Top

Published in:

01-08-2017 | Original Article

Characterization and genome comparisons of three Achromobacter phages of the family Siphoviridae

Authors: Brigitte Dreiseikelmann, Boyke Bunk, Cathrin Spröer, Manfred Rohde, Manfred Nimtz, Johannes Wittmann

Published in: Archives of Virology | Issue 8/2017

Abstract

In this study, we present the characterization and genomic data of three Achromobacter phages belonging to the family Siphoviridae. Phages 83-24, JWX and JWF were isolated from sewage samples in Paris and Braunschweig, respectively, and infect Achromobacter xylosoxidans, an emerging nosocomial pathogen in cystic fibrosis patients. Analysis of morphology and growth parameters revealed that phages 83-24 and JWX have similar properties, both have nearly the same head and tail measurements, and both have a burst size between 85 and 100 pfu/cell. In regard to morphological properties, JWF had a much longer and more flexible tail compared to other phages. The linear double-stranded DNAs of all three phages are terminally redundant and not circularly permutated. The complete nucleotide sequences consist of 81,541 bp for JWF, 49,714 bp for JWX and 48,216 bp for 83-24. Analysis of the genome sequences showed again that phages JWX and 83-24 are quite similar. Comparison to the GenBank database via BLASTN revealed partial similarities to Roseobacter phage RDJL phi1 and Burkholderia phage BcepGomr. In contrast, BLASTN analysis of the genome sequence of phage JWF revealed only few similarities to non-annotated prophage regions in different strains of Burkholderia and Mesorhizobium.

Available only for authorised users

Yabuuchi E, Oyama A (1971) Achromobacter xylosoxidans n. sp. from human ear discharge. Jpn J Microbiol 15(5):477–481CrossRefPubMed

Busse HJ, Auling G (2005) Genus II. Achromobacter Yabuuchi and Yano 1981, 477VP emend. Yabuuchi, Kawamura, Kosako and Ezaki 1998a, 1083. In: Brenner DJ, Krieg NR, Staley JT (eds) Bergey’s manual of systematic bacteriology. Springer, New York, pp 658–662

Spear JB, Fuhrer J, Kirby BD (1988) Achromobacter xylosoxidans (Alcaligenes xylosoxidans subsp. xylosoxidans) bacteremia associated with a well-water source: case report and review of the literature. J Clin Microbiol 26(3):598–599PubMedPubMedCentral

Mahenthiralingam E (2014) Emerging cystic fibrosis pathogens and the microbiome. Paediatr Respir Rev 15(Suppl 1):13–15. doi:10.1016/j.prrv.2014.04.006 PubMed

Trancassini M, Iebba V, Citera N, Tuccio V, Magni A, Varesi P, De Biase RV, Totino V, Santangelo F, Gagliardi A, Schippa S (2014) Outbreak of Achromobacter xylosoxidans in an Italian Cystic fibrosis center: genome variability, biofilm production, antibiotic resistance, and motility in isolated strains. Front Microbiol 5:138. doi:10.3389/fmicb.2014.00138 CrossRefPubMedPubMedCentral

Ahmed MS, Nistal C, Jayan R, Kuduvalli M, Anijeet HK (2009) Achromobacter xylosoxidans, an emerging pathogen in catheter-related infection in dialysis population causing prosthetic valve endocarditis: a case report and review of literature. Clin Nephrol 71(3):350–354CrossRefPubMed

van Hal S, Stark D, Marriott D, Harkness J (2008) Achromobacter xylosoxidans subsp. xylosoxidans prosthetic aortic valve infective endocarditis and aortic root abscesses. J Med Microbiol 57(Pt 4):525–527. doi:10.1099/jmm.0.47496-0 PubMed

Behrens-Muller B, Conway J, Yoder J, Conover CS (2012) Investigation and control of an outbreak of Achromobacter xylosoxidans bacteremia. Infect Control Hosp Epidemiol 33(2):180–184. doi:10.1086/663710 CrossRefPubMed

Tena D, Carranza R, Barbera JR, Valdezate S, Garrancho JM, Arranz M, Saez-Nieto JA (2005) Outbreak of long-term intravascular catheter-related bacteremia due to Achromobacter xylosoxidans subspecies xylosoxidans in a hemodialysis unit. Eur J Clin Microbiol Infect Dis 24(11):727–732. doi:10.1007/s10096-005-0028-4 CrossRefPubMed

10.

Park JH, Song NH, Koh JW (2012) Achromobacter xylosoxidans keratitis after contact lens usage. Korean J Ophthalmol 26(1):49–53. doi:10.3341/kjo.2012.26.1.49 CrossRefPubMedPubMedCentral

11.

