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Molecular characterization and in-depth genomic analysis to unravel the pathogenic features of an environmental isolate Enterobacter sp. S-33

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Abstract

Enterobacter species represent widely distributed opportunistic pathogens, commonly associated with plants and humans. In the present study, we performed a detailed molecular characterization as well as genomic study of a type VI secretion system (T6SS) bacterium belonging to member of the family Enterobacteriaceae and named Enterobacter sp. S-33. The comparative sequence analysis of the 16S rRNA gene showed that the strain was closely related to other Enterobacter species. The complete genome of the strain with a genome size of 4.6 Mbp and GC-content of 55.63% was obtained through high-quality sequencing. The genomic analysis with online tools unravelled the various genes belonging to the bacterial secretion system, antibiotic resistance, virulence, efflux pumps, etc. The isolate showed the motility behavior that contributes to Enterobacter persistence in a stressed environment and further supports infections. PCR amplification and further sequencing confirmed the presence of drug-efflux genes acrA, acrB, and outer membrane genes, viz. OmpA, OmpC, and OmpF. The cell surface hydrophobicity and co-aggregation assay against different bacterial strains illustrated its putative pathogenic nature. Genome mining identified various biosynthetic gene clusters (BGCs) corresponding to non-ribosomal proteins (NRPS), siderophore, and arylpolyene production. Briefly, genome sequencing and detailed characterization of environmental Enterobacter isolate will assist in understanding the epidemiology of Enterobacter species, and the further prevention and treatment of infectious diseases caused by these broad-host range species.

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Data availability

The datasets generated during and/or analyzed during the current study are available in the manuscript and from the corresponding author on reasonable request.

References

  • Abby SS, Rocha EP (2012) The non-flagellar type III secretion system evolved from the bacterial flagellum and diversified into host cell adapted systems. PLoS Genet 8:e1002983

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Abedinzadeh A, Falahi Charkhabi N, Aeini M, Amani M (2023) Enterobacter species, emerging plant-pathogenic bacteria, associated with decline and offshoot rot of date palm in Iran. Eur J Plant Pathol 166:341–351

    Article  CAS  Google Scholar 

  • Akbari M, Bakhshi B, Najar Peerayeh S (2016) Particular distribution of Enterobacter cloacae strains isolated from urinary tract infection within clonal complexes. Iran Biomed J 20:49–55

    PubMed  PubMed Central  Google Scholar 

  • Alikhan NF et al (2011) BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons. BMC Genom 12:402

    Article  CAS  Google Scholar 

  • Anastay M, Lagier E, Blanc V, Chardon H (2013) Epidémiologie des bêtalactamases à spectre étendu (BLSE) chez les entérobactéries dans un hôpital du sud de la France, 1997–2007. Pathol Biol 61:38–43

    Article  CAS  PubMed  Google Scholar 

  • Andrés-Barrao C, Saad MM, Cabello Ferrete E, Bravo D, Chappuis ML, Ortega Pérez R et al (2016) Metaproteomics and ultrastructure characterization of Komagataeibacter spp. involved in high-acid spirit vinegar production. Food Microbiol 55:112–122

    Article  PubMed  Google Scholar 

  • Andrews S (2010) FASTQC. A quality control tool for high throughput sequence data. Available online at: http://www.bioinformatics.babraham.ac.uk/projects/fastqc

  • Asaf S, Numan M, Khan AL et al (2020) Sphingomonas: from diversity and genomics to functional role in environmental remediation and plant growth. Crit Rev Biotechnol 40:138–152

    Article  CAS  PubMed  Google Scholar 

  • Bailey DC, Alexander E, Rice MR, Drake EJ, Mydy LS, Aldrich CC, Gulick AM (2018) Structural and functional delineation of aerobactin biosynthesis in hypervirulent Klebsiella pneumoniae. J Biol Chem 293(20):7841–7852

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Basler M, Pilhofer M, Henderson PG, Jensen JG, Mekalanos J (2012) Type VI secretion requires a dynamic contractile phage tail-like structure. Nature 483:182–186

