Comparative Genomics of Cultured and Uncultured Strains Suggests Genes Essential for Free-Living Growth of Liberibacter

Fagen, Jennie R.; Leonard, Michael T.; McCullough, Connor M.; Edirisinghe, Janaka N.; Henry, Christopher S.; Davis, Michael J.; Triplett, Eric W.

doi:10.1371/journal.pone.0084469

Comparative Genomics of Cultured and Uncultured Strains Suggests Genes Essential for Free-Living Growth of Liberibacter

Journal Article · Wed Jan 08 00:00:00 EST 2014 · PLoS ONE

DOI:https://doi.org/10.1371/journal.pone.0084469· OSTI ID:1627668

Fagen, Jennie R. ^[1]; Leonard, Michael T. ^[2]; McCullough, Connor M. ^[2]; Edirisinghe, Janaka N. ^[3]; Henry, Christopher S. ^[3]; Davis, Michael J. ^[4]; Triplett, Eric W. ^[2]

Univ. of Florida, Gainesville, FL (United States). Inst. of Food and Agricultural Sciences. Microbiology and Cell Science Dept.; DOE/OSTI
Univ. of Florida, Gainesville, FL (United States). Inst. of Food and Agricultural Sciences. Microbiology and Cell Science Dept.
Argonne National Lab. (ANL), Argonne, IL (United States). Mathematics and Computer Science Division
Univ. of Florida, Lake Alfred FL (United States). Inst. of Food an dAgricultural Sciences. Citrus Research and Development Center. Plant Pathology Dept.

The full genomes of two uncultured plant pathogenic Liberibacter, Ca. Liberibacter asiaticus and Ca. Liberibacter solanacearum, are publicly available. Recently, the larger genome of a closely related cultured strain, Liberibacter crescens BT-1, was described. To gain insights into our current inability to culture most Liberibacter, a comparative genomics analysis was done based on the RAST, KEGG, and manual annotations of these three organisms. In addition, pathogenicity genes were examined in all three bacteria. Key deficiencies were identified in Ca. L. asiaticus and Ca. L. solanacearum that might suggest why these organisms have not yet been cultured. Over 100 genes involved in amino acid and vitamin synthesis were annotated exclusively in L. crescens BT-1. However, none of these deficiencies are limiting in the rich media used to date. Other genes exclusive to L. crescens BT-1 include those involved in cell division, the stringent response regulatory pathway, and multiple two component regulatory systems. These results indicate that L. crescens is capable of growth under a much wider range of conditions than the uncultured Liberibacter strains. No outstanding differences were noted in pathogenicity-associated systems, suggesting that L. crescens BT-1 may be a plant pathogen on an as yet unidentified host.

View Accepted Manuscript (DOE)

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Earth and Environmental Systems Science Division

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1627668

Journal Information:: PLoS ONE, Journal Name: PLoS ONE Journal Issue: 1 Vol. 9; ISSN 1932-6203

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

References (75)

