First genome sequences of Achromobacter phages reveal new members of the N4 family

Wittmann J, Dreiseikelmann B, Rohde M, Meier-Kolthoff JP, Bunk B, Rohde C (2014)
Virology Journal 11.

Download
No fulltext has been uploaded. References only!
Journal Article | Original Article | Published | English

No fulltext has been uploaded

Author
; ; ; ; ;
Abstract
Background: Multi-resistant Achromobacter xylosoxidans has been recognized as an emerging pathogen causing nosocomially acquired infections during the last years. Phages as natural opponents could be an alternative to fight such infections. Bacteriophages against this opportunistic pathogen were isolated in a recent study. This study shows a molecular analysis of two podoviruses and reveals first insights into the genomic structure of Achromobacter phages so far. Methods: Growth curve experiments and adsorption kinetics were performed for both phages. Adsorption and propagation in cells were visualized by electron microscopy. Both phage genomes were sequenced with the PacBio RS II system based on single molecule, real-time (SMRT) technology and annotated with several bioinformatic tools. To further elucidate the evolutionary relationships between the phage genomes, a phylogenomic analysis was conducted using the genome Blast Distance Phylogeny approach (GBDP). Results: In this study, we present the first detailed analysis of genome sequences of two Achromobacter phages so far. Phages JWAlpha and JWDelta were isolated from two different waste water treatment plants in Germany. Both phages belong to the Podoviridae and contain linear, double-stranded DNA with a length of 72329 bp and 73659 bp, respectively. 92 and 89 putative open reading frames were identified for JWAlpha and JWDelta, respectively, by bioinformatic analysis with several tools. The genomes have nearly the same organization and could be divided into different clusters for transcription, replication, host interaction, head and tail structure and lysis. Detailed annotation via protein comparisons with BLASTP revealed strong similarities to N4-like phages. Conclusions: Analysis of the genomes of Achromobacter phages JWAlpha and JWDelta and comparisons of different gene clusters with other phages revealed that they might be strongly related to other N4-like phages, especially of the Escherichia group. Although all these phages show a highly conserved genomic structure and partially strong similarities at the amino acid level, some differences could be identified. Those differences, e.g. the existence of specific genes for replication or host interaction in some N4-like phages, seem to be interesting targets for further examination of function and specific mechanisms, which might enlighten the mechanism of phage establishment in the host cell after infection.
Publishing Year
ISSN
PUB-ID

Cite this

Wittmann J, Dreiseikelmann B, Rohde M, Meier-Kolthoff JP, Bunk B, Rohde C. First genome sequences of Achromobacter phages reveal new members of the N4 family. Virology Journal. 2014;11.
Wittmann, J., Dreiseikelmann, B., Rohde, M., Meier-Kolthoff, J. P., Bunk, B., & Rohde, C. (2014). First genome sequences of Achromobacter phages reveal new members of the N4 family. Virology Journal, 11. doi:10.1186/1743-422X-11-14
Wittmann, J., Dreiseikelmann, B., Rohde, M., Meier-Kolthoff, J. P., Bunk, B., and Rohde, C. (2014). First genome sequences of Achromobacter phages reveal new members of the N4 family. Virology Journal 11.
Wittmann, J., et al., 2014. First genome sequences of Achromobacter phages reveal new members of the N4 family. Virology Journal, 11.
J. Wittmann, et al., “First genome sequences of Achromobacter phages reveal new members of the N4 family”, Virology Journal, vol. 11, 2014.
Wittmann, J., Dreiseikelmann, B., Rohde, M., Meier-Kolthoff, J.P., Bunk, B., Rohde, C.: First genome sequences of Achromobacter phages reveal new members of the N4 family. Virology Journal. 11, (2014).
Wittmann, Johannes, Dreiseikelmann, Brigitte, Rohde, Manfred, Meier-Kolthoff, Jan P., Bunk, Boyke, and Rohde, Christine. “First genome sequences of Achromobacter phages reveal new members of the N4 family”. Virology Journal 11 (2014).
This data publication is cited in the following publications:
This publication cites the following data publications:

24 Citations in Europe PMC

Data provided by Europe PubMed Central.