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blair JMA, Webber MA, Baylay AJ, Ogbolu DO, Piddock LJV (2015) Molecular mechanisms of antibiotic resistance. Nat Rev Microbiol 13:42–51

    Article  CAS  PubMed  Google Scholar 

  • Blin K et al (2019) antiSMASH 5.0: updates to the secondary metabolite genome mining pipeline. Nucleic Acids Res 47:W81–W87

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boutarfi Z, Rebiahi SA, Morghad T, Pulido RP, Burgos MJ, Mahdi F, Lucas R, Galvez A (2019) Biocide tolerance and antibiotic resistance of Enterobacter spp. isolated from the Algerian hospital environment. J Glob Antimicrob Resist 18:291–297

  • Buchfink B, Xie C, Huson DH (2015) Fast and sensitive protein alignment using DIAMOND. Nat Methods 12(1):59–60

    Article  CAS  PubMed  Google Scholar 

  • Busscher HJ, Van der Mei HC (2012) How do bacteria know they are on a surface and regulate their response to an adhering state? PLoS Pathog 8(1):e1002440

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cascales E, Cambillau C (2012) Structural biology of type VI secretion systems. Philos Trans R Soc Lond Ser B Biol Sci 367:1102–1111

    Article  CAS  Google Scholar 

  • Chassaing B, Cascales E (2018) Antibacterial weapons: targeted destruction in the microbiota. Trends Microbiol 26:329–338

    Article  CAS  PubMed  Google Scholar 

  • Chen C, Yang X, Shen X (2019) Confirmed and potential roles of bacterial T6SSs in the intestinal ecosystem. Front Microbiol 10:1484

    Article  PubMed  PubMed Central  Google Scholar 

  • Clinical and Laboratory Standards Institute (CLSI) (2012) Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically; approved standard, seventh edn. CLSI; CLSI document, Wayne, pp M07–MA7

    Google Scholar 

  • Collado MC, Meriluoto J, Salminen S (2008) Adhesion and aggregation properties of probiotic and pathogen strains. Eur Food Res Technol 226:1065–1073

    Article  CAS  Google Scholar 

  • Confer AW, Ayalew S (2013) The OmpA family of proteins: roles in bacterial pathogenesis and immunity. Vet Microbiol 163:207–222

    Article  CAS  PubMed  Google Scholar 

  • Coulthurst S (2019) The Type VI secretion system: a versatile bacterial weapon. Microbiology 165:503–515

    Article  CAS  PubMed  Google Scholar 

  • Davin-Regli A, Lavigne JP, Pagès JM (2019) Enterobacter spp.: update on taxonomy, clinical aspects, and emerging antimicrobial resistance. Clin Microbiol Rev 32(4):e00002–19

  • Davin-Regli A, Pagès JM (2015) Enterobacter aerogenes and Enterobacter cloacae; versatile bacterial pathogens confronting antibiotic treatment. Front Microbiol 6:392

    Article  PubMed  PubMed Central  Google Scholar 

  • de Kort G, Bolton A, Martin G, Stephen J, van de Klundert JAM (1994) Invasion of rabbit ileal tissue by Enterobacter cloacae varies with the concentration of OmpX in the outer membrane. Infect Immun 62:4722–4726

    Article  PubMed  PubMed Central  Google Scholar 

  • Delepelaire P (2004) Type I secretion in Gram-negative bacteria. Biomembranes 1694:149–161

    CAS  Google Scholar 

  • Dillon JK, Fuerst JA, Hayward AC, Davis GHG (1986) A comparison of five methods for assaying bacterial hydrophobicity. J Microbiol Methods 6:13–19

    Article  CAS  Google Scholar 

  • Douzi B, Logger L, Spinelli S, Blangy S, Cambillau C, Cascales E (2018) Structure-function analysis of the C-terminal domain of the type VI secretion TssB tail sheath subunit. J Mol Biol 430:297–309