The ABC transporters in Candidatus Liberibacter asiaticus Li, Wenlin; Cong, Qian; Pei, Jimin Proteins: Structure, Function, and Bioinformatics, Vol. 80, Issue 11 https://doi.org/10.1002/prot.24147	journal	July 2012
Characterization of a novel Azorhizobium caulinodans ORS571 two-component regulatory system, NtrY/NtrX, involved in nitrogen fixation and metabolism Pawlowski, K.; Klosse, U.; de Bruijn, F. J. Molecular and General Genetics MGG, Vol. 231, Issue 1 https://doi.org/10.1007/bf00293830	journal	December 1991
Polyamines: essential factors for growth and survival Kusano, T.; Berberich, T.; Tateda, C. Planta, Vol. 228, Issue 3 https://doi.org/10.1007/s00425-008-0772-7	journal	July 2008
Basic local alignment search tool Altschul, Stephen F.; Gish, Warren; Miller, Webb Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410 https://doi.org/10.1016/s0022-2836(05)80360-2	journal	October 1990
A global pH sensor: Agrobacterium sensor protein ChvG regulates acid-inducible genes on its two chromosomes and Ti plasmid Li, L.; Jia, Y.; Hou, Q. Proceedings of the National Academy of Sciences, Vol. 99, Issue 19 https://doi.org/10.1073/pnas.192439499	journal	September 2002
The Zinc-responsive Regulator Zur and Its Control of the znu Gene Cluster Encoding the ZnuABC Zinc Uptake System in Escherichia coli Patzer, Silke I.; Hantke, Klaus Journal of Biological Chemistry, Vol. 275, Issue 32 https://doi.org/10.1074/jbc.m001775200	journal	May 2000
Evolution and Multifarious Horizontal Transfer of an Alternative Biosynthetic Pathway for the Alternative Polyamine sym-Homospermidine* Shaw, Frances L.; Elliott, Katherine A.; Kinch, Lisa N. Journal of Biological Chemistry, Vol. 285, Issue 19 https://doi.org/10.1074/jbc.m110.107219	journal	May 2010
EnvZ-OmpR Interaction and Osmoregulation in Escherichia coli Cai, Sheng Jian; Inouye, Masayori Journal of Biological Chemistry, Vol. 277, Issue 27 https://doi.org/10.1074/jbc.m110715200	journal	April 2002
The Bacterial Signal Molecule, ppGpp, Mediates the Environmental Regulation of Both the Invasion and Intracellular Virulence Gene Programs of Salmonella Thompson, Arthur; Rolfe, Matthew D.; Lucchini, Sacha Journal of Biological Chemistry, Vol. 281, Issue 40 https://doi.org/10.1074/jbc.m605616200	journal	August 2006
A defect in cell wall recycling triggers autolysis during the stationary growth phase of Escherichia coli Templin, M. F. The EMBO Journal, Vol. 18, Issue 15 https://doi.org/10.1093/emboj/18.15.4108	journal	August 1999
KEGG: Kyoto Encyclopedia of Genes and Genomes Kanehisa, Minoru; Goto, Susumu Nucleic Acids Research, Vol. 28, Issue 1, p. 27-30 https://doi.org/10.1093/nar/28.1.27	journal	January 2000
The Subsystems Approach to Genome Annotation and its Use in the Project to Annotate 1000 Genomes Overbeek, R. Nucleic Acids Research, Vol. 33, Issue 17 https://doi.org/10.1093/nar/gki866	journal	September 2005
KEGG for integration and interpretation of large-scale molecular data sets Kanehisa, M.; Goto, S.; Sato, Y. Nucleic Acids Research, Vol. 40, Issue D1 https://doi.org/10.1093/nar/gkr988	journal	November 2011
Sinorhizobium meliloti 1021 Loss-of-Function Deletion Mutation in chvI and Its Phenotypic Characteristics Wang, Chunxia; Kemp, Jocelyn; Da Fonseca, Isabel O. Molecular Plant-Microbe Interactions®, Vol. 23, Issue 2 https://doi.org/10.1094/mpmi-23-2-0153	journal	February 2010
Biosynthesis of indole-3-acetic acid via the indole-3-acetamide pathway in Streptomyces spp. Manulis, Shulamit; Shafrir, Hadas; Epstein, Ephraim Microbiology, Vol. 140, Issue 5 https://doi.org/10.1099/13500872-140-5-1045	journal	May 1994
'Candidatus Liberibacter solanacearum', associated with plants in the family Solanaceae Liefting, L. W.; Weir, B. S.; Pennycook, S. R. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 59, Issue 9 https://doi.org/10.1099/ijs.0.007377-0	journal	July 2009
