Skip to main content

Advertisement

SpringerLink
Log in

Identification of virulence-associated factors in Vibrio parahaemolyticus with special reference to moonlighting protein: a secretomics study

  • Research
  • Published:
International Microbiology Aims and scope Submit manuscript

Abstract

Vibrio parahaemolyticus causes seafood-borne gastroenteritis infection in human which can even lead to death. The pathogenic strain of V. parahaemolyticus secretes different types of virulence factors that are directly injected into the host cell by a different type of secretion system which helps bacteria to establish its own ecological niche within the organism. Therefore, the aim of this study was to isolate the extracellular secreted proteins from the trh positive strain of V. parahaemolyticus and identify them using two-dimensional gel electrophoresis and MALDI-TOFMS/MS. Seventeen different cellular proteins viz, Carbamoyl-phosphate synthase, 5-methyltetrahydropteroyltriglutamate, tRNA-dihydrouridine synthase, Glycerol-3-phosphate dehydrogenase, Orotidine 5′-phosphate decarboxylase, Molybdenum import ATP-binding protein, DnaJ, DNA polymerase IV, Ribosomal RNA small subunit methyltransferase G, ATP synthase subunit delta and gamma, Ribosome-recycling factor, 4-hydroxy-3-methylbut-2-en-1-yl diphosphate synthase, tRNA pseudouridine synthase B, Ditrans, polycis-undecaprenyl-diphosphate synthase, Oxygen-dependent coproporphyrinogen-III oxidase, and Peptide deformylase 2 were identified which are mainly involved in different metabolic and biosynthetic pathways. Furthermore, the molecular function of the identified proteins were associated with catalytic activity, ligase activity, transporter, metal binding, and ATP synthase when they are intercellular. However, to understand the importance of these secreted proteins in the infection and survival of bacteria inside the host cell, pathogen–host protein-protein interactions (PPIs) were carried out which identified the association of eight secreted proteins with 41 human proteins involved in different cellular pathways, including ubiquitination degradation, adhesion, inflammation, immunity, and programmed cell death. The present study provides unreported strategies on host-cell environment’s survival and adaptation mechanisms for the successful establishment of infections and intracellular propagation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Data availability

The article and supplementary information contain all the relevant data pertaining to the study.

References

  • Aguilera L, Ferreira E, Giménez R, Fernández FJ, Taulés M, Aguilar J, Vega MC, Badia J, Baldomà L (2012) Secretion of the housekeeping protein glyceraldehyde-3-phosphate dehydrogenase by the LEE-encoded type III secretion system in enteropathogenic Escherichia coli. Int J Biochem Cell Biol 44(6):955–962

    Article  CAS  PubMed  Google Scholar 

  • Albuquerque PC, Nakayasu ES, Rodrigues ML, Frases S, Casadevall A, Zancope-Oliveira RM, Almeida IC, Nosanchuk JD (2008) Vesicular transport in Histoplasma capsulatum: an effective mechanism for trans-cell wall transfer of proteins and lipids in ascomycetes. Cell Microbiol 10(8):1695–1710

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alvarez AH, Martinez-Cadena G, Silva ME, Saavedra E, Avila EE (2007) Entamoeba histolytica: ADP-ribosylation of secreted glyceraldehyde-3-phosphate dehydrogenase. Exp Parasitol 117(4):349–356

    Article  CAS  PubMed  Google Scholar 

  • Ammari MG, Gresham CR, McCarthy FM, Nanduri B (2016) HPIDB 2.0: a curated database for host–pathogen interactions. Database (Oxford) 3:2016

    Google Scholar 

  • Ashida H, Mimuro H, Ogawa M, Kobayashi T, Sanada T, Kim M, Sasakawa C (2011) Cell death and infection: a double-edged sword for host and pathogen survival. J Cell Biol 195(6):931–942

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barbey C, Budin-Verneuil A, Cauchard S, Hartke A, Laugier C, Pichereau V, Petry S (2009) Proteomic analysis and immunogenicity of secreted proteins from Rhodococcus equi ATCC 33701. Vet Microbiol 135(3-4):334–345