    Article  CAS  PubMed  Google Scholar 

  • Dupont M, De E, Chollet R, Chevalier J, Pages JM (2004) Enterobacter aerogenes OmpX, a cation-selective channel mar- and osmoregulated. FEBS Lett 569:27–30

    Article  CAS  PubMed  Google Scholar 

  • Fernández L, Hancock REW (2012) Adaptive and mutational resistance: role of porins and efflux pumps in drug resistance. Clin Microbiol Rev 25:661–681

    Article  PubMed  PubMed Central  Google Scholar 

  • Gallique M, Decoin V, Barbey C, Rosay T, Feuilloley MG, Orange N et al (2017) Contribution of the Pseudomonas fluorescens MFE01 Type VI secretion system to biofilm formation. PLoS One 12:e0170770

    Article  PubMed  PubMed Central  Google Scholar 

  • García-González T, Sáenz-Hidalgo HK, Silva-Rojas HV, Morales-Nieto C, Vancheva T, Koebnik R, Ávila-Quezada GD (2018) Enterobacter cloacae, an emerging plant-pathogenic bacterium affecting chili pepper seedlings. Plant Pathol J 34:1–10

    Article  PubMed  PubMed Central  Google Scholar 

  • Gilmour MW, Graham M, Reimer A, Van Domselaar G (2013) Public health genomics and the new molecular epidemiology of bacterial pathogens. Public Health Genom 16:25–30

    Article  CAS  Google Scholar 

  • Green ER, Mecsas J (2016) Bacterial secretion systems: an overview. Microbiol Spect 4:1

    Article  CAS  Google Scholar 

  • Gulick AM (2017) Nonribosomal peptide synthetase biosynthetic clusters of ESKAPE pathogens. Nat Prod Rep 34:981–1009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Habimana O, Semião AJC, Casey E (2014) The role of cell-surface interactions in bacterial initial adhesion and consequent biofilm formation on nanofiltration/reverse osmosis membranes. J Membr Sci 454:82–96

    Article  CAS  Google Scholar 

  • Haiko J, Wikström BW (2013) The role of the bacterial flagellum in adhesion and virulence. MDPI Biology 2:1242–1267

    Google Scholar 

  • Harley JP, Prescott LM (2002) Laboratory exercises in microbiology, 5th edn. Mc Graw Hill, New York 65-64

    Google Scholar 

  • Hejair HMA, Zhu Y, Ma J, Zhang Y, Pan Z, Zhang W et al (2017) Microbial pathogenesis functional role of ompF and ompC porins in pathogenesis of avian pathogenic Escherichia coli. Microb Pathog 107:29–37

    Article  CAS  PubMed  Google Scholar 

  • Iredell J, Brown J, Tagg K (2016) Antibiotic resistance in Enterobacteriaceae: mechanisms and clinical implications. Bmj 352:h6420

    Article  PubMed  Google Scholar 

  • Jana TK, Srivastava AK, Csery K, Arora DK (1999) Influence of growth and environmental conditions on cell surface hydrophobicity of Pseudomonas fluorescens in non-specific adhesion. Can J Microbiol 46:28–37

    Article  Google Scholar 

  • Journet L, Cascales E (2016) The type VI secretion system in Escherichia coli and related species. Eco Sal Plus 7:1–20

    Google Scholar 

  • Khan S, Paravastu P, Marathe SA (2020) Elucidating the pathogenic potential of Enterobacter cloacae SBP-8 using Caenorhabditis elegans as a model host. Microb Pathog 148:104449

    Article  CAS  PubMed  Google Scholar 

  • Kim KK, Choi J, Lim J, Lee J, Hwang S et al (2010) Outer membrane proteins A (OmpA) and X (OmpX) are essential for basolateral invasion of Cronobacter sakazakii. Appl Environ Microbiol 76:5188–5198

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumari K, Rawat V, Shadan A, Sharma PK, Deb S, Singh RP (2023) In-depth genome and pan-genome analysis of a metal-resistant bacterium Pseudomonas parafulva OS-1. Front Microbiol 14:1140249