A SitABCD homologue from an avian pathogenic Escherichia coli strain mediates transport of iron and manganese and resistance to hydrogen peroxide Sabri, Mourad; Léveillé, Simon; Dozois, Charles M. Microbiology, Vol. 152, Issue 3 https://doi.org/10.1099/mic.0.28682-0	journal	March 2006
Hormonal Control of Tobacco Crown Gall Tumor Morphology Amasino, Richard M.; Miller, Carlos O. Plant Physiology, Vol. 69, Issue 2 https://doi.org/10.1104/pp.69.2.389	journal	February 1982
Characterization and crystallization of DivK, an essential response regulator for cell division and differentiation in Caulobacter crescentus Cabantous, Stéphanie; Guillet, Valérie; Ohta, Noriko Acta Crystallographica Section D Biological Crystallography, Vol. 58, Issue 7 https://doi.org/10.1107/s0907444902008338	journal	June 2002
Genetic characterization of oligopeptide uptake systems in Sinorhizobium meliloti Nogales, Joaquina; MuÃ±oz, Socorro; Olivares, JosÃ© FEMS Microbiology Letters, Vol. 293, Issue 2 https://doi.org/10.1111/j.1574-6968.2009.01527.x	journal	April 2009
Bacterial peptidoglycan (murein) hydrolases Vollmer, Waldemar; Joris, Bernard; Charlier, Paulette FEMS Microbiology Reviews, Vol. 32, Issue 2 https://doi.org/10.1111/j.1574-6976.2007.00099.x	journal	March 2008
A New Huanglongbing Species, “Candidatus Liberibacter psyllaurous,” Found To Infect Tomato and Potato, Is Vectored by the Psyllid Bactericera cockerelli (Sulc) Hansen, A. K.; Trumble, J. T.; Stouthamer, R. Applied and Environmental Microbiology, Vol. 74, Issue 18 https://doi.org/10.1128/aem.01268-08	journal	August 2008
An Anhydro-N-Acetylmuramyl-l-Alanine Amidase with Broad Specificity Tethered to the Outer Membrane of Escherichia coli Uehara, Tsuyoshi; Park, James T. Journal of Bacteriology, Vol. 189, Issue 15 https://doi.org/10.1128/jb.00446-07	journal	May 2007
Characterization of an ATP Translocase Identified in the Destructive Plant Pathogen “Candidatus Liberibacter asiaticus” Vahling, Cheryl M.; Duan, Yongping; Lin, Hong Journal of Bacteriology, Vol. 192, Issue 3 https://doi.org/10.1128/jb.01279-09	journal	November 2009
Uptake of cell wall peptides by Salmonella typhimurium and Escherichia coli. Goodell, E. W.; Higgins, C. F. Journal of Bacteriology, Vol. 169, Issue 8 https://doi.org/10.1128/jb.169.8.3861-3865.1987	journal	August 1987
Division behavior and shape changes in isogenic ftsZ, ftsQ, ftsA, pbpB, and ftsE cell division mutants of Escherichia coli during temperature shift experiments. Taschner, P. E.; Huls, P. G.; Pas, E. Journal of Bacteriology, Vol. 170, Issue 4 https://doi.org/10.1128/jb.170.4.1533-1540.1988	journal	January 1988
Cytochrome o (cyoABCDE) and d (cydAB) oxidase gene expression in Escherichia coli is regulated by oxygen, pH, and the fnr gene product. Cotter, P. A.; Chepuri, V.; Gennis, R. B. Journal of Bacteriology, Vol. 172, Issue 11 https://doi.org/10.1128/jb.172.11.6333-6338.1990	journal	January 1990
The lethal phenotype caused by null mutations in the Escherichia coli htrB gene is suppressed by mutations in the accBC operon, encoding two subunits of acetyl coenzyme A carboxylase. Karow, M.; Fayet, O.; Georgopoulos, C. Journal of Bacteriology, Vol. 174, Issue 22 https://doi.org/10.1128/jb.174.22.7407-7418.1992	journal	January 1992
ftsE(Ts) Affects Translocation of K+-Pump Proteins into the Cytoplasmic Membrane ofEscherichia coli Ukai, Hideki; Matsuzawa, Hiroshi; Ito, Koreaki Journal of Bacteriology, Vol. 180, Issue 14 https://doi.org/10.1128/jb.180.14.3663-3670.1998	journal	July 1998
Genes Involved in Copper Homeostasis inEscherichia coli Grass, Gregor; Rensing, Christopher Journal of Bacteriology, Vol. 183, Issue 6 https://doi.org/10.1128/jb.183.6.2145-2147.2001	journal	March 2001
Mutations in DivL and CckA Rescue a divJ Null Mutant of Caulobacter crescentus by Reducing the Activity of CtrA Pierce, Deanne L.; O'Donnol, Danielle S.; Allen, Rebecca C. Journal of Bacteriology, Vol. 188, Issue 7 https://doi.org/10.1128/jb.188.7.2473-2482.2006	journal	April 2006
