Skip to main content
Log in

Analysis of resistance genes of clinical Pannonibacter phragmitetus strain 31801 by complete genome sequencing

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

A Correction to this article was published on 27 September 2018

This article has been updated

Abstract

To clarify the resistance mechanisms of Pannonibacter phragmitetus 31801, isolated from the blood of a liver abscess patient, at the genomic level, we performed whole genomic sequencing using a PacBio RS II single-molecule real-time long-read sequencer. Bioinformatic analysis of the resulting sequence was then carried out to identify any possible resistance genes. Analyses included Basic Local Alignment Search Tool searches against the Antibiotic Resistance Genes Database, ResFinder analysis of the genome sequence, and Resistance Gene Identifier analysis within the Comprehensive Antibiotic Resistance Database. Prophages, clustered regularly interspaced short palindromic repeats (CRISPR), and other putative virulence factors were also identified using PHAST, CRISPRfinder, and the Virulence Factors Database, respectively. The circular chromosome and single plasmid of P. phragmitetus 31801 contained multiple antibiotic resistance genes, including those coding for three different types of β-lactamase [NPS β-lactamase (EC 3.5.2.6), β-lactamase class C, and a metal-dependent hydrolase of β-lactamase superfamily I]. In addition, genes coding for subunits of several multidrug-resistance efflux pumps were identified, including those targeting macrolides (adeJ, cmeB), tetracycline (acrB, adeAB), fluoroquinolones (acrF, ceoB), and aminoglycosides (acrD, amrB, ceoB, mexY, smeB). However, apart from the tripartite macrolide efflux pump macAB-tolC, the genome did not appear to contain the complete complement of subunit genes required for production of most of the major multidrug-resistance efflux pumps.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Change history

  • 27 September 2018

    Subsequent to publication it has been noticed that the below listed text parts, figures and tables of the above paper were taken from paper

References

  • Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M, Meyer F, Olsen GJ, Olson R, Osterman AL, Overbeek RA, McNeil LK, Paarmann D, Paczian T, Parrello B, Pusch GD, Reich C, Stevens R, Vassieva O, Vonstein V, Wilke A, Zagnitko O (2008) The RAST server: rapid annotations using subsystems technology. BMC Genom 9:75

    Article  Google Scholar 

  • Bandyopadhyay S, Schumann P, Das SK (2013) Pannonibacter indica sp. nov., a highly arsenate-tolerant bacterium isolated from a hot spring in India. Arch Microbiol 195:1–8

    Article  CAS  Google Scholar 

  • Besemer J, Borodovsky M (2005) GeneMark: web software for gene finding in prokaryotes, eukaryotes and viruses. Nucleic Acids Res 33:W451–454

    Article  CAS  Google Scholar 

  • Borsodi AK, Micsinai A, Kovács G, Tóth E, Schumann P, Kovács AL, Böddi B, Márialigeti K (2003) Pannonibacter phragmitetus gen. nov., sp. nov., a novel alkalitolerant bacterium isolated from decomposing reed rhizomes in a Hungarian soda lake. Int J Syst Evol Microbiol 53:555–561

    Article  CAS  Google Scholar 

  • Borsodi AK, Micsinai A, Rusznyák A, Vladár P, Kovács G, Tóth EM, Márialigeti K (2005) Diversity of alkaliphilic and alkalitolerant bacteria cultivated from decomposing reed rhizomes in a Hungarian soda lake. Microb Ecol 50:9–18

    Article  CAS  Google Scholar 

  • Carver T, Harris SR, Berriman M, Parkhill J, McQuillan JA (2012) Artemis: an integrated platform for visualization and analysis of high-throughput sequence-based experimental data. Bioinformatics 28:464–469

    Article  CAS  Google Scholar 

  • Chen L, Xiong Z, Sun L, Yang J, Jin Q (2012) VFDB 2012 update: toward the genetic diversity and molecular evolution of bacterial virulence factors. Nucleic Acids Res 40:D641–645