    Article  PubMed  PubMed Central  Google Scholar 

  • Lalucat J, Mulet M, Gomila M, Elena García-Valdés E (2020) Genomics in bacterial taxonomy: impact on the genus Pseudomonas. Genes 11:139

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Mandelco L, Wiegel J (1993) Isolation and characterization of a moderately thermophilic anaerobic alkaliphile, Clostridium paradoxum sp. nov. Int J Syst Bacteriol 43:450–460

    Article  Google Scholar 

  • Lin J, Huang S, Zhang Q (2002) Outer membrane proteins: key players for bacterial adaptation in host niches. Microbes Infect 4(3):325–331

    Article  CAS  PubMed  Google Scholar 

  • Lloyd DH (2007) Reservoirs of antimicrobial resistance in pet animals. Clin Infect Dis 45:S148–S152

    Article  PubMed  Google Scholar 

  • Magdalena J et al (2002) 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maurelli AT (2007) Black holes, antivirulence genes, and gene inactivation in the evolution of bacterial pathogens. FEMS Microbiol Lett 267(1):1–8

    Article  CAS  PubMed  Google Scholar 

  • Mcarthur AG, Waglechner N, Nizam F et al (2013) The comprehensive antibiotic resistance database. Antimicrob Agents Chemother 57:3348–3357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mezzatesta ML, Gona F, Stefani S (2012) Enterobacter cloacae complex: clinical impact and emerging antibiotic resistance. Future Microbiol 7:887–902

    Article  CAS  PubMed  Google Scholar 

  • Mishra M, Panda S, Barik S, Sarkar A, Singh DV, Mohapatra H (2020) Antibiotic resistance profile, outer membrane proteins, virulence factors and genome sequence analysis reveal clinical isolates of Enterobacter are potential pathogens compared to environmental isolates. Front Cell Infect Microbiol 21(10):54

    Article  Google Scholar 

  • Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M (2007) KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res 35:W182–W185

    Article  PubMed  PubMed Central  Google Scholar 

  • Nishino K, Nikaido E, Yamaguchi A (2009) Regulation and physiological function of multidrug efflux pumps in Escherichia coli and Salmonella. Biochim Biophys Acta 1794:834–843

    Article  CAS  PubMed  Google Scholar 

  • Paauw A et al (2008) Genomic diversity within the Enterobacter cloacae complex. PLoS One 3:e301

    Article  Google Scholar 

  • Pagès JM, James CE, Winterhalter M (2008) The porin and the permeating antibiotic: a selective diffusion barrier in Gram-negative bacteria. Nat Rev Microbiol 6:893–903

    Article  PubMed  Google Scholar 

  • Pan M, Kumaree KK, Shah NP (2017) Physiological changes of surface membrane in Lactobacillus with pebiotics. J Food Sci 82:3

    Article  Google Scholar 

  • Records AR (2011) The type VI secretion system: a multipurpose delivery system with a phage-like machinery. Mol Plant-Microbe Interact 24:751–757

    Article  CAS  PubMed  Google Scholar 

  • Ren Y, Zhou Z, Guo X, Li Y, Feng L, Wang L (2010) Complete genome sequence of Enterobacter cloacae subsp. cloacae Type strain ATCC 13047. J Bacteriol 192:2463–2464

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Repizo GD, Gagne S, Foucault-Grunenwald ML et al (2015) Differential role of the T6SS in Acinetobacter baumannii virulence. PLoS One 10:e0138265

    Article  PubMed  PubMed Central  Google Scholar 

  • Rozwandowicz M, Brouwer MSM, Fischer J, Wagenaar JA, Gonzalez-Zorn B, Guerra B, Mevius DJ, Hordijk J (2018) Plasmids carrying antimicrobial resistance genes in Enterobacteriaceae. J Antimicrob Chemother 73:1121–1137