Comparative Genomic Analyses of the Bacterial Phosphotransferase System Barabote, R. D.; Saier, M. H. Microbiology and Molecular Biology Reviews, Vol. 69, Issue 4 https://doi.org/10.1128/mmbr.69.4.608-634.2005	journal	December 2005
Bacterial biosynthesis of indole-3-acetic acid Patten, Cheryl L.; Glick, Bernard R. Canadian Journal of Microbiology, Vol. 42, Issue 3 https://doi.org/10.1139/m96-032	journal	March 1996
The RAST Server: Rapid Annotations using Subsystems Technology Aziz, Ramy K.; Bartels, Daniela; Best, Aaron A. BMC Genomics, Vol. 9, Issue 1, Article No. 75 https://doi.org/10.1186/1471-2164-9-75	journal	January 2008
The Complete Genome Sequence of ‘Candidatus Liberibacter solanacearum’, the Bacterium Associated with Potato Zebra Chip Disease Lin, Hong; Lou, Binghai; Glynn, Jonathan M. PLoS ONE, Vol. 6, Issue 4 https://doi.org/10.1371/journal.pone.0019135	journal	April 2011
Comparison of the ‘Ca. Liberibacter asiaticus’ Genome Adapted for an Intracellular Lifestyle with Other Members of the Rhizobiales Hartung, John S.; Shao, Jonathan; Kuykendall, L. David PLoS ONE, Vol. 6, Issue 8 https://doi.org/10.1371/journal.pone.0023289	journal	August 2011
Predictive Sequence Analysis of the Candidatus Liberibacter asiaticus Proteome Cong, Qian; Kinch, Lisa N.; Kim, Bong-Hyun PLoS ONE, Vol. 7, Issue 7 https://doi.org/10.1371/journal.pone.0041071	journal	July 2012
Complete genome sequence of Liberibacter crescens BT-1 Leonard, Michael T.; Fagen, Jennie R.; Davis-Richardson, Austin G. Standards in Genomic Sciences, Vol. 7, Issue 2 https://doi.org/10.4056/sigs.3326772	journal	December 2012
Characterization of a novel Azorhizobium caulinodans ORS571 two-component regulatory system, NtrY/NtrX, involved in nitrogen fixation and metabolism Pawlowski, K.; Klosse, U.; de Bruijn, F. J. Molecular and General Genetics MGG, Vol. 231, Issue 1 https://doi.org/10.1007/BF00293830	journal	December 1991
Comparative genomics and functional analysis of the NiaP family uncover nicotinate transporters from bacteria, plants, and mammals Jeanguenin, Linda; Lara-Núñez, Aurora; Rodionov, Dmitry A. Functional & Integrative Genomics, Vol. 12, Issue 1 https://doi.org/10.1007/s10142-011-0255-y	journal	September 2011
Kup is the major K + uptake system in Escherichia coli upon hyper-osmotic stress at a low pH Trchounian, Armen; Kobayashi, Hiroshi FEBS Letters, Vol. 447, Issue 2-3 https://doi.org/10.1016/S0014-5793(99)00288-4	journal	March 1999
Iron (III) hydroxamate transport into Escherichia coli. Substrate binding to the periplasmic FhuD protein. Köster, W.; Braun, V. Journal of Biological Chemistry, Vol. 265, Issue 35 https://doi.org/10.1016/S0021-9258(18)45749-3	journal	December 1990
Escherichia coli ppGpp synthetase II activity requires spoT. Hernandez, V. J.; Bremer, H. Journal of Biological Chemistry, Vol. 266, Issue 9 https://doi.org/10.1016/S0021-9258(19)67695-7	journal	March 1991
Basic local alignment search tool Altschul, Stephen F.; Gish, Warren; Miller, Webb Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410 https://doi.org/10.1016/S0022-2836(05)80360-2	journal	October 1990
The cytochrome bd respiratory oxygen reductases Borisov, Vitaliy B.; Gennis, Robert B.; Hemp, James Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1807, Issue 11 https://doi.org/10.1016/j.bbabio.2011.06.016	journal	November 2011
The Transcription Factor DksA Prevents Conflicts between DNA Replication and Transcription Machinery Tehranchi, Ashley K.; Blankschien, Matthew D.; Zhang, Yan Cell, Vol. 141, Issue 4 https://doi.org/10.1016/j.cell.2010.03.036	journal	May 2010
Symbiotic effectiveness and bacteriocin production by Rhizobium leguminosarum bv. viciae isolated from agriculture soils in Faisalabad Hafeez, Fauzia Y.; Naeem, Farrukh I.; Naeem, Rehan Environmental and Experimental Botany, Vol. 54, Issue 2 https://doi.org/10.1016/j.envexpbot.2004.06.008	journal	September 2005