Reddy AK, Garg P, Shah V, Gopinathan U (2009) Clinical, microbiological profile and treatment outcome of ocular infections caused by Achromobacter xylosoxidans. Cornea 28(10):1100–1103. doi:10.1097/ICO.0b013e3181a1658f CrossRefPubMed

12.

Tena D, Gonzalez-Praetorius A, Perez-Balsalobre M, Sancho O, Bisquert J (2008) Urinary tract infection due to Achromobacter xylosoxidans: report of 9 cases. Scand J Infect Dis 40(2):84–87. doi:10.1080/00365540701558714 CrossRefPubMed

13.

Wittmann J, Dreiseikelmann B, Rohde C, Rohde M, Sikorski J (2014) Isolation and characterization of numerous novel phages targeting diverse strains of the ubiquitous and opportunistic pathogen Achromobacter xylosoxidans. PLoS One 9(1):e86935. doi:10.1371/journal.pone.0086935 CrossRefPubMedPubMedCentral

14.

Abedon ST, Kuhl SJ, Blasdel BG, Kutter EM (2011) Phage treatment of human infections. Bacteriophage 1(2):66–85. doi:10.4161/bact.1.2.15845 CrossRefPubMedPubMedCentral

15.

Johnson RP, Gyles CL, Huff WE, Ojha S, Huff GR, Rath NC, Donoghue AM (2008) Bacteriophages for prophylaxis and therapy in cattle, poultry and pigs. Anim Health Res Rev 9(2):201–215. doi:10.1017/s1466252308001576 CrossRefPubMed

16.

Zaczek M, Weber-Dabrowska B, Gorski A (2014) Phages in the global fruit and vegetable industry. J Appl Microbiol. doi:10.1111/jam.12700 PubMed

17.

Jones PT, Pretorius GHJ (1981) Achromobacter sp. 2 Phage a3: a physical characterization. J Gen Virol 55:275–281CrossRef

18.

Thomson JA, Woods DR (1974) Bacteriophages and cryptic lysogeny in Achromobacter. J Gen Virol 22(1):153–157CrossRefPubMed

19.

Wittmann J, Klumpp J, Moreno Switt AI, Yagubi A, Ackermann HW, Wiedmann M, Svircev A, Nash JH, Kropinski AM (2015) Taxonomic reassessment of N4-like viruses using comparative genomics and proteomics suggests a new subfamily—”Enquartavirinae”. Arch Virol 160(12):3053–3062. doi:10.1007/s00705-015-2609-6 CrossRefPubMed

20.

Wittmann J, Dreiseikelmann B, Rohde M, Meier-Kolthoff JP, Bunk B, Rohde C (2014) First genome sequences of Achromobacter phages reveal new members of the N4 family. Virol J 11:14. doi:10.1186/1743-422x-11-14 CrossRefPubMedPubMedCentral

21.

Li E, Zhao J, Ma Y, Wei X, Li H, Lin W, Wang X, Li C, Shen Z, Zhao R, Jiang A, Yang H, Yuan J, Zhao X (2016) Characterization of a novel Achromobacter xylosoxidans specific siphoviruse: phiAxp-1. Sci Rep 6:21943. doi:10.1038/srep21943 CrossRefPubMedPubMedCentral

22.

Ma Y, Li E, Qi Z, Li H, Wei X, Lin W, Zhao R, Jiang A, Yang H, Yin Z, Yuan J, Zhao X (2016) Isolation and molecular characterisation of Achromobacter phage phiAxp-3, an N4-like bacteriophage. Sci Rep 6:24776. doi:10.1038/srep24776 CrossRefPubMedPubMedCentral

23.

Beilstein F, Dreiseikelmann B (2006) Bacteriophages of freshwater Brevundimonas vesicularis isolates. Res Microbiol 157(3):213–219. doi:10.1016/j.resmic.2005.07.005 CrossRefPubMed

24.

Thorvaldsdottir H, Robinson JT, Mesirov JP (2013) Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform 14(2):178–192. doi:10.1093/bib/bbs017 CrossRefPubMed

25.

Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, Rajandream MA, Barrell B (2000) Artemis: sequence visualization and annotation. Bioinformatics 16(10):944–945CrossRefPubMed

26.

Lowe TM, Eddy SR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25(5):955–964CrossRefPubMedPubMedCentral

27.

Laslett D, Canback B (2004) ARAGORN, a program to detect tRNA genes and tmRNA genes in nucleotide sequences. Nucleic Acids Res 32(1):11–16. doi:10.1093/nar/gkh152 CrossRefPubMedPubMedCentral

28.