    Article  CAS  PubMed  Google Scholar 

  • Russell AB, LeRoux M, Hathazi K, Agnello DM, Ishikawa T, Wiggins PA et al (2013) Diverse type VI secretion phospholipases are functionally plastic antibacterial effectors. Nature 496:508–512

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Russell AB, Wexler AG, Harding BN, Whitney JC, Bohn AJ, Goo YA et al (2014) A type VI secretion-related pathway in Bacteroidetes mediates interbacterial antagonism. Cell Host Microbe 16:227–236

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sato Y, Unno Y, Kawakami S, Ubagai T, Ono Y (2017) Virulence characteristics of Acinetobacter baumannii clinical isolates vary with the expression levels of omps. J Med Microbiol 66:203–212

    Article  PubMed  Google Scholar 

  • Seemann T (2014) Prokka: rapid prokaryotic genome annotation. Bioinformatics 15(30):2068–2069

    Article  Google Scholar 

  • Silverman JM, Brunet YR, Cascales E, Mougous JD (2012) Structure and regulation of the type VI secretion system. Annu Rev Microbiol 66:453–72

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh RP, Jha P, Jha PN (2015) The plant-growth-promoting bacterium Klebsiella sp. SBP-8 confers induced systemic tolerance in wheat (Triticum aestivum) under salt stress. J Plant Physiol 20:57–67

    Article  Google Scholar 

  • Singh RP, Nalwaya S, Jha PN (2017) The draft genome sequence of the plant growth promoting rhizospheric bacterium Enterobacter cloacae SBP-8. Genome Data 12:81–83

    Article  Google Scholar 

  • Song S, Hwang S, Lee S, Ha N-C, Lee K (2014) Interaction mediated by the putative tip regions of MdsA and MdsC in the formation of a Salmonella-specific tripartite efflux pump. PLoS One 9:e100881

    Article  PubMed  PubMed Central  Google Scholar 

  • Soria-Bustos J, Ares MA, Gómez-Aldapa CA, González-y-Merchand JA, Girón JA, Cruz MA (2020) Two Type VI secretion systems of Enterobacter cloacae are required for bacterial competition, cell adherence, and intestinal colonization. Front Microbiol 11:560488

    Article  PubMed  PubMed Central  Google Scholar 

  • Steinke K, Mohite OS, Weber T, Kovacs AT (2021) Phylogenetic distribution of secondary metabolites in the Bacillus subtilis species complex. mSystems 6:e00057–e00021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun J, Deng Z, Yan A (2014) Bacterial multidrug efflux pumps: mechanisms, physiology and pharmacological exploitations. Biochem Biophys Res Commun 453:254–267

    Article  CAS  PubMed  Google Scholar 

  • Villa J, Viedma E, Otero JR, Chaves F (2013) Draft whole-genome sequence of VIM-1- producing multidrug-resistant Enterobacter cloacae EC_38VIM1. Genome Announc 1:e00694–e00613

    Article  PubMed  PubMed Central  Google Scholar 

  • Viveiros M, Dupont M, Rodrigues L, Couto I, Davin-Regli A, Martins M et al (2007) Antibiotic stress, genetic response and altered permeability of E. coli. PLoS One 2:e365

    Article  PubMed  PubMed Central  Google Scholar 

  • Vot DE, Broederdorf LJ, Graham JG (2012) Bacterial type IV secretion systems: versatile virulence machines. Future Microbiol 7:241–257

    Article  Google Scholar 

  • Wang J, Brodmann M, Basler M (2019) Assembly and subcellular localization of bacterial type VI secretion systems. Annu Rev Microbiol 73:621–638

    Article  CAS  PubMed  Google Scholar 

  • Xu L et al (2019) OrthoVenn2: a web server for whole-genome comparison and annotation of orthologous clusters across multiple species. Nucleic Acids Res 47:W52–W58

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu X, Liu W, Tian S, Wang W, Qi Q, Jiang P, Gao X, Li F, Li H, Yu H (2018) Petroleum hydrocarbon-degrading bacteria for the remediation of oil pollution under aerobic conditions: a perspective analysis. Front Microbiol 3(9):2885

    Article  Google Scholar 

  • Zhong C, Zhang C, Fu J, Chen W, Jiang T, Cao G (2017) Complete genome sequence of Enterobacter cloacae R11 reveals multiple genes potentially associated with high-level polymyxin E resistance. Can J Microbiol. https://doi.org/10.1139/cjm-2017-0475

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Acknowledgements

The author acknowledges the Dept. of Biotechnology, Jaypee Institute of Information Technology, Noida, India, for providing the infrastructure.