    Article  CAS  PubMed  Google Scholar 

  • Barbosa MS, Báo SN, Andreotti PF, de Faria FP, Felipe MSS, dos Santos FL, de Almeida M-GMJS, Soares CM (2006) Glyceraldehyde-3-phosphate dehydrogenase of Paracoccidioides brasiliensis is a cell surface protein involved in fungal adhesion to extracellular matrix proteins and interaction with cells. Infect Immun 74(1):382–389

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baron C (2009) Mechanistic and Structural Analysis of Type IV Secretion Systems. In: Wooldridge K (ed) Bacterial Secreted Proteins: Secretory Mechanisms and Role in Pathogenesis. Caister Academic Press, Hethersett, Norwich, UK, pp 117–137

    Google Scholar 

  • Bennuru S, Semnani R, Meng Z, Ribeiro JM, Veenstra TD, Nutman TB (2009) Brugia malayi excreted/secreted proteins at the host/parasite interface: stage-and gender-specific proteomic profiling. PLoS Negl Trop Dis 3(4):e410

    Article  PubMed  PubMed Central  Google Scholar 

  • Beys-da-Silva WO, Santi L, Berger M, Calzolari D, Passos DO, Guimarães JA, Moresco JJ, Yates JR (2014) Secretome of the biocontrol agent Metarhizium anisopliae induced by the cuticle of the cotton pest Dysdercus peruvianus reveals new insights into infection. J Proteome Res 13(5):2282–2296

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72(1-2):248–254

    Article  CAS  PubMed  Google Scholar 

  • Burdette DL, Yarbrough ML, Orvedahl A, Gilpin CJ, Orth K (2008) Vibrio parahaemolyticus orchestrates a multifaceted host cell infection by induction of autophagy, cell rounding, and then cell lysis. Proc Natl Acad Sci USA 105(34):12497–12500

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chitlaru T, Gat O, Grosfeld H, Inbar I, Gozlan Y, Shafferman A (2007) Identification of in vivo-expressed immunogenic proteins by serological proteome analysis of the Bacillus anthracis secretome. Infect Immun 75(6):2841–2852

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Christie-Oleza JA, Armengaud J, Guerin P, Scanlan DJ (2015) Functional distinctness in the exoproteomes of marine S. ynechococcus. Environ Microbiol 17(10):3781–3794

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cline MS, Smoot M, Cerami E, Kuchinsky A, Landys N, Workman C, Christmas R, Avila-Campilo I, Creech M, Gross B, Hanspers K (2007) Integration of biological networks and gene expression data using Cytoscape. Nat Protoc 2(10):2366–2382

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coburn B, Sekirov I, Finlay BB (2007) Type III secretion systems and disease. Clin Microbiol Rev 20(4):535–549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cornejo-Granados F, Zatarain-Barrón ZL, Cantu-Robles VA, Mendoza-Vargas A, Molina-Romero C, Sánchez F, Del Pozo-Yauner L, Hernandez-Pando R, Ochoa-Leyva A (2017) Secretome prediction of two M. tuberculosis clinical isolates reveals their high antigenic density and potential drug targets. Front Microbiol 8:128

    Article  PubMed  PubMed Central  Google Scholar 

  • Cornells GR (2000) Type III secretion: a bacterial device for close combat with cells of their eukaryotic host. Philos Trans R Soc Lond B Biol Sci 355(1397):681–693

    Article  Google Scholar 

  • Cui T, Li W, Liu L, Huang Q, He ZG (2016) Uncovering new pathogen–host protein–protein interactions by pairwise structure similarity. PLoS One 11(1):e0147612

    Article  PubMed  PubMed Central  Google Scholar 

  • Delannoy A, Wilhelm E, Eilebrecht S, Alvarado-Cuevas EM, Benecke AG, Bell B (2018) BIM and NOXA are mitochondrial effectors of TAF6δ-driven apoptosis. Cell Death Dis 9(2):1–15

    Article  CAS  Google Scholar 

  • Deng W, Marshall NC, Rowland JL, McCoy JM, Worrall LJ, Santos AS, Strynadka NC, Finlay BB (2017) Assembly, structure, function and regulation of type III secretion systems. Nat Rev Microbiol 15(6):323