Isolation and characterization of a novel bacteriophage infecting Vibrio alginolyticus.
Kokkari C, Sarropoulou E, Bastias R, Mandalakis M, Katharios P., Arch Microbiol (), 2018
PMID: 29372278
Isolation of bacteriophages and their application to control Pseudomonas aeruginosa in planktonic and biofilm models.
Kwiatek M, Parasion S, Rutyna P, Mizak L, Gryko R, Niemcewicz M, Olender A, Łobocka M., Res Microbiol 168(3), 2017
PMID: 27818282
Characterization and genome comparisons of three Achromobacter phages of the family Siphoviridae.
Dreiseikelmann B, Bunk B, Spröer C, Rohde M, Nimtz M, Wittmann J., Arch Virol 162(8), 2017
PMID: 28357512
Three novel Pseudomonas phages isolated from composting provide insights into the evolution and diversity of tailed phages.
Amgarten D, Martins LF, Lombardi KC, Antunes LP, de Souza APS, Nicastro GG, Kitajima EW, Quaggio RB, Upton C, Setubal JC, da Silva AM., BMC Genomics 18(1), 2017
PMID: 28472930
Isolation and Characterization of phiLLS, a Novel Phage with Potential Biocontrol Agent against Multidrug-Resistant Escherichia coli.
Amarillas L, Rubí-Rangel L, Chaidez C, González-Robles A, Lightbourn-Rojas L, León-Félix J., Front Microbiol 8(), 2017
PMID: 28785246
Complete genome sequence of lytic bacteriophage RG-2014 that infects the multidrug resistant bacterium Delftia tsuruhatensis ARB-1.
Bhattacharjee AS, Motlagh AM, Gilcrease EB, Islam MI, Casjens SR, Goel R., Stand Genomic Sci 12(), 2017
PMID: 29270250
Isolation and characterization of a N4-like lytic bacteriophage infecting Vibrio splendidus, a pathogen of fish and bivalves.
Katharios P, Kalatzis PG, Kokkari C, Sarropoulou E, Middelboe M., PLoS One 12(12), 2017
PMID: 29284014
A novel bacteriophage cocktail reduces and disperses Pseudomonas aeruginosa biofilms under static and flow conditions.
Alves DR, Perez-Esteban P, Kot W, Bean JE, Arnot T, Hansen LH, Enright MC, Jenkins AT., Microb Biotechnol 9(1), 2016
PMID: 26347362
Characterization of a novel Achromobacter xylosoxidans specific siphoviruse: phiAxp-1.
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., Sci Rep 6(), 2016
PMID: 26908262
Isolation and molecular characterisation of Achromobacter phage phiAxp-3, an N4-like bacteriophage.
Ma Y, Li E, Qi Z, Li H, Wei X, Lin W, Zhao R, Jiang A, Yang H, Yin Z, Yuan J, Zhao X., Sci Rep 6(), 2016
PMID: 27094846
Characterization of the first cultured representative of Verrucomicrobia subdivision 5 indicates the proposal of a novel phylum.
Spring S, Bunk B, Spröer C, Schumann P, Rohde M, Tindall BJ, Klenk HP., ISME J 10(12), 2016
PMID: 27300277
Testing hypotheses for the presence of tRNA genes in mycobacteriophage genomes.
Delesalle VA, Tanke NT, Vill AC, Krukonis GP., Bacteriophage 6(3), 2016
PMID: 27738556
Identification and molecular characterization of bacteriophage phiAxp-2 of Achromobacter xylosoxidans.
Li E, Yin Z, Ma Y, Li H, Lin W, Wei X, Zhao R, Jiang A, Yuan J, Zhao X., Sci Rep 6(), 2016
PMID: 27669904
Comparative Functional Genomic Analysis of Two Vibrio Phages Reveals Complex Metabolic Interactions with the Host Cell.
Skliros D, Kalatzis PG, Katharios P, Flemetakis E., Front Microbiol 7(), 2016
PMID: 27895630
Novel N4 Bacteriophages Prevail in the Cold Biosphere.
Zhan Y, Buchan A, Chen F., Appl Environ Microbiol 81(15), 2015
PMID: 26025897
Paenibacillus larvae-Directed Bacteriophage HB10c2 and Its Application in American Foulbrood-Affected Honey Bee Larvae.
Beims H, Wittmann J, Bunk B, Spröer C, Rohde C, Günther G, Rohde M, von der Ohe W, Steinert M., Appl Environ Microbiol 81(16), 2015
PMID: 26048941
Bacteriophage therapy for membrane biofouling in membrane bioreactors and antibiotic-resistant bacterial biofilms.
Bhattacharjee AS, Choi J, Motlagh AM, Mukherji ST, Goel R., Biotechnol Bioeng 112(8), 2015
PMID: 25728819
Taxonomic reassessment of N4-like viruses using comparative genomics and proteomics suggests a new subfamily - "Enquartavirinae".
Wittmann J, Klumpp J, Moreno Switt AI, Yagubi A, Ackermann HW, Wiedmann M, Svircev A, Nash JH, Kropinski AM., Arch Virol 160(12), 2015
PMID: 26395091
Unlocking the mystery of the hard-to-sequence phage genome: PaP1 methylome and bacterial immunity.
Lu S, Le S, Tan Y, Li M, Liu C, Zhang K, Huang J, Chen H, Rao X, Zhu J, Zou L, Ni Q, Li S, Wang J, Jin X, Hu Q, Yao X, Zhao X, Zhang L, Huang G, Hu F., BMC Genomics 15(), 2014
PMID: 25233860
Emerging methods to study bacteriophage infection at the single-cell level.
Dang VT, Sullivan MB., Front Microbiol 5(), 2014
PMID: 25566233

75 References

Data provided by Europe PubMed Central.

