by 848
Cytokinesis in Bacteria
Errington, J., Daniel, R. A., & Scheffers, D. (2003) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.67.1.52-65.2003 · Cited by 613
Temporal comparisons in bacterial chemotaxis.
Segall, J. E., Block, S. M., & Berg, H. C. (1986) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.83.23.8987 · Cited by 497
Diversity in Chemotaxis Mechanisms among the Bacteria and Archaea
Szurmant, H., & Ordal, G. (2004) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.68.2.301-319.2004 · Cited by 473
Broad-Host-Range cre-lox System for Antibiotic Marker Recycling in Gram-Negative Bacteria
Marx, C. J., & Lidstrom, M. E. (2002) · BioTechniques · doi:10.2144/02335rr01 · Cited by 335
Collaborative signaling by mixed chemoreceptor teams in Escherichia coli
Ames, P., Studdert, C. A., Reiser, R. H., et al. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.092071899 · Cited by 329
"Frizzy" genes of Myxococcus xanthus are involved in control of frequency of reversal of gliding motility.
Blackhart, B. D., & Zusman, D. R. (1985) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.82.24.8767 · Cited by 266
Flocculation in Azospirillum brasilense and Azospirillum lipoferum: exopolysaccharides and cyst formation
Sadasivan, L., & Neyra, C. A. (1985) · Journal of Bacteriology · doi:10.1128/jb.163.2.716-723.1985 · Cited by 204
Histidine and aspartate phosphorylation: two-component systems and the limits of homology
Swanson, R. V., Alex, L. A., & Simon, M. I. (1994) · Trends in Biochemical Sciences · doi:10.1016/0968-0004(94)90135-x · Cited by 185
Attenuation of sensory receptor signaling by covalent modification.
Borkovich, K. A., Alex, L. A., & Simon, M. I. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.15.6756 · Cited by 182
The superfamily of chemotaxis transducers: From physiology to genomics and back
Zhulin, I. B. (2001) · Advances in microbial physiology/Advances in Microbial Physiology · doi:10.1016/s0065-2911(01)45004-1 · Cited by 144
Relation of Capsular Polysaccharide Production and Colonial Cell Organization to Colony Morphology in Vibrio parahaemolyticus
Enos-Berlage, J. L., & McCarter, L. L. (2000) · Journal of Bacteriology · doi:10.1128/jb.182.19.5513-5520.2000 · Cited by 143
Aggregation in Azospirillum brasilense: effects of chemical and physical factors and involvement of extracellular components
Burdman, S., Jurkevitch, É., Schwartsburd, B. I., et al. (1998) · Microbiology · doi:10.1099/00221287-144-7-1989 · Cited by 143
Stable RK2-Derived Cloning Vectors for the Analysis of Gene Expression and Gene Function in Gram-Negative Bacteria
Dombrecht, B., Vanderleyden, J., & Michiels, J. J. (2001) · Molecular Plant-Microbe Interactions · doi:10.1094/mpmi.2001.14.3.426 · Cited by 136
A new set of chemotaxis homologues is essential for Myxococcus xanthus social motility
Yang, Z., Geng, Y., Xu, D., et al. (1998) · Molecular Microbiology · doi:10.1046/j.1365-2958.1998.01160.x · Cited by 136
Oxygen taxis and proton motive force in Azospirillum brasilense
Zhulin, I. B., Bespalov, V. A., Johnson, M. S., & Taylor, B. L. (1996) · Journal of Bacteriology · doi:10.1128/jb.178.17.5199-5204.1996 · Cited by 134
Comparative Genomic and Protein Sequence Analyses of a Complex System Controlling Bacterial Chemotaxis
Wuichet, K., Alexander, R. P., & Zhulin, I. B. (2007) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(06)22001-9 · Cited by 131
Energy Taxis Is the Dominant Behavior in Azospirillum brasilense
Alexandre, G. M., Greer‐Phillips, S. E., & Zhulin, I. B. (2000) · Journal of Bacteriology · doi:10.1128/jb.182.21.6042-6048.2000 · Cited by 130
Self-citation
The major chemotaxis gene cluster of Rhizobium leguminosarum bv. viciae is essential for competitive nodulation
Miller, L. D., Yost, C. K., Hynes, M. F., et al. (2006) · Molecular Microbiology · doi:10.1111/j.1365-2958.2006.05515.x · Cited by 125
Chemosensory regulation of developmental gene expression in Myxococcus xanthus
Kirby, J. R., & Zusman, D. R. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0330944100 · Cited by 121
Arabinose content of extracellular polysaccharide plays a role in cell aggregation of Azospirillum brasilense