    Article  CAS  PubMed  Google Scholar 

  • Dufies O, Boyer L (2021) RhoGTPases and inflammasomes: guardians of effector-triggered immunity. PLoS Pathog 17(4):e1009504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dyer MD, Neff C, Dufford M, Rivera CG, Shattuck D, Bassaganya-Riera J, Murali TM, Sobral BW (2010) The human-bacterial pathogen protein interaction networks of Bacillus anthracis, Francisella tularensis, and Yersinia pestis. PLoS One 5(8):e12089

    Article  PubMed  PubMed Central  Google Scholar 

  • Ebner P, Luqman A, Reichert S, Hauf K, Popella P, Forchhammer K, Otto M, Götz F (2017) Non-classical protein excretion is boosted by PSMα-induced cell leakage. Cell Rep 20(6):1278–1286

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Egea L, Aguilera L, Gimenez R, Sorolla MA, Aguilar J, Badía J, Baldoma L (2007) Role of secreted glyceraldehyde-3-phosphate dehydrogenase in the infection mechanism of enterohemorrhagic and enteropathogenic Escherichia coli: interaction of the extracellular enzyme with human plasminogen and fibrinogen. Int J Biochem Cell Biol 39(6):1190–1203

    Article  CAS  PubMed  Google Scholar 

  • Farhan H, Rabouille C (2011) Signalling to and from the secretory pathway. J Cell Sci 124(2):171–180

    Article  CAS  PubMed  Google Scholar 

  • Galka F, Wai SN, Kusch H, Engelmann S, Hecker M, Schmeck B, Hippenstiel S, Uhlin BE, Steinert M (2008) Proteomic characterization of the whole secretome of Legionella pneumophila and functional analysis of outer membrane vesicles. Infect Immun 76(5):1825–1836

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • García K, Yáñez C, Plaza N, Peña F, Sepúlveda P, Pérez-Reytor D, Espejo RT (2017) Gene expression of Vibrio parahaemolyticus growing in laboratory isolation conditions compared to those common in its natural ocean environment. BMC Microbial 17(1):1–10

    Google Scholar 

  • Geraci J, Neubauer S, Pöllath C, Hansen U, Rizzo F, Krafft C, Westermann M, Hussain M, Peters G, Pletz MW, Löffler B (2017) The Staphylococcus aureus extracellular matrix protein (Emp) has a fibrous structure and binds to different extracellular matrices. Sci Rep 7(1):13665

    Article  PubMed  PubMed Central  Google Scholar 

  • Glowalla E, Tosetti B, Krönke M, Krut O (2009) Proteomics-based identification ofanchorless cell wall proteins as vaccine candidates against Staphylococcus aureus. Infect Immun 77(7):2719–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gotoh K, Kodama T, Hiyoshi H, Izutsu K, Park KS, Dryselius R, Akeda Y, Honda T, Iida T (2010) Bile acid-induced virulence gene expression of Vibrio parahaemolyticus reveals a novel therapeutic potential for bile acid sequestrants. PLoS One 5(10):e13365

    Article  PubMed  PubMed Central  Google Scholar 

  • Gralnick JA, Newman DK (2007) Extracellular respiration. Mol Microbiol 65(1):1–11

    Article  PubMed  PubMed Central  Google Scholar 

  • Green ER, Mecsas J (2016) Bacterial secretion systems: an overview. Virulence mechanisms of bacterial pathogen. Microbiol Spectr 4(1):1–19

    Article  CAS  Google Scholar 

  • Gupta MK, Subramanian V, Yadav JS (2009) Immunoproteomic identification of secretory and subcellular protein antigens and functional evaluation of the secretome fraction of Mycobacterium immunogenum, a newly recognized species of the Mycobacterium chelonae-Mycobacterium abscessus group. J Proteome Res 8(5):2319–2330

    Article  CAS  PubMed  Google Scholar 

  • Hallgren J, Tsirigos KD, Pedersen MD, Armenteros JJA, Marcatili P, Nielsen H, Krogh A, Winther O (2022) DeepTMHMM predicts alpha and beta transmembrane proteins using deep neural networks. bioRxiv 10:2022 04