    Article  CAS  Google Scholar 

  • Coman C, Drugă B, Hegedus A, Sicora C, Dragoş N (2013) Archaeal and bacterial diversity in two hot spring microbial mats from a geothermal region in Romania. Extremophiles 17:523–534

    Article  Google Scholar 

  • Coyne S, Rosenfeld N, Lambert T, Courvalin P, Périchon B (2010) Overexpression of resistance-nodulation-cell division pump AdeFGH confers multidrug resistance in Acinetobacter baumannii. Antimicrob Agents Chemother 54:4389–4393

    Article  CAS  Google Scholar 

  • Coyne S, Courvalin P, Périchon B (2011) Efflux-mediated antibiotic resistance in Acinetobacter spp. Antimicrob Agents Chemother 55:947–953

    Article  CAS  Google Scholar 

  • Damier-Piolle L, Magnet S, Brémont S, Lambert T, Courvalin P (2008) AdeIJK, a resistance-nodulation-cell division pump effluxing multiple antibiotics in Acinetobacter baumannii. Antimicrob Agents Chemother 52:557–562

    Article  CAS  Google Scholar 

  • Delcher AL, Harmon D, Kasif S, White O, Salzberg SL (1999) Improved microbial gene identification with GLIMMER. Nucleic Acids Res 27:4636–4641

    Article  CAS  Google Scholar 

  • Delcher AL, Bratke KA, Powers EC, Salzberg SL (2007) Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics 23:673–679

    Article  CAS  Google Scholar 

  • Galperin MY, Makarova KS, Wolf YI, Koonin EV (2015) Expanded microbial genome coverage and improved protein family annotation in the COG database. Nucleic Acids Res 43:D261–269

    Article  CAS  Google Scholar 

  • Grant JR, Stothard P (2008) The CGView server: a comparative genomics tool for circular genomes. Nucleic Acids Res 36:W181–184

    Article  CAS  Google Scholar 

  • Grissa I, Vergnaud G, Pourcel C (2008) CRISPRcompar: a website to compare clustered regularly interspaced short palindromic repeats. Nucleic Acids Res 36:W145–148

    Article  CAS  Google Scholar 

  • Holmes B, Lapage SP, Malnick H (1975) Strains of Pseudomonas putrefaciens from clinical material. J Clin Pathol 28:149–155

    Article  CAS  Google Scholar 

  • Holmes B, Lewis R, Trevett A (1992) Septicaemia due to Achromobacter group B: a report of two cases. Med Microbiol Lett 1:177–184

    Google Scholar 

  • Holmes B, Moss CW, Daneshvar MI (1993) Cellular fatty acid compositions of “Achromobacter groups B and E”. J Clin Microbiol 31:1007–1008

    CAS  PubMed  PubMed Central  Google Scholar 

  • Holmes B, Segers P, Coenye T, Vancanneyt M, Vandamme P (2006) Pannonibacter phragmitetus, described from a Hungarian soda lake in 2003, had been recognized several decades earlier from human blood cultures as Achromobacter groups B and E. Int J Syst Evol Microbiol 56:2945–2948

    Article  CAS  Google Scholar 

  • Jeannot K, Sobel ML, El Garch F, Poole K, Plésiat P (2005) Induction of the MexXY efflux pump in Pseudomonas aeruginosa is dependent on drug–ribosome interaction. J Bacteriol 187:5341–5346

    Article  CAS  Google Scholar 

  • Jenks PJ, Shaw EJ (1997) Recurrent septicaemia due to “Achromobacter group B”. J Infect 34:143–145

    Article  CAS  Google Scholar 

  • Kehrenberg C, Aarestrup FM, Schwarz S (2007) IS21-558 insertion sequences are involved in the mobility of the multiresistance gene cfr. Antimicrob Agents Chemother 51:483–487

    Article  CAS  Google Scholar 

  • Kobayashi N, Nishino K, Yamaguchi A (2001) Novel macrolide-specific ABC-type efflux transporter in Escherichia coli. J Bacteriol 183:5639–5644

    Article  CAS  Google Scholar 

  • Labro MT (1992) Immunological evaluation of cefodizime: a unique molecule among cephalosporins. Infection 20:S45-47

