Infection-Blocking Genes of a Symbiotic Rhizobium leguminosarum Strain That Are Involved in Temperature-Dependent Protein Secretion

M. R. Bladergroen; K. Badelt; H. P. Spaink

doi:10.1094/mpmi.2003.16.1.53

journal article Open Access Jan 01, 2003

Infection-Blocking Genes of a Symbiotic Rhizobium leguminosarum Strain That Are Involved in Temperature-Dependent Protein Secretion

M. R. Bladergroen K. Badelt H. P. Spaink

Molecular Plant-Microbe Interactions® Vol. 16 No. 1 pp. 53-64 · Scientific Societies

View at Publisher Save 10.1094/mpmi.2003.16.1.53

Abstract

Rhizobium leguminosarum strain RBL5523 is able to form nodules on pea, but these nodules are ineffective for nitrogen fixation. The impairment in nitrogen fixation appears to be caused by a defective infection of the host plant and is host specific for pea. A Tn5 mutant of this strain, RBL5787, is able to form effective nodules on pea. We have sequenced a 33-kb region around the phage-transductable Tn5 insertion. The Tn5 insertion was localized to the 10th gene of a putative operon of 14 genes that was called the imp (impaired in nitrogen fixation) locus. Several highly similar gene clusters of unknown function are present in Pseudomonas aeruginosa, Vibrio cholerae, Edwardsiella ictaluri, and several other animal pathogens. Homology studies indicate that several genes of the imp locus are involved in protein phosphorylation, either as a kinase or dephosphorylase, or contain a phosphoprotein-binding module called a forkhead-associated domain. Other proteins show similarity to proteins involved in type III protein secretion. Two dimensional gel electrophoretic analysis of the secreted proteins in the supernatant fluid of cultures of RBL5523 and RBL5787 showed the absence in the mutant strain of at least four proteins with molecular masses of approximately 27 kDa and pIs between 5.5 and 6.5. The production of these proteins in the wild-type strain is temperature dependent. Sequencing of two of these proteins revealed that their first 20 amino acids are identical. This sequence showed homology to that of secreted ribose binding proteins (RbsB) from Bacilus subtilis and V. cholerae. Based on this protein sequence, the corresponding gene encoding a close homologue of RbsB was cloned that contains a N-terminal signal sequence that is recognized by type I secretion systems. Inoculation of RBL5787 on pea plants in the presence of supernatant of RBL5523 caused a reduced ability of RBL5787 to nodulate pea and fix nitrogen. Boiling of this supernatant before inoculation restored the formation of effective nodules to the original values, indicating that secreted proteins are indeed responsible for the impaired phenotype. These data suggest that the imp locus is involved in the secretion to the environment of proteins, including periplasmic RbsB protein, that cause blocking of infection specifically in pea plants.

Topics

No keywords indexed for this article. Browse by subject →

References

40

[1]

10.1577/1548-8667(1992)004<0148:eowtoe>2.3.co;2

[2]

10.1099/00221287-84-1-188

[3]

10.1016/1369-5266(88)80059-1

[4]

10.1007/bf01160385

[5]

10.1016/s0966-842x(00)01792-3

[6]

10.1016/s0966-842x(99)01657-1

[7]

Broad host range DNA cloning system for gram-negative bacteria: construction of a gene bank of Rhizobium meliloti.

G Ditta, S Stanfield, D Corbin et al.

Proceedings of the National Academy of Sciences 10.1073/pnas.77.12.7347

[8]

Francis-Floyd R. J. Am. Vet. Med. Assoc. (1987)

[9]

10.1046/j.1365-2958.1998.01144.x

[10]

10.1002/elps.1150090913

[11]

10.1094/mpmi-2-004

[12]

10.1099/00221287-98-2-477

[13]

10.1038/291351a0

[14]

10.1128/mmbr.62.2.379-433.1998

[15]

10.1073/pnas.170281997

[16]

10.1046/j.1365-2958.2000.01769.x

[17]

10.1128/jb.173.9.2791-2799.1991

[18]

Li J. J. Cell Sci. (2000) 10.1242/jcs.113.23.4143

[19]

10.1146/annurev.ge.23.120189.002411

[20]

10.1016/0378-1119(84)90022-2

[21]

Pollock T. J. J. Bacteriol. (1998) 10.1128/jb.180.3.586-593.1998

[22]

10.1111/j.1574-6968.1984.tb01466.x

[23]

Purcell M. Infect. Immun. (1998) 10.1128/iai.66.5.2245-2255.1998

[24]

10.1128/jb.169.5.2231-2238.1987

[25]

10.1071/pp00107

[26]

10.1023/a:1006054607850

[27]

Roest, H. P. 1995. Symbiotic regulation of Rhizobium leguminosarum outer membrane proteins. Ph.D. thesis, Leiden University, Leiden, The Netherlands.

[28]

10.1094/mpmi.1997.10.7.938

[29]

Sambrook, J., Fritsch, E. F., and Maniatis, T. 1989. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, U.S.A.