Funding

The work was supported by the Ramalingaswami grant provided by Department of Biotechnology, Government of India (BT/RLF/2020-21).

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  1. Department of Bioengineering and Biotechnology, Birla Institute of Technology, Mesra, Ranchi, Jharkhand, 835215, India

    Kiran Kumari & Yogender Aggarwal

  2. Department of Biotechnology, Jaypee Institute of Information Technology, Noida, India

    Rajnish Prakash Singh

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  1. Kiran Kumari
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K.K. analyzed the data. Y.A. helped in the interpretation of data and editing of manuscript. R.P.S. designed the work and wrote the manuscript. All authors reviewed the manuscript.

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Correspondence to Rajnish Prakash Singh.

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Supplementary S1 The 16S rRNA gene sequence of S-33 was compared to type strains of the genus Enterobacter available at EzBioCloud database for the phylogenetic analysis. Tree was inferred with MEGA 7.0 tool. Supplementary S2 The efflux gene acrA and acrB amplification in Enterobacter sp. S-33. Supplementary S3 a The cell surface hydrophobicity of Enterobacter sp. S-33 was evaluated in different solvents like Hexane, Hexadecane, Toluene, Xylene; b The co-aggregation was analyzed against different bacteria like B. subtilis, S. aureus, E. coli and S. typhi. Supplementary S4 Comparison of the cluster of orthologous groups (COGs) in five Enterobacter species. The numbers in overlapped regions of Venn diagram represent CDS numbers shared by the tested genomes. The analysis was done by using Orthovenn2 using default parameters with protein sequences of Enterobacter sp. S-33, E. mori LMG 25706, E. cancerogenus ATCC 35316, E. cloacae ATCC 13047 and E. cloacae GS1. Supplementary S5 Phylogenetic analysis of Enterobacter sp. S-33 based on whole genome sequences. Tree was inferred with FastME 2.1.6.1 from the Genome Blast Distance Phylogeny (GBDP) distances calculated from whole-genome sequences. The branch lengths are scaled in terms of GBDP distance formula d5. The numbers above branches are GBDP pseudo-bootstrap support values >60% from 100 replications, with an average branch support of 92.3%. The different parameters such as species and subspecies cluster, GC-percentage, genome size, and protein count were considered during phylogram construction and comparison with other Enterobacter species. Supplementary S6 A Schematic representation of identified putative BGCs in S-33 genome identified using antiSMASH server; B; The gene clusters showed the homology to nonribosomal polypeptides (NRPS) C; aerobactin like siderophores, and D arylpolyenes. Supplementary S7 Schematic representation of different drug class and identified gene numbers in each class by Comprehensive Antibiotic Resistance Database (CARD) database. Supplementary S8 The genome comparison of Enterobacter sp. S-33 was performed against reference genome E. vonholyi, E. roggenkakampii, E. quasiroggen kampii, and E. asburiae using Bio Ring Image Generator (BRIG) Tool. Supplementary S9 The comparison of virulence factors in the selected genome of Enterobacter sp. S-33, E. mori LMG 25706, E. cancerogenus ATCC 35316, E. cloacae ATCC 13047, and E. cloacae GS1 (DOCX 3411 kb)

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Kumari, K., Aggarwal, Y. & Singh, R.P. Molecular characterization and in-depth genomic analysis to unravel the pathogenic features of an environmental isolate Enterobacter sp. S-33. Int Microbiol (2023). https://doi.org/10.1007/s10123-023-00461-y

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