    Article  Google Scholar 

  • Lau CH, Hughes D, Poole K (2014) MexY-promoted aminoglycoside resistance in Pseudomonas aeruginosa: involvement of a putative proximal binding pocket in aminoglycoside recognition. MBio 5:e01068

    Article  Google Scholar 

  • Li XZ, Zhang L, Poole K (2002) SmeC, an outer membrane multidrug efflux protein of Stenotrophomonas maltophilia. Antimicrob Agents Chemother 46:333–343

    Article  CAS  Google Scholar 

  • Lin MF, Lin YY, Yeh HW, Lan CY (2014) Role of the BaeSR two-component system in the regulation of Acinetobacter baumannii adeAB genes and its correlation with tigecycline susceptibility. BMC Microbiol 14:119

    Article  CAS  Google Scholar 

  • Liu B, Pop M (2009) ARDB–antibiotic resistance genes database. Nucleic Acids Res 37:D443-447

    Google Scholar 

  • Livermore DM, Jones CS (1986) Characterization of NPS-1, a novel plasmid-mediated beta-lactamase, from two Pseudomonas aeruginosa isolates. Antimicrob Agents Chemother 29:99–103

    Article  CAS  Google Scholar 

  • Magnet S, Courvalin P, Lambert T (2001) Resistance-nodulation-cell division-type efflux pump involved in aminoglycoside resistance in Acinetobacter baumannii strain BM4454. Antimicrob Agents Chemother 45:3375–3380

    Article  CAS  Google Scholar 

  • Markowitz VM, Mavromatis K, Ivanova NN, Chen IM, Chu K, Kyrpides NC (2009) IMG ER: a system for microbial genome annotation expert review and curation. Bioinformatics 25:2271–2278

    Article  CAS  Google Scholar 

  • Markowitz VM, Chen IM, Palaniappan K, Chu K, Szeto E, Pillay M, Ratner A, Huang J, Woyke T, Huntemann M, Anderson I, Billis K, Varghese N, Mavromatis K, Pati A, Ivanova NN, Kyrpides NC (2014) IMG 4 version of the integrated microbial genomes comparative analysis system. Nucleic Acids Res 42:D560-567

    Google Scholar 

  • McArthur AG, Waglechner N, Nizam F, Yan A, Azad MA, Baylay AJ, Bhullar K, Canova MJ, De Pascale G, Ejim L, Kalan L, King AM, Koteva K, Morar M, Mulvey MR, O’Brien JS, Pawlowski AC, Piddock LJ, Spanogiannopoulos P, Sutherland AD, Tang I, Taylor PL, Thaker M, Wang W, Yan M, Yu T, Wright GD (2013) The comprehensive antibiotic resistance database. Antimicrob Agents Chemother 57:3348–3357

    Article  CAS  Google Scholar 

  • McKinley KP, Laundy TJ, Masterton RG (1990) Achromobacter group B replacement valve endocarditis. J Infect 20:262–263

    Article  CAS  Google Scholar 

  • Olliver A, Vallé M, Chaslus-Dancla E, Cloeckaert A (2005) Overexpression of the multidrug efflux operon acrEF by insertional activation with IS1 or IS10 elements in Salmonella enterica serovar typhimurium DT204 acrB mutants selected with fluoroquinolones. Antimicrob Agents Chemother 49:289–301

    Article  CAS  Google Scholar 

  • Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ, Disz T, Edwards RA, Gerdes S, Parrello B, Shukla M, Vonstein V, Wattam AR, Xia F, Stevens R (2014) The SEED and the rapid annotation of microbial genomes using subsystems technology (RAST). Nucleic Acids Res 42:D206-214

    Article  Google Scholar 

  • Pai H, Jacoby GA (2001) Sequences of the NPS-1 and TLE-1 beta-lactamase genes. Antimicrob Agents Chemother 45:2947–2948

    Article  CAS  Google Scholar 

  • Piddock LJ (2006) Clinically relevant chromosomally encoded multidrug resistance efflux pumps in bacteria. Clin Microbiol Rev 19:382–402