Bahat-Samet, E., Castro‐Sowinski, S., & Okon, Y. (2004) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2004.tb09696.x · Cited by 114
Extracellular polysaccharide composition ofAzospirillum brasilenseand its relation with cell aggregation
Burdman, S., Jurkevitch, É., Soria-DÃaz, M. E., et al. (2000) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2000.tb09240.x · Cited by 112
A nutrient uptake role for bacterial cell envelope extensions
Wagner, J. K., Setayeshgar, S., Sharon, L. A., et al. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0602047103 · Cited by 105
A mutant of Azospirillum brasilense Sp7 impaired in flocculation with a modified colonization pattern and superior nitrogen fixation in association with wheat
Katupitiya, S., Millet, J., Vesk, M., et al. (1995) · Applied and Environmental Microbiology · doi:10.1128/aem.61.5.1987-1995.1995 · Cited by 102
Involvement of a Che‐like signal transduction cascade in regulating cyst cell development in Rhodospirillum centenum
Berleman, J. E., & Bauer, C. E. (2005) · Molecular Microbiology · doi:10.1111/j.1365-2958.2005.04646.x · Cited by 100
New Mobilizable Vectors Suitable for Gene Replacement in Gram-Negative Bacteria and Their Use in Mapping of the 3′ End of the Xanthomonas campestris pv. campestris gum Operon
Katzen, F., Becker, A., Ielmini, M. V., et al. (1999) · Applied and Environmental Microbiology · doi:10.1128/aem.65.1.278-282.1999 · Cited by 86
Aerotactic response of Azospirillum brasilense
Barak, R., Nur, I., Okon, Y., et al. (1982) · Journal of Bacteriology · doi:10.1128/jb.152.2.643-649.1982 · Cited by 81
Chemotactic methylation and behavior in Bacillus subtilis: role of two unique proteins, CheC and CheD
Rosario, M. M. L., Kirby, J. R., Bochar, D. A., et al. (1995) · Biochemistry · doi:10.1021/bi00011a040 · Cited by 66
Improved Antibiotic-Resistance Cassettes Through Restriction Site Elimination Using Pfu DNA Polymerase PCR
Dennis, J. J., & Zylstra, G. J. (1998) · BioTechniques · doi:10.2144/98255bm04 · Cited by 61
CheC and CheD interact to regulate methylation of Bacillus subtilis methyl‐accepting chemotaxis proteins
Rosario, M. M. L., & Ordal, G. (1996) · Molecular Microbiology · doi:10.1111/j.1365-2958.1996.tb02560.x · Cited by 60
Chemosensory and photosensory perception in purple photosynthetic bacteria utilize common signal transduction components
Jiang, Z. Y., Gest, H., & Bauer, C. E. (1997) · Journal of Bacteriology · doi:10.1128/jb.179.18.5720-5727.1997 · Cited by 60
A che‐like signal transduction cascade involved in controlling flagella biosynthesis in Rhodospirillum centenum
Berleman, J. E., & Bauer, C. E. (2005) · Molecular Microbiology · doi:10.1111/j.1365-2958.2005.04489.x · Cited by 59
Role of CheB and CheR in the Complex Chemotactic and Aerotactic Pathway of Azospirillum brasilense
Stephens, B. B., Loar, S. N., & Alexandre, G. M. (2006) · Journal of Bacteriology · doi:10.1128/jb.00267-06 · Cited by 53
Self-citation
A major chemotaxis gene cluster inAzospirillum brasilenseand relationships between chemotaxis operons in α-proteobacteria
Hauwaerts, D., Alexandre, G. M., Das, S. K., et al. (2002) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2002.tb11061.x · Cited by 52
Self-citation
A CheW Homologue Is Required for Myxococcus xanthus Fruiting Body Development, Social Gliding Motility, and Fibril Biogenesis
Bellenger, K., Ma, X., Shi, W., et al. (2002) · Journal of Bacteriology · doi:10.1128/jb.184.20.5654-5660.2002 · Cited by 49
Azospirillum brasilense Sp7 produces an outer-membrane lectin that specifically binds to surface-exposed extracellular polysaccharide produced by the bacterium
Mora, P., Rosconi, F., Fraguas, L. F., et al. (2007) · Archives of Microbiology · doi:10.1007/s00203-007-0343-5 · Cited by 47
Regulation of Switching Frequency and Bias of the Bacterial Flagellar Motor by CheY and Fumarate
Montrone, M., Eisenbach, M., Oesterhelt, D., et al. (1998) · Journal of Bacteriology · doi:10.1128/jb.180.13.3375-3380.1998 · Cited by 35
Effect of loss of CheC and other adaptational proteins on chemotactic behaviour in Bacillus subtilis
Saulmon, M. M., Karatan, E., & Ordal, G. (2004) · Microbiology · doi:10.1099/mic.0.26463-0 · Cited by 18