    Google Scholar 

  • He Y, Wang H, Chen L (2015) Comparative secretomics reveals novel virulence-associated factors of Vibrio parahaemolyticus. Front Microbiol 6:707

    Article  PubMed  PubMed Central  Google Scholar 

  • Hiller K, Grote A, Scheer M, Münch R, Jahn D (2004) PrediSi: prediction of signal peptides and their cleavage positions. Nucleic Acids Res 32:W375–W379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hubbard TP, Chao MC, Abel S, Blondel CJ, zur Wiesch PA, Zhou X, Davis BM, Waldor MK (2016) Genetic analysis of Vibrio parahaemolyticus intestinal colonization. Proc Natl Acad Sci USA 113:6283–6288

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huo T, Liu W, Guo Y, Yang C, Lin J, Rao Z (2015) Prediction of host-pathogen protein interactions between Mycobacterium tuberculosis and Homo sapiens using sequence motifs. BMC Bioinform 16:100

    Article  Google Scholar 

  • Islam N, Nagy A, Garrett WM, Shelton D, Cooper B, Nou X (2016) Different cellular origins and functions of extracellular proteins from Escherichia coli O157: H7 and O104: H4 as determined by comparative proteomic analysis. Appl Environ Microbiol 82:4371–4378

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kapur SK, Katz AJ (2013) Review of the adipose derived stem cell secretome. Biochimie 95:2222–2228

    Article  CAS  PubMed  Google Scholar 

  • Karam J, Méresse S, Kremer L, Daher W (2020) The roles of tetraspanins in bacterial infections. Cell Microbiol 22:e13260

    Article  CAS  PubMed  Google Scholar 

  • Kenny B, Finlay BB (1995) Protein secretion by enteropathogenic Escherichia coli is essential for transducing signals to epithelial cells. Proc Natl Acad Sci USA 92:7991–7995

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar R, Nanduri B (2010) HPIDB-a unified resource for host-pathogen interactions. BMC Bioinform 11:S16

    Article  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680

    Article  CAS  PubMed  Google Scholar 

  • Lamkanfi M, Dixit VM (2010) Manipulation of host cell death pathways during microbial infections. Cell Host Microbe 8:44–54

    Article  CAS  PubMed  Google Scholar 

  • Lehr S, Hartwig S, Sell H (2012) Adipokines: a treasure trove for the discovery of biomarkers for metabolic disorders. Proteomics Clin Appl 6:91–101

    Article  CAS  PubMed  Google Scholar 

  • Lerm M, Schmidt G, Aktories K (2000) Bacterial protein toxins targeting rho GTPases. FEMS Microbiol Lett 188:1–6

    Article  CAS  PubMed  Google Scholar 

  • Letchumanan V, Chan KG, Khan TM, Bukhari SI, Ab Mutalib NS, Goh BH, Lee LH (2017) Bile sensing: the activation of Vibrio parahaemolyticus virulence. Front Microbiol 8:728

    Article  PubMed  PubMed Central  Google Scholar 

  • Li P, Rivera-Cancel G, Kinch LN, Salomon D, Tomchick DR, Grishin NV, Orth K (2016) Bile salt receptor complex activates a pathogenic type III secretion system. Elife 5:e15718

    Article  PubMed  PubMed Central  Google Scholar 

  • Löwer M, Weydig C, Metzler D, Reuter A, Starzinski-Powitz A, Wessler S, Schneider G (2008) Prediction of extracellular proteases of the human pathogen Helicobacter pylori reveals proteolytic activity of the Hp1018/19 protein HtrA. PLoS One 3(10):e3510

    Article  PubMed  PubMed Central  Google Scholar 

  • Ma W, Guttman DS (2008) Evolution of prokaryotic and eukaryotic virulence effectors. Curr Opin Plant Biol 11:412–419

    Article  CAS  PubMed  Google Scholar 

  • Maffei B, Francetic O, Subtil A (2017) Tracking proteins secreted by bacteria: what's in the toolbox? Front Cell Infect Microbiol 7:221