    Article  CAS  Google Scholar 

  • Pos KM (2009) Drug transport mechanism of the AcrB efflux pump. Biochim Biophys Acta 1794:782–793

    Article  CAS  Google Scholar 

  • Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, Rajandream MA, Barrell B (2000) Artemis: sequence visualization and annotation. Bioinformatics 16:944–945

    Article  CAS  Google Scholar 

  • Shi Y, Chai L, Yang Z, Jing Q, Chen R, Chen Y (2012) Identification and hexavalent chromium reduction characteristics of Pannonibacter phragmitetus. Bioprocess Biosyst Eng 35:843–850

    Article  CAS  Google Scholar 

  • Sobel ML, McKay GA, Poole K (2003) Contribution of the MexXY multidrug transporter to aminoglycoside resistance in Pseudomonas aeruginosa clinical isolates. Antimicrob Agents Chemother 47:3202–3207

    Article  CAS  Google Scholar 

  • Swick MC, Morgan-Linnell SK, Carlson KM, Zechiedrich L (2011) Expression of multidrug efflux pump genes acrAB-tolC, mdfA, and norE in Escherichia coli clinical isolates as a function of fluoroquinolone and multidrug resistance. Antimicrob Agents Chemother 55:921–924

    Article  CAS  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  Google Scholar 

  • Turlin E, Heuck G, Simões Brandão MI, Szili N, Mellin JR, Lange N, Wandersman C (2014) Protoporphyrin (PPIX) efflux by the MacAB-TolC pump in Escherichia coli. Microbiologyopen 3:849–859

    Article  CAS  Google Scholar 

  • Wang Y, Yang Z, Peng B, Chai L, Wu B, Wu R (2013) Biotreatment of chromite ore processing residue by Pannonibacter phragmitetus BB. Environ Sci Pollut Res Int 20:55935–55602

    Google Scholar 

  • Westbrock-Wadman S, Sherman DR, Hickey MJ, Coulter SN, Zhu YQ, Warrener P, Nguyen LY, Shawar RM, Folger KR, Stover CK (1999) Characterization of a Pseudomonas aeruginosa efflux pump contributing to aminoglycoside impermeability. Antimicrob Agents Chemother 43:2975–2983

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wu S, Zhu Z, Fu L, Niu B, Li W (2011) WebMGA: a customizable web server for fast metagenomic sequence analysis. BMC Genom 12:444

    Article  Google Scholar 

  • Xu L, Luo M, Yang L, Wei X, Lin X, Liu H (2011) Encapsulation of Pannonibacter phragmitetus LSSE-09 in alginate-carboxymethyl cellulose capsules for reduction of hexavalent chromium under alkaline conditions. J Ind Microbiol Biotechnol 38:1709–1718

    Article  CAS  Google Scholar 

  • Zankari E, Hasman H, Cosentino S, Vestergaard M, Rasmussen S, Lund O, Aarestrup FM, Larsen MV (2012) Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother 67:2640–2644

    Article  CAS  Google Scholar 

  • Zhou Y, Liang Y, Lynch KH, Dennis JJ, Wishart DS (2011) PHAST: a fast phage search tool. Nucleic Acids Res 39:W347–352

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank the staff of the Yun Leung Laboratory for Molecular Diagnostics, School of Biomedical Sciences, Huaqiao University, Xiamen, for their providing bioinformatic analysis, especially Dr. Mingxi Wang for his kind assistance. This work was supported by the Fujian Province Science and Technology Planning Foundations (2015J01514), the Quanzhou high level talent innovation and Entrepreneurship Project (2017Z36).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to De-song Ming.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interests.

Additional information

Communicated by Djamel Drider.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ming, Ds., Chen, Qq. & Chen, Xt. Analysis of resistance genes of clinical Pannonibacter phragmitetus strain 31801 by complete genome sequencing. Arch Microbiol 200, 1101–1109 (2018). https://doi.org/10.1007/s00203-018-1522-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00203-018-1522-2

Keywords

Navigation