The Escherichia coli amidase AmiC is a periplasmic septal ring component exported via the twin-arginine transport pathway: Amidase transport and localization Bernhardt, Thomas G.; De Boer, Piet A. J. Molecular Microbiology, Vol. 48, Issue 5 https://doi.org/10.1046/j.1365-2958.2003.03511.x	journal	May 2003
Occurrence of enzymes involved in biosynthesis of indole-3-acetic acid from indole-3-acetonitrile in plant-associated bacteria, Agrobacterium and Rhizobium. Kobayashi, M.; Suzuki, T.; Fujita, T. Proceedings of the National Academy of Sciences, Vol. 92, Issue 3 https://doi.org/10.1073/pnas.92.3.714	journal	January 1995
The Zinc-responsive Regulator Zur and Its Control of the znu Gene Cluster Encoding the ZnuABC Zinc Uptake System in Escherichia coli Patzer, Silke I.; Hantke, Klaus Journal of Biological Chemistry, Vol. 275, Issue 32 https://doi.org/10.1074/jbc.M001775200	journal	May 2000
Evolution and Multifarious Horizontal Transfer of an Alternative Biosynthetic Pathway for the Alternative Polyamine sym-Homospermidine* Shaw, Frances L.; Elliott, Katherine A.; Kinch, Lisa N. Journal of Biological Chemistry, Vol. 285, Issue 19 https://doi.org/10.1074/jbc.M110.107219	journal	May 2010
EnvZ-OmpR Interaction and Osmoregulation in Escherichia coli Cai, Sheng Jian; Inouye, Masayori Journal of Biological Chemistry, Vol. 277, Issue 27 https://doi.org/10.1074/jbc.M110715200	journal	April 2002
The Bacterial Signal Molecule, ppGpp, Mediates the Environmental Regulation of Both the Invasion and Intracellular Virulence Gene Programs of Salmonella Thompson, Arthur; Rolfe, Matthew D.; Lucchini, Sacha Journal of Biological Chemistry, Vol. 281, Issue 40 https://doi.org/10.1074/jbc.M605616200	journal	August 2006
GeneMark: web software for gene finding in prokaryotes, eukaryotes and viruses Besemer, J.; Borodovsky, M. Nucleic Acids Research, Vol. 33, Issue Web Server https://doi.org/10.1093/nar/gki487	journal	July 2005
Complete Genome Sequence of Citrus Huanglongbing Bacterium, ‘ Candidatus Liberibacter asiaticus’ Obtained Through Metagenomics Duan, Yongping; Zhou, Lijuan; Hall, David G. Molecular Plant-Microbe Interactions, Vol. 22, Issue 8 https://doi.org/10.1094/MPMI-22-8-1011	journal	August 2009
Sinorhizobium meliloti 1021 Loss-of-Function Deletion Mutation in chvI and Its Phenotypic Characteristics Wang, Chunxia; Kemp, Jocelyn; Da Fonseca, Isabel O. Molecular Plant-Microbe Interactions®, Vol. 23, Issue 2 https://doi.org/10.1094/MPMI-23-2-0153	journal	February 2010
Association of ‘ Candidatus Liberibacter solanacearum’ with Zebra Chip Disease of Potato Established by Graft and Psyllid Transmission, Electron Microscopy, and PCR Secor, G. A.; Rivera, V. V.; Abad, J. A. Plant Disease, Vol. 93, Issue 6 https://doi.org/10.1094/PDIS-93-6-0574	journal	June 2009
Heat Treatment Eliminates ‘ Candidatus Liberibacter asiaticus’ from Infected Citrus Trees Under Controlled Conditions Hoffman, Michele T.; Doud, Melissa S.; Williams, Lisa Phytopathology®, Vol. 103, Issue 1 https://doi.org/10.1094/PHYTO-06-12-0138-R	journal	January 2013
The Phloem-Limited Bacterium of Greening Disease of Citrus Is a Member of the Subdivision of the Proteobacteria Jagoueix, S.; Bove, J. -M.; Garnier, M. International Journal of Systematic Bacteriology, Vol. 44, Issue 3 https://doi.org/10.1099/00207713-44-3-379	journal	July 1994
'Candidatus Liberibacter americanus', associated with citrus huanglongbing (greening disease) in Sao Paulo State, Brazil Teixeira, D. d. C. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 55, Issue 5 https://doi.org/10.1099/ijs.0.63677-0	journal	September 2005
Auxin and Plant-Microbe Interactions Spaepen, S.; Vanderleyden, J. Cold Spring Harbor Perspectives in Biology, Vol. 3, Issue 4 https://doi.org/10.1101/cshperspect.a001438	journal	November 2010