    Article  PubMed  PubMed Central  Google Scholar 

  • Mahdavi A, Szychowski J, Ngo JT, Sweredoski MJ, Graham RL, Hess S, Schneewind O, Mazmanian SK, Tirrell DA (2014) Identification of secreted bacterial proteins by noncanonical amino acid tagging. Proc Natl Acad Sci USA 111:433–438

    Article  CAS  PubMed  Google Scholar 

  • Marketon JIW, Sternberg EM (2010) The glucocorticoid receptor: a revisited target for toxins. Toxins 2:1357–1380

    Article  PubMed  PubMed Central  Google Scholar 

  • Michel GP, Voulhoux R (2009) The type II secretory system (T2SS) in Gram-negative bacteria: a molecular nanomachine for secretion of Sec and Tatdependent extracellular proteins. In: Wooldridge KG (ed) Bacterial Secreted Proteins: Secretory Mechanisms and Role in Pathogenesis. Caister Academic Press, Norfolk, pp 67–92

    Google Scholar 

  • Mota LJ, Sorg I, Cornelis GR (2005) Type III secretion: the bacteria-eukaryotic cell express. FEMS Microbiol Lett 252(1):1–10

    Article  CAS  PubMed  Google Scholar 

  • Muthukrishnan G, Quinn GA, Lamers RP, Diaz C, Cole AL, Chen S, Cole AM (2011) Exoproteome of Staphylococcus aureus reveals putative determinants of nasal carriage. J Proteome Res 10(4):2064–2078

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Naderer T, Fulcher MC (2018) Targeting apoptosis pathways in infections. J Leukoc Biol 103(2):275–285

    Article  CAS  PubMed  Google Scholar 

  • O’Farrell PH (1975) High- resolution two-dimentional electrophoresis of proteins. J Biol Chem 250(10):4007–4027

    Article  PubMed  Google Scholar 

  • Pace JL, Chai TJ, Rossi HA, Jiang X (1997) Effect of bile on Vibrio parahaemolyticus. Appl Environ Microbiol 63(6):2372–2377

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paria P, Behera BK, Mohapatra PKD, Parida PK (2021) Virulence factor genes and comparative pathogenicity study of tdh, trh and tlh positive Vibrio parahaemolyticus strains isolated from Whiteleg shrimp, Litopenaeus vannamei (Boone, 1931) in India. Infect Genet Evol 95:105083

    Article  CAS  PubMed  Google Scholar 

  • Paria P, Chakraborty HJ, Behera BK (2022) Identification of novel salt tolerance-associated proteins from the secretome of Enterococcus faecalis. World J Microbiol Biotechnol 38(10):177

    Article  CAS  PubMed  Google Scholar 

  • Paria P, Chakraborty HJ, Behera BK, Mohapatra PKD, Das BK (2019) Computational characterization and molecular dynamics simulation of the thermostable direct hemolysin-related hemolysin (TRH) amplified from Vibrio parahaemolyticus. Microb Pathog 127:172–182

    Article  CAS  PubMed  Google Scholar 

  • Park KS, Ono T, Rokuda M, Jang MH, Okada K, Iida T, Honda T (2004) Functional characterization of two type III secretion systems of Vibrio parahaemolyticus. Infect Immun 72(11):6659–6665

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pathak VM (2017) Review on the current status of polymer degradation: a microbial approach. Bioresour Bioprocess 4:1–31

    Article  Google Scholar 

  • Pearson WR (2013) An introduction to sequence similarity (“homology”) searching. Curr Protoc Bioinformatics 42(1):3–1

    Article  Google Scholar 

  • Petronella N, Ronholm J (2018) The mechanisms that regulate Vibrio parahaemolyticus virulence gene expression differ between pathotypes. Microb Genom 4(6):e000182

    PubMed  PubMed Central  Google Scholar 

  • Renier S, Micheau P, Talon R, Hébraud M, Desvaux M (2012) Subcellular localization of extracytoplasmic proteins in monoderm bacteria: rational secretomics-based strategy for genomic and proteomic analyses. PLoS One 7(8):e42982

