Genome-wide Analysis of Four Enterobacter cloacae complex type strains: Insights into Virulence and Niche Adaptation.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
18 05 2020
18 05 2020
Historique:
received:
13
12
2019
accepted:
23
04
2020
entrez:
20
5
2020
pubmed:
20
5
2020
medline:
15
12
2020
Statut:
epublish
Résumé
Enterobacter cloacae complex (Ecc) species are widely distributed opportunistic pathogens mainly associated with humans and plants. In this study, the genomes of clinical isolates including E. hormaechei, E. kobei, and E. ludwigii and non-clinical isolate including E. nimipressuralis were analysed in combination with the genome of E. asburiae by using the reference strain E. cloacae subsp. cloacae ATCC 13047; the Ecc strains were tested on artificial sputum media (ASM), which mimics the host, to evaluate T6SS genes as a case study. All five Ecc strains were sequenced in our lab. Comparative genome analysis of the Ecc strains revealed that genes associated with the survival of Ecc strains, including genes of metal-requiring proteins, defence-associated genes and genes associated with general physiology, were highly conserved in the genomes. However, the genes involved in virulence and drug resistance, specifically those involved in bacterial secretion, host determination and colonization of different strains, were present in different genomic regions. For example, T6SS accessory and core components, T4SS, and multidrug resistance genes/efflux system genes seemed vital for the survival of Ecc strains in various environmental niches, such as humans and plants. Moreover, the ASM host-mimicking growth medium revealed significantly high expression of T6SS genes, including PrpC, which is a regulatory gene of the T6SS, in all tested Ecc strains compared to the control medium. The variations in T6SS gene expression in ASM vs. control showed that the ASM system represents a simple, reproducible and economical alternative to animal models for studies such as those aimed at understanding the divergence of Ecc populations. In summary, genome sequencing of clinical and environmental Ecc genomes will assist in understanding the epidemiology of Ecc strains, including the isolation, virulence characteristics, prevention and treatment of infectious disease caused by these broad-host-range niche-associated species.
Identifiants
pubmed: 32424332
doi: 10.1038/s41598-020-65001-4
pii: 10.1038/s41598-020-65001-4
pmc: PMC7235008
doi:
Substances chimiques
Bacterial Proteins
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
8150Références
Hormaeche, E. & Edwards, P. R. Observations on the genus Aerobacter with a description of two species. Int. Bull. Bacteriol. Nomen. Taxon. 8, 111–116 (1958).
Paauw, A. et al. Genomic diversity within the Enterobacter cloacae complex. Plos one 3, e301 (2008).
doi: 10.1371/journal.pone.0003018
Streit, J. M., Jones, R. N., Sader, H. S. & Fritsche, T. R. Assessment of pathogen occurrences and resistance profiles among infected patients in the intensive care unit: report from the sentry Antimicrobial Surveillance Program (North America, 2001). Int. J. Ant. Agen. 24, 111–118 (2004).
Harbarth, S., Sudre, P., Dharan, S., Cadenas, M. & Pittet, D. Outbreak of Enterobacter cloacae related to understaffing, overcrowding, and poor hygiene practices. Inf. Con. Hos. Epid. 20, 598–603 (1999).
doi: 10.1086/501677
Ren, Y. et al. Complete genome sequence of Enterobacter cloacae subsp. cloacae Type strain ATCC 13047. J. Bact. 192, 2463–2464 (2010).
pubmed: 20207761
doi: 10.1128/JB.00067-10
Garcia-Gonzalez, T. et al. Enterobacter cloacae, an emerging plant-pathogenic bacterium affecting chili pepper seedlings. Plant Pathol. J. 34, 1–10 (2018).
pubmed: 29422783
pmcid: 5796745
Harada, K. et al. Phenotypic and molecular characterization of antimicrobial resistance in Enterobacter spp. isolates from companion animals in Japan. Plos One. 12, e0174178 (2017).
pubmed: 28328967
pmcid: 5362103
doi: 10.1371/journal.pone.0174178
Zhu, B., Li, O., Hussain, A. & Ibrahim, M. High quality genome sequence of human pathogen Enterobacter asburiae type strain 1497 78T. J. Glob. Antimicrob. Resist. 8, 104–105 (2017).