Phloem Metabolism and Function Have to Cope with Low Internal Oxygen van Dongen, Joost T.; Schurr, Ulrich; Pfister, Michelle Plant Physiology, Vol. 131, Issue 4 https://doi.org/10.1104/pp.102.017202	journal	April 2003
Characterization and crystallization of DivK, an essential response regulator for cell division and differentiation in Caulobacter crescentus Cabantous, Stéphanie; Guillet, Valérie; Ohta, Noriko Acta Crystallographica Section D Biological Crystallography, Vol. 58, Issue 7 https://doi.org/10.1107/S0907444902008338	journal	June 2002
EfeUOB (YcdNOB) is a tripartite, acid-induced and CpxAR-regulated, low-pH Fe ²⁺ transporter that is cryptic in Escherichia coli K-12 but functional in E. coli O157:H7: Low pH, Fe ²⁺ transporter in E. coli Cao, Jieni; Woodhall, Mark R.; Alvarez, Javier Molecular Microbiology, Vol. 65, Issue 4 https://doi.org/10.1111/j.1365-2958.2007.05802.x	journal	June 2007
‘Candidatus Liberibacter europaeus’ sp. nov. that is associated with and transmitted by the psyllid Cacopsylla pyri apparently behaves as an endophyte rather than a pathogen: ‘Ca. iberibacter europaeus’ associated with C. pyri Raddadi, Noura; Gonella, Elena; Camerota, Caterina Environmental Microbiology, Vol. 13, Issue 2 https://doi.org/10.1111/j.1462-2920.2010.02347.x	journal	October 2010
A Plant miRNA Contributes to Antibacterial Resistance by Repressing Auxin Signaling Navarro, L.; Dunoyer, P.; Jay, F. Science, Vol. 312, Issue 5772 https://doi.org/10.1126/science.1126088	journal	April 2006
A New Huanglongbing Species, “Candidatus Liberibacter psyllaurous,” Found To Infect Tomato and Potato, Is Vectored by the Psyllid Bactericera cockerelli (Sulc) Hansen, A. K.; Trumble, J. T.; Stouthamer, R. Applied and Environmental Microbiology, Vol. 74, Issue 18 https://doi.org/10.1128/AEM.01268-08	journal	August 2008
An Anhydro-N-Acetylmuramyl-l-Alanine Amidase with Broad Specificity Tethered to the Outer Membrane of Escherichia coli Uehara, Tsuyoshi; Park, James T. Journal of Bacteriology, Vol. 189, Issue 15 https://doi.org/10.1128/JB.00446-07	journal	May 2007
Characterization of a γ-Aminobutyric Acid Transport System of Rhizobium leguminosarum bv. viciae 3841 White, J. P.; Prell, J.; Ramachandran, V. K. Journal of Bacteriology, Vol. 191, Issue 5 https://doi.org/10.1128/JB.00926-08	journal	December 2008
Characterization of an ATP Translocase Identified in the Destructive Plant Pathogen “Candidatus Liberibacter asiaticus” Vahling, Cheryl M.; Duan, Yongping; Lin, Hong Journal of Bacteriology, Vol. 192, Issue 3 https://doi.org/10.1128/JB.01279-09	journal	November 2009
ftsE(Ts) Affects Translocation of K+-Pump Proteins into the Cytoplasmic Membrane ofEscherichia coli Ukai, Hideki; Matsuzawa, Hiroshi; Ito, Koreaki Journal of Bacteriology, Vol. 180, Issue 14 https://doi.org/10.1128/JB.180.14.3663-3670.1998	journal	July 1998
Genes Involved in Copper Homeostasis inEscherichia coli Grass, Gregor; Rensing, Christopher Journal of Bacteriology, Vol. 183, Issue 6 https://doi.org/10.1128/JB.183.6.2145-2147.2001	journal	March 2001
Mutations in DivL and CckA Rescue a divJ Null Mutant of Caulobacter crescentus by Reducing the Activity of CtrA Pierce, Deanne L.; O'Donnol, Danielle S.; Allen, Rebecca C. Journal of Bacteriology, Vol. 188, Issue 7 https://doi.org/10.1128/JB.188.7.2473-2482.2006	journal	April 2006
Comparative Genomic Analyses of the Bacterial Phosphotransferase System Barabote, R. D.; Saier, M. H. Microbiology and Molecular Biology Reviews, Vol. 69, Issue 4 https://doi.org/10.1128/MMBR.69.4.608-634.2005	journal	December 2005
A chromosomally encoded two-component sensory transduction system is required for virulence of Agrobacterium tumefaciens. Charles, T. C.; Nester, E. W. Journal of Bacteriology, Vol. 175, Issue 20 https://doi.org/10.1128/jb.175.20.6614-6625.1993	journal	January 1993