[30]

10.1073/pnas.95.4.1669

[31]

10.1146/annurev.micro.54.1.257

[32]

10.1094/mpmi.2000.13.11.1163

[33]

van Brussel A. A. N. Lett. (1982)

[34]

10.1128/jb.181.16.4790-4797.1999

[35]

van Workum, W. A. T., van der Linden, S., Wijfjes, A. H. M., and Kijne, J. W. 1997a. Identification of a novel locus involved in production of exopolysaccharides by Rhizobium leguminosarum. Pages 99-112 in: Biosynthesis and Function of Exopolysaccharides from Rhizobium leguminosarum. Ph.D. thesis, Leiden University, Leiden, The Netherlands.

[36]

10.1094/mpmi.1998.11.12.1233

[37]

10.1046/j.1365-2958.1998.00920.x

[38]

10.1038/83007

[39]

10.1073/pnas.96.11.6456

[40]

10.1007/bf00392802

Cited By

195

Harnessing contact-dependent killing for next-generation agricultural biocontrol solutions

Xiaolong Shao, Yifei Zhang · 2026

Fundamental Research

The role of microbial interactions on rhizobial fitness

Margarita Granada Agudelo, Bryan Ruiz · 2023

Frontiers in Plant Science

Bacterial protein secretion systems: Game of types

Alain Filloux · 2022

Microbiology

Defending against the Type Six Secretion System: beyond Immunity Genes

Steven J. Hersch, Kevin Manera · 2020

Cell Reports

Klebsiella pneumoniae type VI secretion system-mediated microbial competition is PhoPQ controlled and reactive oxygen species dependent

Daniel Storey, Alan McNally · 2020

PLOS Pathogens

Plant-Influenced Gene Expression in the Rice Endophyte Burkholderia kururiensis M130

Bruna G. Coutinho, Danilo Licastro · 2015

Molecular Plant-Microbe Interaction...

Coevolution of the ATPase ClpV, the Sheath Proteins TssB and TssC, and the Accessory Protein TagJ/HsiE1 Distinguishes Type VI Secretion Classes

Andreas Förster, Sara Planamente · 2014

Journal of Biological Chemistry

Two Functional Type VI Secretion Systems in Avian Pathogenic Escherichia coli Are Involved in Different Pathogenic Pathways

Jiale Ma, Yinli Bao · 2014

Infection and Immunity

Identification of a Functional Type VI Secretion System in Campylobacter jejuni Conferring Capsule Polysaccharide Sensitive Cytotoxicity

Nancy M. C. Bleumink-Pluym, Lieke B. van Alphen · 2013

PLOS Pathogens

Type VI secretion system regulation as a consequence of evolutionary pressure

Sarah T. Miyata, Verena Bachmann · 2013

Journal of Medical Microbiology

A Plant Arabinogalactan-Like Glycoprotein Promotes a Novel Type of Polar Surface Attachment by Rhizobium leguminosarum

Fang Xie, Alan Williams · 2012

Molecular Plant-Microbe Interaction...

Type VI Secretion System in Pseudomonas aeruginosa

Abderrahman Hachani, Nadine S. Lossi · 2011

Journal of Biological Chemistry

Regulation of Type VI Secretion Gene Clusters by σ 54 and Cognate Enhancer Binding Proteins

Christophe S. Bernard, Yannick R. Brunet · 2011

Journal of Bacteriology

Comparative genomics of the type VI secretion systems of Pantoea and Erwinia species reveals the presence of putative effector islands that may be translocated by the VgrG and Hcp proteins

Pieter De Maayer, Stephanus N Venter · 2011

BMC Genomics

The Type VI Secretion System: A Multipurpose Delivery System with a Phage-Like Machinery

Angela R. Records · 2011

Molecular Plant-Microbe Interaction...

What is type VI secretion doing in all those bugs?

Sandra Schwarz, Rachel D. Hood · 2010

Trends in Microbiology

Nooks and Crannies in Type VI Secretion Regulation

Christophe S. Bernard, Yannick R. Brunet · 2010

Journal of Bacteriology

Tubules and donuts: a type VI secretion story

Gabriele Bönemann, Aleksandra Pietrosiuk · 2010

Molecular Microbiology

A Pathobiont of the Microbiota Balances Host Colonization and Intestinal Inflammation

Janet Chow, Sarkis K. Mazmanian · 2010

Cell Host & Microbe

In silico analysis reveals multiple putative type VI secretion systems and effector proteins in Pseudomonas syringae pathovars

PANAGIOTIS F. SARRIS, NICHOLAS SKANDALIS · 2010

Molecular Plant Pathology

Metrics

195

Citations

40

References

Details

Published: Jan 01, 2003
Vol/Issue: 16(1)
Pages: 53-64

Authors

Cite This Article

M. R. Bladergroen, K. Badelt, H. P. Spaink (2003). Infection-Blocking Genes of a Symbiotic Rhizobium leguminosarum Strain That Are Involved in Temperature-Dependent Protein Secretion. Molecular Plant-Microbe Interactions®, 16(1), 53-64. https://doi.org/10.1094/mpmi.2003.16.1.53

Infection-Blocking Genes of a Symbiotic Rhizobium leguminosarum Strain That Are Involved in Temperature-Dependent Protein Secretion

You May Also Like