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salomon D, Klimko JA, Orth K (2014) H-NS regulates the Vibrio parahaemolyticus type VI secretion system 1. Microbiology 160(Pt 9):1867

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sangsri T, Saiprom N, Tubsuwan A, Monk P, Partridge LJ, Chantratita N (2020) Tetraspanins are involved in Burkholderia pseudomallei-induced cell-to-cell fusion of phagocytic and non-phagocytic cells. Sci Rep 10(1):17972

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Satala D, Karkowska-Kuleta J, Zelazna A, Rapala-Kozik M, Kozik A (2020) Moonlighting proteins at the candidal cell surface. Microorganisms 8(7):1046

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schweppe DK, Harding C, Chavez JD, Wu X, Ramage E, Singh PK, Manoil C, Bruce JE (2015) Host-microbe protein interactions during bacterial infection. Chem Biol 22(11):1521–1530

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shan X, Fu J, Li X, Peng X, Chen L (2022) Comparative proteomics and secretomics revealed virulence, and coresistance-related factors in non O1/O139 Vibrio cholerae recovered from 16 species of consumable aquatic animals. J Proteome 251:104408

    Article  CAS  Google Scholar 

  • Shevchenko A, Tomas H, Havli J, Olsen JV, Mann M (2006) In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protoc 1(6):2856–2860

    Article  CAS  PubMed  Google Scholar 

  • Singh B, Fleury C, Jalalvand F, Riesbeck K (2012) Human pathogens utilize host extracellular matrix proteins laminin and collagen for adhesion and invasion of the host. FEMS Microbiol Rev 36(6):1122–1180

    Article  CAS  PubMed  Google Scholar 

  • Stojanovic M, Germain M, Nguyen M, Shore GC (2005) BAP31 and its caspase cleavage product regulate cell surface expression of tetraspanins and integrin-mediated cell survival. J Biol Chem 280(34):30018–30024

    Article  CAS  PubMed  Google Scholar 

  • Szklarczyk D, Gable AL, Lyon D, Junge A, Wyder S, Huerta-Cepas J, Simonovic M, Doncheva NT, Morris JH, Bork P, Jensen LJ (2019) STRING v11: protein–protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res 47(D1):D607–D613

    Article  CAS  PubMed  Google Scholar 

  • Tato CM, Hunter CA (2002) Host-pathogen interactions: subversion and utilization of the NF-κB pathway during infection. Infect Immun 70(7):3311–3317

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Terán LC, Distefano M, Bellich B, Petrosino S, Bertoncin P, Cescutti P, Sblattero D (2020) Proteomic studies of the biofilm matrix including outer membrane vesicles of Burkholderia multivorans C1576, a strain of clinical importance for cystic fibrosis. Microorganisms 8(11):1826

    Article  PubMed  PubMed Central  Google Scholar 

  • Teufel F, Almagro Armenteros JJ, Johansen AR, Gíslason MH, Pihl SI, Tsirigos KD, Winther O, Brunak S, von Heijne G, Nielsen H (2022) SignalP 6.0 predicts all five types of signal peptides using protein language models. Nat Biotechnol 40(7):1023–1025

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trost M, Wehmhöner D, Kärst U, Dieterich G, Wehland J, Jänsch L (2005) Comparative proteome analysis of secretory proteins from pathogenic and nonpathogenic Listeria species. Proteomics 5(6):1544–1557

    Article  CAS  PubMed  Google Scholar 

  • Tunio SA, Oldfield NJ, Ala'Aldeen DA, Wooldridge KG, Turner DP (2010) The role of glyceraldehyde 3-phosphate dehydrogenase (GapA-1) in Neisseria meningitidis adherence to human cells. BMC Microbiol 10:280

    Article  PubMed  PubMed Central  Google Scholar 

  • Ulett GC, Maclean KH, Nekkalapu S, Cleveland JL, Adderson EE (2005) Mechanisms of group B streptococcal-induced apoptosis of murine macrophages. J Immunol 175(4):2555–2562