Cited By (21)

Liberibacter crescens biofilm formation in vitro: establishment of a model system for pathogenic ‘Candidatus Liberibacter spp.’ Naranjo, Eber; Merfa, Marcus V.; Ferreira, Virginia Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-41495-5	journal	March 2019
LdtR is a master regulator of gene expression in L iberibacter asiaticus Pagliai, Fernando A.; Coyle, Janelle F.; Kapoor, Sharan Microbial Biotechnology, Vol. 10, Issue 4 https://doi.org/10.1111/1751-7915.12728	journal	May 2017
Controlled replication of ‘ Candidatus Liberibacter asiaticus ‘ DNA in citrus leaf discs Attaran, Elham; Berim, Anna; Killiny, Nabil Microbial Biotechnology, Vol. 13, Issue 3 https://doi.org/10.1111/1751-7915.13531	journal	January 2020
Growth Dynamics and Survival of Liberibacter crescens BT-1, an Important Model Organism for the Citrus Huanglongbing Pathogen “ Candidatus Liberibacter asiaticus” Sena-Vélez, Marta; Holland, Sean D.; Aggarwal, Manu Applied and Environmental Microbiology, Vol. 85, Issue 21 https://doi.org/10.1128/aem.01656-19	journal	November 2019
Growth parameters of Liberibacter crescens suggest ammonium and phosphate as essential molecules in the Liberibacter-plant host interface Cruz-Munoz, Maritsa; Munoz-Beristain, Alam; Petrone, Joseph R. BMC Microbiology, Vol. 19, Issue 1 https://doi.org/10.1186/s12866-019-1599-z	journal	October 2019
Comprehensive meta-analysis, co-expression, and miRNA nested network analysis identifies gene candidates in citrus against Huanglongbing disease Rawat, Nidhi; Kiran, Sandhya P.; Du, Dongliang BMC Plant Biology, Vol. 15, Issue 1 https://doi.org/10.1186/s12870-015-0568-4	journal	July 2015
Development of a Microemulsion Formulation for Antimicrobial SecA Inhibitors Hu, Jiahuai; Akula, Nagaraju; Wang, Nian PLOS ONE, Vol. 11, Issue 3 https://doi.org/10.1371/journal.pone.0150433	journal	March 2016
Genomic sequence of 'Candidatus Liberibacter solanacearum' haplotype C and its comparison with haplotype A and B genomes Wang, Jinhui; Haapalainen, Minna; Schott, Thomas PLOS ONE, Vol. 12, Issue 2 https://doi.org/10.1371/journal.pone.0171531	journal	February 2017
Identification of the Genes Required for the Culture of Liberibacter crescens, the Closest Cultured Relative of the Liberibacter Plant Pathogens Lai, Kin-Kwan; Davis-Richardson, Austin G.; Dias, Raquel Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00547	journal	April 2016
SEC-Translocon Dependent Extracytoplasmic Proteins of Candidatus Liberibacter asiaticus Prasad, Samiksha; Xu, Jin; Zhang, Yunzeng Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.01989	journal	December 2016
Identification of the Tolfenamic Acid Binding Pocket in PrbP from Liberibacter asiaticus Pan, Lei; Gardner, Christopher L.; Pagliai, Fernando A. Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01591	journal	August 2017
Genome Analysis of Haplotype D of Candidatus Liberibacter Solanacearum Katsir, Leron; Zhepu, Ruan; Santos Garcia, Diego Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.02933	journal	December 2018
Lessons from One Fastidious Bacterium to Another: What Can We Learn about Liberibacter Species from Xylella fastidiosa Kruse, Angela; Fleites, Laura A.; Heck, Michelle Insects, Vol. 10, Issue 9 https://doi.org/10.3390/insects10090300	journal	September 2019
Liberibacter crescens gen. nov., sp. nov., the first cultured member of the genus Liberibacter Fagen, Jennie R.; Leonard, Michael T.; Coyle, Janelle F. International Journal of Systematic and Evolutionary Microbiology, Vol. 64, Issue Pt_7 https://doi.org/10.1099/ijs.0.063255-0	journal	July 2014
Potential soil transmission of a novel Candidatus Liberibacter strain detected in citrus seedlings grown in soil from a huanglongbing infested citrus grove Nunes da Rocha, Ulisses; Shin, Keumchul; Timilsina, Sujan bioRxiv https://doi.org/10.1101/821553	posted_content	January 2019
Novel ‘ Candidatus Liberibacter’ species identified in the Australian eggplant psyllid, Acizzia solanicola Morris, Jacqueline; Shiller, Jason; Mann, Rachel Microbial Biotechnology, Vol. 10, Issue 4 https://doi.org/10.1111/1751-7915.12707	journal	April 2017
Biology and epidemics of Candidatus Liberibacter species, psyllid-transmitted plant-pathogenic bacteria Haapalainen, M. Annals of Applied Biology, Vol. 165, Issue 2 https://doi.org/10.1111/aab.12149	journal	August 2014
Multiple guests in a single host: interactions across symbiotic and phytopathogenic bacteria in phloem‐feeding vectors – a review Gonella, Elena; Tedeschi, Rosemarie; Crotti, Elena Entomologia Experimentalis et Applicata, Vol. 167, Issue 3 https://doi.org/10.1111/eea.12766	journal	February 2019
“Candidatus Liberibacter asiaticus” Prophage Late Genes May Limit Host Range and Culturability Fleites, Laura A.; Jain, Mukesh; Zhang, Shujian Applied and Environmental Microbiology, Vol. 80, Issue 19 https://doi.org/10.1128/aem.01958-14	journal	October 2014
A novel Zn chelate (TSOL) that moves systemically in citrus plants inhibits growth and biofilm formation of bacterial pathogens Mendis, Hajeewaka C.; Ozcan, Ali; Santra, Swadeshmukul PLOS ONE, Vol. 14, Issue 6 https://doi.org/10.1371/journal.pone.0218900	journal	June 2019
A Comprehensive Overview of Online Resources to Identify and Predict Bacterial Essential Genes Peng, Chong; Lin, Yan; Luo, Hao Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.02331	journal	November 2017