pubmed: 28082144
doi: 10.1016/j.jgar.2016.12.003
Mezzatesta, M. L., Gona, F. & Stefani, S. Enterobacter cloacae complex: clinical impact and emerging antibiotic resistance. Future Microbiol. 7, 887–902 (2012).
pubmed: 22827309
doi: 10.2217/fmb.12.61
Hoffmann, H. & Roggenkamp, A. Population Genetics of the Nomenspecies Enterobacter cloacae. Appl. Env. Microbiol. 69, 5306–5318 (2003).
doi: 10.1128/AEM.69.9.5306-5318.2003
Singh, T. et al. Transcriptome analysis of beta-lactamase genes in diarrheagenic Escherichia coli. Sci. Rep. 9, 3626 (2019).
pubmed: 30842518
pmcid: 6403342
doi: 10.1038/s41598-019-40279-1
Wood, J. M. Bacterial responses to osmotic challenges. J. Gen. Physiol. 145, 381–388 (2015).
pubmed: 25870209
pmcid: 4411257
doi: 10.1085/jgp.201411296
Green, E. R. & Mecsas, J. Bacterial secretion systems: an overview. Microbiol. Spect. 4, 1 (2016).
Kirzinger, M. W., Nadarasah, G. & Stavrinides, J. Insights into cross-kingdom plant pathogenic bacteria. Genes. 2, 980–997 (2011).
pubmed: 24710301
pmcid: 3927606
doi: 10.3390/genes2040980
Costa, T. R., Felisberto, R. C., Meir, A., Prevost, M. S. & Redzej, A. Secretion systems in Gram-negative bacteria: structural and mechanistic insights. Nat. Rev. Microbiol. 13, 343–59 (2015).
pubmed: 25978706
doi: 10.1038/nrmicro3456
pmcid: 25978706
Delepelaire, P. Type I secretion in Gram-negative bacteria. Biomembranes. 1694, 149–161 (2004).
Nivaskumar, M. & Francetic, O. Type II secretion system: a magic beanstalk or a protein escalator. Mol. Cell Res. 1843, 1568–1577 (2014).
Rondelet, A. & Condemine, G. Type II secretion: the substrates that won’t go away. Res. Microbiol. 164, 556–561 (2013).
pubmed: 23538405
doi: 10.1016/j.resmic.2013.03.005
Holland, I. B., Schmitt, L. & Young, J. Type 1 protein secretion in bacteria, the ABC-transporter dependent pathway. Mol. Membr. Biol. 22, 29–39 (2005).
pubmed: 16092522
doi: 10.1080/09687860500042013
Minamino, T. & Namba, K. Distinct roles of the FliI ATPase and proton motive force in bacterial flagellar protein export. Nature. 451, 485–488 (2008).
pubmed: 18216858
doi: 10.1038/nature06449
Magdalena, J. et al. Spa32 regulates a switch in substrate specificity of the type III secretion of Shigella flexneri from needle components to Ipa proteins. J. Bacteriol. 184, 3433–3441 (2002).
pubmed: 12057936
pmcid: 135143
doi: 10.1128/JB.184.13.3433-3441.2002
Abby, S. S. & Rocha, E. P. The non-flagellar type III secretion system evolved from the bacterial flagellum and diversified into host-cell adapted systems. PLoS Gen. 8, e1002983 (2012).
doi: 10.1371/journal.pgen.1002983
Voth, D. E., Broederdorf, L. J. & Graham, J. G. Bacterial type IV secretion systems: versatile virulence machines. Future Microbiol. 7, 241–257 (2012).
pubmed: 22324993
pmcid: 3563059
doi: 10.2217/fmb.11.150
Wallden, K., Rivera-Calzada, A. & Waksman, G. Type IV secretion systems: versatility and diversity in function. Cell Microbiol. 12, 1203–1212 (2010).
pubmed: 20642798
pmcid: 3070162
doi: 10.1111/j.1462-5822.2010.01499.x
Records, A. R. The type VI secretion system: a multipurpose delivery system with a phage-like machinery. Mol. Plant Microbe. Interact. 24, 751–757 (2011).
pubmed: 21361789
doi: 10.1094/MPMI-11-10-0262
Esser, D. et al. Protein phosphorylation and its role in archaeal signal transduction. FEMS Microbiol. Rev. 40, 625–647 (2016).