    Article  CAS  PubMed  Google Scholar 

  • Vaca DJ, Thibau A, Schütz M, Kraiczy P, Happonen L, Malmström J, Kempf VA (2020) Interaction with the host: the role of fibronectin and extracellular matrix proteins in the adhesion of Gram-negative bacteria. Med Microbiol Immunol 209(3):277–299

    Article  CAS  PubMed  Google Scholar 

  • Van den Bossche S, Vandeplassche E, Ostyn L, Coenye T, Crabbé A (2020) Bacterial interference with lactate dehydrogenase assay leads to an underestimation of cytotoxicity. Front Cell Infect Microbiol 10:494

    Article  PubMed  PubMed Central  Google Scholar 

  • Welling GW, Weijer WJ, van der Zee R, Welling-Wester S (1985) Prediction of sequential antigenic regions in proteins. FEBS Lett 188(2):215–218

    Article  CAS  PubMed  Google Scholar 

  • Wilhelm E, Kornete M, Targat B, Vigneault-Edwards J, Frontini M, Tora L, Benecke A, Bell B (2010) TAF6δ orchestrates an apoptotic transcriptome profile and interacts functionally with p53. BMC Mol Biol 11(1):1–15

    Article  Google Scholar 

  • Yu CS, Chen YC, Lu CH, Hwang JK (2006) Prediction of protein subcellular localization. Proteins 64(3):643–651

    Article  CAS  PubMed  Google Scholar 

  • Zhang L, Orth K (2013) Virulence determinants for Vibrio parahaemolyticus infection. Curr Opin Microbiol 16(1):70–77

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors are grateful to Dr. Praveen Maurye, Scientist, ICAR-Central Inland Fisheries Research Institute, Barrackpore, Kolkata, for providing laboratory support and guidance for 2D Gel Electrophoresis. The authors express their gratitude to Dr. Satabdi Ganguly, ICAR-CIFRI, Barrackpore for reviewing the manuscript and providing valuable suggestions that contributed to its improvement.

Author information

Authors and Affiliations

  1. Aquatic Environmental Biotechnology and Nanotechnology Division, ICAR-Central Inland Fisheries Research Institute, Barrackpore, Kolkata, West Bengal, 700120, India

    Prasenjit Paria, Hirak Jyoti Chakraborty, Manoharmayum Shaya Devi & Bijay Kumar Behera

  2. Vidyasagar University, Midnapur, West Bengal, 721102, India

    Prasenjit Paria

  3. Department of Zoology, Vivekananda Mahavidyalaya, Hooghly, West Bengal, 712405, India

    Abhijit Pakhira

  4. Department of Microbiology, Raiganj University, Uttar Dinajpur, Raiganj, West Bengal, 733134, India

    Pradeep Kumar Das Mohapatra

Authors
  1. Prasenjit Paria
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hirak Jyoti Chakraborty
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Abhijit Pakhira
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Manoharmayum Shaya Devi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Pradeep Kumar Das Mohapatra
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Bijay Kumar Behera
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Prasenjit Paria: conceptualization, data curation, formal analysis, writing—original draft, methodology, investigation; Hirak Jyoti Chakraborty: formal analysis, investigation, methodology; Abhijit Pakhira: writing—original draft, formal analysis, investigation; Manoharmayum Shaya Devi: formal analysis, writing—review and editing; Pradeep Kumar Das Mohapatra: conceptualization, supervision, writing—review and editing. Bijay Kumar Behera: supervision, funding acquisition, review and editing

Corresponding author

Correspondence to Bijay Kumar Behera.

Ethics declarations

Ethics approval

This article does not contain any studies with human participants or live vertebrates and/or higher invertebrates.

Consent to participate

Not applicable

Consent for publication

All authors have provided their consent for the publication of this manuscript.

Institutional review board statement

Not applicable.

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

ESM 1

(XLSX 13 kb)

ESM 2

(XLS 25 kb)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Paria, P., Chakraborty, H.J., Pakhira, A. et al. Identification of virulence-associated factors in Vibrio parahaemolyticus with special reference to moonlighting protein: a secretomics study. Int Microbiol (2023). https://doi.org/10.1007/s10123-023-00429-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10123-023-00429-y

Keywords

Search

Navigation