Park M, Lee JH, Shin H, Kim M, Choi J, Kang DH, Heu S, Ryu S (2012) Characterization and comparative genomic analysis of a novel bacteriophage, SFP10, simultaneously inhibiting both Salmonella enterica and Escherichia coli O157:H7. Appl Environ Microbiol 78(1):58–69. doi:10.1128/aem.06231-11 CrossRefPubMedPubMedCentral

29.

Wittmann J, Gartemann KH, Eichenlaub R, Dreiseikelmann B (2011) Genomic and molecular analysis of phage CMP1 from Clavibacter michiganensis subspecies michiganensis. Bacteriophage 1(1):6–14. doi:10.4161/bact.1.1.13873 CrossRefPubMedPubMedCentral

30.

Valentine RC, Shapiro BM, Stadtman ER (1968) Regulation of glutamine synthetase. XII. Electron microscopy of the enzyme from Escherichia coli. Biochemistry 7(6):2143–2152CrossRefPubMed

31.

Jakobsen TH, Hansen MA, Jensen PO, Hansen L, Riber L, Cockburn A, Kolpen M, Ronne Hansen C, Ridderberg W, Eickhardt S, Hansen M, Kerpedjiev P, Alhede M, Qvortrup K, Burmolle M, Moser C, Kuhl M, Ciofu O, Givskov M, Sorensen SJ, Hoiby N, Bjarnsholt T (2013) Complete genome sequence of the cystic fibrosis pathogen Achromobacter xylosoxidans NH44784-1996 complies with important pathogenic phenotypes. PLoS One 8(7):e68484. doi:10.1371/journal.pone.0068484 CrossRefPubMedPubMedCentral

32.

Strnad H, Ridl J, Paces J, Kolar M, Vlcek C, Paces V (2011) Complete genome sequence of the haloaromatic acid-degrading bacterium Achromobacter xylosoxidans A8. J Bacteriol 193(3):791–792. doi:10.1128/JB.01299-10 CrossRefPubMed

33.

Rocha EP, Danchin A (2002) Base composition bias might result from competition for metabolic resources. Trends Genet 18(6):291–294. doi:10.1016/s0168-9525(02)02690-2 CrossRefPubMed

34.

Seemann T (2014) Prokka: rapid prokaryotic genome annotation. Bioinformatics 30(14):2068–2069. doi:10.1093/bioinformatics/btu153 CrossRefPubMed

35.

Zhou Y, Liang Y, Lynch KH, Dennis JJ, Wishart DS (2011) PHAST: a fast phage search tool. Nucleic Acids Res 39((Web Server issue)):W347–W352. doi:10.1093/nar/gkr485 CrossRefPubMedPubMedCentral

36.

Ceyssens PJ, Mesyanzhinov V, Sykilinda N, Briers Y, Roucourt B, Lavigne R, Robben J, Domashin A, Miroshnikov K, Volckaert G, Hertveldt K (2008) The genome and structural proteome of YuA, a new Pseudomonas aeruginosa phage resembling M6. J Bacteriol 190(4):1429–1435. doi:10.1128/jb.01441-07 CrossRefPubMed

37.

Seguritan V, Feng IW, Rohwer F, Swift M, Segall AM (2003) Genome sequences of two closely related Vibrio parahaemolyticus phages, VP16T and VP16C. J Bacteriol 185(21):6434–6447CrossRefPubMedPubMedCentral

38.

Groth AC, Calos MP (2004) Phage integrases: biology and applications. J Mol Biol 335(3):667–678CrossRefPubMed

39.

Casjens SR, Gilcrease EB, Winn-Stapley DA, Schicklmaier P, Schmieger H, Pedulla ML, Ford ME, Houtz JM, Hatfull GF, Hendrix RW (2005) The generalized transducing Salmonella bacteriophage ES18: complete genome sequence and DNA packaging strategy. J Bacteriol 187(3):1091–1104. doi:10.1128/jb.187.3.1091-1104.2005 CrossRefPubMedPubMedCentral

40.

Fouts DE, Klumpp J, Bishop-Lilly KA, Rajavel M, Willner KM, Butani A, Henry M, Biswas B, Li M, Albert MJ, Loessner MJ, Calendar R, Sozhamannan S (2013) Whole genome sequencing and comparative genomic analyses of two Vibrio cholerae O139 Bengal-specific Podoviruses to other N4-like phages reveal extensive genetic diversity. Virol J 10:165. doi:10.1186/1743-422x-10-165 CrossRefPubMedPubMedCentral

41.

Merrill BD, Grose JH, Breakwell DP, Burnett SH (2014) Characterization of Paenibacillus larvae bacteriophages and their genomic relationships to firmicute bacteriophages. BMC Genom 15:745. doi:10.1186/1471-2164-15-745 CrossRef

42.

Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28(10):2731–2739. doi:10.1093/molbev/msr121 CrossRefPubMedPubMedCentral

43.

Krogh A, Larsson B, von Heijne G, Sonnhammer EL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305(3):567–580. doi:10.1006/jmbi.2000.4315 CrossRefPubMed

44.

Young R (2002) Bacteriophage holins: deadly diversity. J Mol Microbiol Biotechnol 4(1):21–36PubMed

45.

Stewart CR, Casjens SR, Cresawn SG, Houtz JM, Smith AL, Ford ME, Peebles CL, Hatfull GF, Hendrix RW, Huang WM, Pedulla ML (2009) The genome of Bacillus subtilis bacteriophage SPO1. J Mol Biol 388(1):48–70. doi:10.1016/j.jmb.2009.03.009 CrossRefPubMedPubMedCentral

46.

Ong KS, Aw YK, Gan HM, Yule CM, Lee SM (2014) Draft genome sequences of two antimicrobial-producing Burkholderia sp. strains, MSh1 and MSh2, isolated from Malaysian Tropical Peat Swamp Forest Soil. Genome Announc. doi:10.1128/genomeA.01032-14

47.

Summer EJ, Berry J, Tran TA, Niu L, Struck DK, Young R (2007) Rz/Rz1 lysis gene equivalents in phages of Gram-negative hosts. J Mol Biol 373(5):1098–1112. doi:10.1016/j.jmb.2007.08.045 CrossRefPubMed

48.

Mahadevan P, King JF, Seto D (2009) CGUG: in silico proteome and genome parsing tool for the determination of “core” and unique genes in the analysis of genomes up to ca. 1.9 Mb. BMC Res Notes 2:168. doi:10.1186/1756-0500-2-168 CrossRefPubMedPubMedCentral

49.

Lavigne R, Seto D, Mahadevan P, Ackermann HW, Kropinski AM (2008) Unifying classical and molecular taxonomic classification: analysis of the Podoviridae using BLASTP-based tools. Res Microbiol 159(5):406–414. doi:10.1016/j.resmic.2008.03.005 CrossRefPubMed

50.

Hatfull GF (2008) Bacteriophage genomics. Curr Opin Microbiol 11(5):447–453. doi:10.1016/j.mib.2008.09.004 CrossRefPubMedPubMedCentral

51.

Casjens SR, Thuman-Commike PA (2011) Evolution of mosaically related tailed bacteriophage genomes seen through the lens of phage P22 virion assembly. Virology 411(2):393–415. doi:10.1016/j.virol.2010.12.046 CrossRefPubMed

52.

Maynaud G, Brunel B, Mornico D, Durot M, Severac D, Dubois E, Navarro E, Cleyet-Marel JC, Le Quere A (2013) Genome-wide transcriptional responses of two metal-tolerant symbiotic Mesorhizobium isolates to zinc and cadmium exposure. BMC Genom 14:292. doi:10.1186/1471-2164-14-292 CrossRef

53.

Lohr JE, Chen F, Hill RT (2005) Genomic analysis of bacteriophage PhiJL001: insights into its interaction with a sponge-associated alpha-proteobacterium. Appl Environ Microbiol 71(3):1598–1609. doi:10.1128/aem.71.3.1598-1609.2005 CrossRefPubMedPubMedCentral

Title: Characterization and genome comparisons of three Achromobacter phages of the family Siphoviridae
Authors: Brigitte Dreiseikelmann
Boyke Bunk
Cathrin Spröer
Manfred Rohde
Manfred Nimtz
Johannes Wittmann
Publication date: 01-08-2017
Publisher: Springer Vienna
Published in: Archives of Virology / Issue 8/2017
Print ISSN: 0304-8608
Electronic ISSN: 1432-8798
DOI: https://doi.org/10.1007/s00705-017-3347-8

Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Reserve your place

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin

Prof. Florian Limbourg

Prof. Anoop Chauhan

Developed by: Springer Medicine

Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 8/2017

NS3 protease resistance-associated substitutions in liver tissue and plasma samples from patients infected by hepatitis C virus genotype 1A or 1B

Exposure to cold impairs interferon-induced antiviral defense

Characterization of cross-clade monoclonal antibodies against H5N1 highly pathogenic avian influenza virus and their application to the antigenic analysis of diverse H5 subtype viruses

A dose-response study in mice of a tetravalent vaccine candidate composed of domain III-capsid proteins from dengue viruses

Evolution of H5 highly pathogenic avian influenza: sequence data indicate stepwise changes in the cleavage site

Grass carp reovirus outer capsid proteins VP5 and VP7 interact in vitro

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

At a glance: The STEP trials