pubmed: 27476079
pmcid: 5007285
doi: 10.1093/femsre/fuw020
Blair, J. M., Webber, M. A., Baylay, A. J., Ogbolu, D. O. & Piddock, L. J. Molecular mechanisms of antibiotic resistance. Nat. Rev. Microbiol. 13, 42–51 (2015).
pubmed: 25435309
doi: 10.1038/nrmicro3380
Peng, P. et al. Roles of Hcp family proteins in the pathogenesis of the porcine extra intestinal pathogenic Escherichia coli type VI secretion system. Sci. Rep. 6, 26816 (2016).
pubmed: 27229766
pmcid: 4882540
doi: 10.1038/srep26816
Suzuki, S., Horinouchi, T. & Furusawa, C. Prediction of antibiotic resistance by gene expression profiles. Nat. Commun. 5, 5792 (2014).
pubmed: 25517437
pmcid: 4351646
doi: 10.1038/ncomms6792
Jousset, A.B. et al. False-positive carbapenem-hydrolyzing confirmatory tests due to ACT-28, a chromosomally-encoded AmpC with weak carbapenemase activity from Enterobacter kobei. Antimicrob. Agents Chemother. 25, 63(5) (2019).
Nazir, F. et al. Genetic Diversity and Functional Analysis of Sigma Factors in Enterobacter cloacae Complex Resourced From Various Niche. Evol. Bioinform. Online 14, 1–6 (2018).
doi: 10.1177/1176934318754878
Overbeek, R., Olson, R., Pusch, G. D., Olsen, G. J. & Davis, J. J. The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST). Nucl. Acids Res. (Database Issue) 42, D206–D214 (2014).
doi: 10.1093/nar/gkt1226
Petersen, T. N., Brunak, S., Von Heijne, G. & Nielsen, H. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat. Methods. 8, 785–786 (2011).
pubmed: 21959131
doi: 10.1038/nmeth.1701
Darling, A. C. E., Mau, B., Blattner, F. R. & Perna, N. T. Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res. 14, 1394–1403 (2004).
pubmed: 15231754
pmcid: 442156
doi: 10.1101/gr.2289704
Stothard, P. & Wishart, D. S. Circular genome visualization and exploration using CGView. BMC Bioinform. 21, 537–539 (2005).
doi: 10.1093/bioinformatics/bti054
Naquin, D. et al. CIRCUS: a package for Circos display of structural genome variations from paired-end and mate-pair sequencing data. BMC Bioinform. 15, 198 (2014).
doi: 10.1186/1471-2105-15-198
Capella-Gutierrez, S., Silla-Martinez, J. M. & Gabaldon, T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 1972–1973 (2009).
pubmed: 19505945
pmcid: 2712344
doi: 10.1093/bioinformatics/btp348
Liu, B. & Pop, M. ARDB-Antibiotic Resistance Genes Database. Nucl. Acid Res. 37, D443–D447 (2009).
doi: 10.1093/nar/gkn656
Chen, L. et al. VFDB: a reference database for bacterial virulence factors. Nucl. Acid Res. 33, D325–D328 (2005).
doi: 10.1093/nar/gki008
Martinez-Garcia, P. M., Ramos, C. & Rodriguez-Palenzuela, P. T346Hunter: A Novel Web-Based Tool for the Prediction of type III, type IV and type VI Secretion Systems in Bacterial Genomes. Plos one. 10, e0119317 (2015).
pubmed: 25867189
pmcid: 4395097
doi: 10.1371/journal.pone.0119317
Li, J. et al. SecReT6: a web-based resource for type VI secretion systems found in bacteria. Plos one. 10, e0119317 (2015).
doi: 10.1371/journal.pone.0119317
Kumar, S., Stecher, G. & Tamura, K. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870–1874 (2016).
doi: 10.1093/molbev/msw054
Lawal, O. et al. BreathDx consortium. TD/GC-MS analysis of volatile markers emitted from mono- and co-cultures of Enterobacter cloacae and Pseudomonas aeruginosa in artificial sputum. Metabolomics. 14, 66 (2018).
pubmed: 29725275
pmcid: 5920131
doi: 10.1007/s11306-018-1357-5