Peptidoglycan types of bacterial cell walls and their taxonomic implications.
Schleifer KH, Kandler O., Bacteriol Rev 36(4), 1972
PMID: 4568761
Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes.
Krogh A, Larsson B, von Heijne G, Sonnhammer EL., J. Mol. Biol. 305(3), 2001
PMID: 11152613
Phages will out: strategies of host cell lysis.
Young I, Wang I, Roof WD., Trends Microbiol. 8(3), 2000
PMID: 10707065
The endolysins of bacteriophages CMP1 and CN77 are specific for the lysis of Clavibacter michiganensis strains.
Wittmann J, Eichenlaub R, Dreiseikelmann B., Microbiology (Reading, Engl.) 156(Pt 8), 2010
PMID: 20447991
Whole-genome prokaryotic phylogeny.
Henz SR, Huson DH, Auch AF, Nieselt-Struwe K, Schuster SC., Bioinformatics 21(10), 2005
PMID: 15166018
Genome BLAST distance phylogenies inferred from whole plastid and whole mitochondrion genome sequences.
Auch AF, Henz SR, Holland BR, Goker M., BMC Bioinformatics 7(), 2006
PMID: 16854218
Genome sequence-based species delimitation with confidence intervals and improved distance functions.
Meier-Kolthoff JP, Auch AF, Klenk HP, Goker M., BMC Bioinformatics 14(), 2013
PMID: 23432962
An empirical test of the midpoint rooting method
AUTHOR UNKNOWN, 2007
BLAST+: architecture and applications.
Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL., BMC Bioinformatics 10(), 2009
PMID: 20003500
Isolation and characterization of a novel indigenous intestinal N4-related coliphage vB_EcoP_G7C.
Kulikov E, Kropinski AM, Golomidova A, Lingohr E, Govorun V, Serebryakova M, Prokhorov N, Letarova M, Manykin A, Strotskaya A, Letarov A., Virology 426(2), 2012
PMID: 22341309
Complete genome sequence of the bacteriophages ECBP1 and ECBP2 isolated from two different Escherichia coli strains.
Nho SW, Ha MA, Kim KS, Kim TH, Jang HB, Cha IS, Park SB, Kim YK, Jung TS., J. Virol. 86(22), 2012
PMID: 23087106
Complete genome sequence of IME11, a new N4-like bacteriophage.
Fan H, Fan H, An X, Huang Y, Zhang Z, Mi Z, Tong Y., J. Virol. 86(24), 2012
PMID: 23166261
Complete genome of Pseudomonas aeruginosa phage PA26.
Kim MS, Cha KE, Myung H., J. Virol. 86(18), 2012
PMID: 22923802
Bacteriophages of freshwater Brevundimonas vesicularis isolates.
Beilstein F, Dreiseikelmann B., Res. Microbiol. 157(3), 2006
PMID: 16183261
Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration.
Thorvaldsdottir H, Robinson JT, Mesirov JP., Brief. Bioinformatics 14(2), 2013
PMID: 22517427
Artemis: sequence visualization and annotation.
Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, Rajandream MA, Barrell B., Bioinformatics 16(10), 2000
PMID: 11120685
Genomic and molecular analysis of phage CMP1 from Clavibacter michiganensis subspecies michiganensis.
Wittmann J, Gartemann KH, Eichenlaub R, Dreiseikelmann B., Bacteriophage 1(1), 2011
PMID: 21687530
Regulation of glutamine synthetase. XII. Electron microscopy of the enzyme from Escherichia coli.
Valentine RC, Shapiro BM, Stadtman ER., Biochemistry 7(6), 1968
PMID: 4873173
A low-viscosity epoxy resin embedding medium for electron microscopy.
Spurr AR., J. Ultrastruct. Res. 26(1), 1969
PMID: 4887011
Highly parallelized inference of large genome-based phylogenies
AUTHOR UNKNOWN, 2013

AUTHOR UNKNOWN, 2003

Export

0 Marked Publications

Open Data PUB

Web of Science

View record in Web of Science®

Sources

PMID: 24468270
PubMed | Europe PMC

Search this title in

Google Scholar