Flagged first, then by citations

Sorted by citations

Bacterial autoaggregation
Trunk, T., Bacterial Cell Surface Group, S. F. G. A. E. B., S. Khalil, H., & C. Leo, J. (2018) · AIMS Microbiology · doi:10.3934/microbiol.2018.1.140 · Cited by 444
“Chemotaxis also plays a role in the autoaggregation of Azospirillum brasiliense, a plant-associated soil bacterium [99].”
Background
Chemotaxis towards autoinducer 2 mediates autoaggregation in Escherichia coli
Laganenka, L., Colin, R., & Sourjik, V. (2016) · Nature Communications · doi:10.1038/ncomms12984 · Cited by 218
The Azospirillum brasilense Che1 Chemotaxis Pathway Controls Swimming Velocity, Which Affects Transient Cell-to-Cell Clumping
Bible, A., Russell, M. H., & Alexandre, G. (2012) · Journal of Bacteriology · doi:10.1128/jb.00310-12 · Cited by 50
Self-citation

Role of CheB and CheR in the Complex Chemotactic and Aerotactic Pathway of Azospirillum brasilense
Stephens, B. B., Loar, S. N., & Alexandre, G. M. (2006) · Journal of Bacteriology · doi:10.1128/jb.00267-06 · Cited by 53
Self-citation
A major chemotaxis gene cluster in Azospirillum brasilense and relationships between chemotaxis operons in α-proteobacteria
Hauwaerts, D. (2002) · FEMS Microbiology Letters · doi:10.1016/s0378-1097(01)00578-x · Cited by 2
Gene inactivation of a chemotaxis operon in the pathogen Leptospira interrogans
Lambert, A., Wong-Ng, J., & Picardeau, M. (2015) · FEMS Microbiology Letters · doi:10.1093/femsle/fnu054 · Cited by 19
Azospirillum brasilense Chemotaxis Depends on Two Signaling Pathways Regulating Distinct Motility Parameters
Mukherjee, T., Kumar, D., Burriss, N., et al. (2016) · Journal of Bacteriology · doi:10.1128/jb.00020-16 · Cited by 43
Functional analysis of a cloned nifA homologous gene of Azospirillum brasilense Yu62
Su, G., Zhao, Y., & Li, J. (1998) · Springer eBooks · doi:10.1007/978-94-011-5232-7_3

Authors: Bible, A. N., Stephens, B. B., Ortega, D. R., Xie, Z., & Alexandre, G.
Affiliations: Department of Biochemistry, Cellular and Molecular Biology
Georgia State University (US)
University of Tennessee at Knoxville (US)
Corresponding author: Alexandre, Gladys
ORCID: Bible, Amber N.
Ortega, Davi R.
Xie, Zhihong
Alexandre, Gladys
Venue: Journal of Bacteriology
Publisher: American Society for Microbiology
Published: 2008-10
Volume: 190
Issue: 19
Pages: 6365-6375
ISSN: 0021-9193 (ISSN-L)
1098-5530
DOI: 10.1128/jb.00734-08
PMC: PMC2565992
OpenAlex: W1991537109
Cited by: 79
References: 49
Citations by year: 2026: 4 · 2025: 2 · 2024: 2 · 2023: 3 · 2022: 2 · 2021: 6 · 2020: 1 · 2019: 3 · 2018: 4 · 2017: 4 · 2016: 4 · 2015: 6 · 2014: 7 · 2013: 5 · 2012: 6
FWCI: 3.80
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: journals.asm.org/non-commercial-tdm-license (tdm)
Locations: Journal of Bacteriology (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Life Sciences › Immunology and Microbiology › Microbiology › Escherichia coli research studies
Life Sciences › Agricultural and Biological Sciences › Plant Science › Legume Nitrogen Fixing Symbiosis
Keywords: Azospirillum brasilense, cell clumping, flocculation, exopolysaccharides, aerotaxis, swimming patterns, CheA, CheY, Cheb, Cher, bacterial motility, gene complementation, Alphaproteobacteria
MeSH terms: Bacterial Proteins, Chemotaxis, Genetic Complementation Test, Models, Genetic, Operon, Signal Transduction, Azospirillum brasilense, Gene Expression Regulation, Bacterial

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Function of a Chemotaxis-Like Signal Transduction Pathway in Modulating Motility, Cell Clumping, and Cell Length in the Alphaproteobacterium Azospirillum brasilense

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Citations

Cites

Cited by

Related

Metadata

Record

About these checks