Identification of the Genes of the Plant Pathogen MB03 Required for the Nematicidal Activity Against Through an Integrated Approach

Overview

Journal Front Microbiol

Specialty Microbiology

Date 2022 Mar 31

PMID 35356513

Authors

Muhammad Ali

Tong Gu

Xun Yu

Anum Bashir

Zhiyong Wang

Xiaowen Sun

Naeem Mahmood Ashraf

Lin Li

Affiliations

Soon will be listed here.

Abstract

Nematicidal potential of the common plant pathogen has been recently identified against . The current study was designed to investigate the detailed genetic mechanism of the bacterial pathogenicity by applying comparative genomics, transcriptomics, mutant library screening, and protein expression. Results showed that strain MB03 could kill in the liquid assay by gut colonization. The genome of MB03 was sequenced and comparative analysis including multi locus sequence typing, and genome-to-genome distance placed MB03 in phylogroup II of . Furthermore, comparative genomics of MB03 with nematicidal strains of (PAO1 and PA14) predicted 115 potential virulence factors in MB03. However, genes for previously reported nematicidal metabolites, such as phenazine, pyochelin, and pyrrolnitrin, were found absent in the MB03 genome. Transcriptomics analysis showed that the growth phase of the pathogen considerably affected the expression of virulence factors, as genes for the flagellum, glutamate ABC transporter, /, /, type VI secretion system, and serralysin were highly up-regulated when stationary phase MB03 cells interacted with Additionally, screening of a transposon insertion mutant library led to the identification of other nematicidal genes such as , and . Finally, the nematicidal activity of selected proteins was confirmed by heterologous expression in .

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References

Ammari M, Gresham C, McCarthy F, Nanduri B . HPIDB 2.0: a curated database for host-pathogen interactions. Database (Oxford). 2016; 2016. PMC: 4930832. DOI: 10.1093/database/baw103. View

Meisel J, Panda O, Mahanti P, Schroeder F, Kim D . Chemosensation of bacterial secondary metabolites modulates neuroendocrine signaling and behavior of C. elegans. Cell. 2014; 159(2):267-80. PMC: 4194030. DOI: 10.1016/j.cell.2014.09.011. View

Bradford M . A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976; 72:248-54. DOI: 10.1016/0003-2697(76)90527-3. View

Abbasi A, Bilal M, Khurshid G, Yiotis C, Zeb I, Hussain J . Expression of cyanobacterial genes enhanced CO assimilation and biomass production in transgenic . PeerJ. 2021; 9:e11860. PMC: 8359801. DOI: 10.7717/peerj.11860. View

Uppalapati S, Ishiga Y, Wangdi T, Urbanczyk-Wochniak E, Ishiga T, Mysore K . Pathogenicity of Pseudomonas syringae pv. tomato on tomato seedlings: phenotypic and gene expression analyses of the virulence function of coronatine. Mol Plant Microbe Interact. 2008; 21(4):383-95. DOI: 10.1094/MPMI-21-4-0383. View

Ray A, Rentas C, Caldwell G, Caldwell K . Phenazine derivatives cause proteotoxicity and stress in C. elegans. Neurosci Lett. 2014; 584:23-7. PMC: 4268026. DOI: 10.1016/j.neulet.2014.09.055. View

Young G, Schmiel D, Miller V . A new pathway for the secretion of virulence factors by bacteria: the flagellar export apparatus functions as a protein-secretion system. Proc Natl Acad Sci U S A. 1999; 96(11):6456-61. PMC: 26903. DOI: 10.1073/pnas.96.11.6456. View

Alegado R, Tan M . Resistance to antimicrobial peptides contributes to persistence of Salmonella typhimurium in the C. elegans intestine. Cell Microbiol. 2008; 10(6):1259-73. DOI: 10.1111/j.1462-5822.2008.01124.x. View

Kirienko N, Kirienko D, Larkins-Ford J, Wahlby C, Ruvkun G, Ausubel F . Pseudomonas aeruginosa disrupts Caenorhabditis elegans iron homeostasis, causing a hypoxic response and death. Cell Host Microbe. 2013; 13(4):406-16. PMC: 3641844. DOI: 10.1016/j.chom.2013.03.003. View

10.

Plotnikova J, Rahme L, Ausubel F . Pathogenesis of the human opportunistic pathogen Pseudomonas aeruginosa PA14 in Arabidopsis. Plant Physiol. 2000; 124(4):1766-74. PMC: 59873. DOI: 10.1104/pp.124.4.1766. View

11.

Gomila M, Busquets A, Mulet M, Garcia-Valdes E, Lalucat J . Clarification of Taxonomic Status within the Species Group Based on a Phylogenomic Analysis. Front Microbiol. 2017; 8:2422. PMC: 5725466. DOI: 10.3389/fmicb.2017.02422. View

12.

Njoroge J, Nguyen Y, Curtis M, Moreira C, Sperandio V . Virulence meets metabolism: Cra and KdpE gene regulation in enterohemorrhagic Escherichia coli. mBio. 2012; 3(5):e00280-12. PMC: 3482499. DOI: 10.1128/mBio.00280-12. View

13.

Berry C, Brassinga A, Donald L, Fernando W, Loewen P, de Kievit T . Chemical and biological characterization of sclerosin, an antifungal lipopeptide. Can J Microbiol. 2012; 58(8):1027-34. DOI: 10.1139/w2012-079. View

14.

Nandi M, Selin C, Brassinga A, Belmonte M, Fernando W, Loewen P . Pyrrolnitrin and Hydrogen Cyanide Production by Pseudomonas chlororaphis Strain PA23 Exhibits Nematicidal and Repellent Activity against Caenorhabditis elegans. PLoS One. 2015; 10(4):e0123184. PMC: 4406715. DOI: 10.1371/journal.pone.0123184. View

15.

Dasgupta N, Wolfgang M, Goodman A, Arora S, Jyot J, Lory S . A four-tiered transcriptional regulatory circuit controls flagellar biogenesis in Pseudomonas aeruginosa. Mol Microbiol. 2003; 50(3):809-24. DOI: 10.1046/j.1365-2958.2003.03740.x. View

16.

Atkinson S, Goldstone R, Joshua G, Chang C, Patrick H, Camara M . Biofilm development on Caenorhabditis elegans by Yersinia is facilitated by quorum sensing-dependent repression of type III secretion. PLoS Pathog. 2011; 7(1):e1001250. PMC: 3017118. DOI: 10.1371/journal.ppat.1001250. View

17.

Dudnik A, Dudler R . Non contiguous-finished genome sequence of Pseudomonas syringae pathovar syringae strain B64 isolated from wheat. Stand Genomic Sci. 2014; 8(3):420-9. PMC: 3910705. DOI: 10.4056/sigs.3997732. View

18.

Lindeberg M, Cartinhour S, Myers C, Schechter L, Schneider D, Collmer A . Closing the circle on the discovery of genes encoding Hrp regulon members and type III secretion system effectors in the genomes of three model Pseudomonas syringae strains. Mol Plant Microbe Interact. 2006; 19(11):1151-8. DOI: 10.1094/MPMI-19-1151. View

19.

Delcher A, Bratke K, Powers E, Salzberg S . Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics. 2007; 23(6):673-9. PMC: 2387122. DOI: 10.1093/bioinformatics/btm009. View

20.

Mougous J, Cuff M, Raunser S, Shen A, Zhou M, Gifford C . A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science. 2006; 312(5779):1526-30. PMC: 2800167. DOI: 10.1126/science.1128393. View