Similar Records

‘Candidatus Liberibacter asiaticus’-Encoded BCP Peroxiredoxin Suppresses Lipopolysaccharide-Mediated Defense Signaling and Nitrosative Stress In Planta

Journal Article · Wed Mar 09 19:00:00 EST 2022 · Molecular Plant-Microbe Interactions · OSTI ID:1963234

Linking metabolic phenotypes to pathogenic traits among “Candidatus Liberibacter asiaticus” and its hosts

Journal Article · Mon Aug 03 20:00:00 EDT 2020 · npj Systems Biology and Applications · OSTI ID:1802443

Structure of Lipopolysaccharide from Liberibacter crescens Is Low Molecular Weight and Offers Insight into Candidatus Liberibacter Biology

Journal Article · Sun Oct 17 20:00:00 EDT 2021 · International Journal of Molecular Sciences (Online) · OSTI ID:1963261

Related Subjects

54 ENVIRONMENTAL SCIENCES
59 BASIC BIOLOGICAL SCIENCES
Invertebrate genomics
bacterial genomics
biosynthesis
gene regulation
genomics
peptidoglycans
plant pathogens
secretion systems

Comparative Genomics of Cultured and Uncultured Strains Suggests Genes Essential for Free-Living Growth of Liberibacter

Citation Formats

References (75)

Cited By (21)

Similar Records

Related Subjects