Sixteen bacteriophages of Achromobacter xylosoxidans distributed into four genera have been isolated from sewage water in Abidjan, Côte d’Ivoire, using a single clinical strain, and their genomes have been sequenced. Three podoviruses belonged to the genus Phikmvvirus, and these represent the first A. xylosoxidans phages of this genus. Seven podoviruses, distributed into three groups, belonged to the genus Jwalphavirus. Among the siphoviruses, three revealed similarities to Pseudomonas phage 73 and members of the genus Septimatrevirus, and three were YuA-like phages. The virulence of these phages toward a panel of 10 genetically diverse strains was tested, with the phiKMV-like phages showing the broadest host range.
This is a preview of subscription content, log in to check access.
Buy single article
Instant access to the full article PDF.
Price includes VAT for USA
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
This is the net price. Taxes to be calculated in checkout.
The genome sequences of the sixteen phages are available at GenBank under the following accession numbers: Axy04 (MK962626), Axy06 (MK962627), Axy09 (MK962628), Axy10 (MK962629), Axy11 (MK962630), Axy12 (MK962631), Axy13 (MK962632), Axy14 (MK962633), Axy16 (MK962634), Axy18 (MK962635), Axy19 (MK962636), Axy20 (MK962637), Axy21 (MK962638), Axy22 (MK962639), Axy23 (MK962640), Axy24 (MK962641). The raw read archives were deposited in bioproject PRJEB33638 together with raw sequencing data from A. xylosoxidans strain 19-32. The project can be accessed at https://www.ebi.ac.uk/ena/data/view/PRJEB33638.
Dupont C, Jumas-Bilak E, Doisy C, Aujoulat F, Chiron R, Marchandin H (2018) Chronic airway colonization by Achromobacter xylosoxidans in cystic fibrosis patients is not sustained by their domestic environment. Appl Environ Microbiol. https://doi.org/10.1128/aem.01739-18
Perez Barragan E, Sandino Perez J, Corbella L, Orellana MA, Fernandez-Ruiz M (2018) Achromobacter xylosoxidans bacteremia: clinical and microbiological features in a 10-year case series. Rev Esp Quimioter 31(3):268–273
Habib S, Fuca N, Azam M, Siddiqui AH, Rajdev K, Chalhoub M (2018) Achromobacter xylosoxidans/denitrificans bacteremia and subsequent fatal Escherichia coli/Streptococcus anginosus pleural empyema. Respir Med Case Rep 25:311–313. https://doi.org/10.1016/j.rmcr.2018.10.010
Tokuyasu H, Fukushima T, Nakazaki H, Shimizu E (2012) Infective endocarditis caused by Achromobacter xylosoxidans: a case report and review of the literature. Intern Med 51(9):1133–1138
Lee B, Cai CX, Srikumaran D, Woreta FA (2018) Severe Achromobacter xylosoxidans keratitis with deep corneal involvement. Am J Ophthalmol Case Rep 11:128–130. https://doi.org/10.1016/j.ajoc.2018.06.006
Jeukens J, Freschi L, Vincent AT, Emond-Rheault JG, Kukavica-Ibrulj I, Charette SJ, Levesque RC (2017) A pan-genomic approach to understand the basis of host adaptation in Achromobacter. Genome Biol Evol. https://doi.org/10.1093/gbe/evx061
Traglia GM, Almuzara M, Merkier AK, Adams C, Galanternik L, Vay C, Centron D, Ramirez MS (2012) Achromobacter xylosoxidans: an emerging pathogen carrying different elements involved in horizontal genetic transfer. Curr Microbiol 65(6):673–678. https://doi.org/10.1007/s00284-012-0213-5
Hoyle N, Zhvaniya P, Balarjishvili N, Bolkvadze D, Nadareishvili L, Nizharadze D, Wittmann J, Rohde C, Kutateladze M (2018) Phage therapy against Achromobacter xylosoxidans lung infection in a patient with cystic fibrosis: a case report. Res Microbiol 169(9):540–542. https://doi.org/10.1016/j.resmic.2018.05.001
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. https://doi.org/10.1371/journal.pone.0086935
Dreiseikelmann B, Bunk B, Sproer C, Rohde M, Nimtz M, Wittmann J (2017) Characterization and genome comparisons of three Achromobacter phages of the family Siphoviridae. Arch Virol 162(8):2191–2201. https://doi.org/10.1007/s00705-017-3347-8
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. https://doi.org/10.1186/1743-422X-11-14
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. https://doi.org/10.1038/srep24776
Li E, Yin Z, Ma Y, Li H, Lin W, Wei X, Zhao R, Jiang A, Yuan J, Zhao X (2016) Identification and molecular characterization of bacteriophage phiAxp-2 of Achromobacter xylosoxidans. Sci Rep 6:34300. https://doi.org/10.1038/srep34300
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. https://doi.org/10.1038/srep21943
Ceyssens PJ, Lavigne R, Mattheus W, Chibeu A, Hertveldt K, Mast J, Robben J, Volckaert G (2006) Genomic analysis of Pseudomonas aeruginosa phages LKD16 and LKA1: establishment of the phiKMV subgroup within the T7 supergroup. J Bacteriol 188(19):6924–6931. https://doi.org/10.1128/JB.00831-06
Spilker T, Vandamme P, Lipuma JJ (2012) A multilocus sequence typing scheme implies population structure and reveals several putative novel Achromobacter species. J Clin Microbiol 50(9):3010–3015. https://doi.org/10.1128/JCM.00814-12
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. https://doi.org/10.1186/1471-2164-9-75
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. https://doi.org/10.1007/s00705-015-2609-6
Schattner P, Brooks AN, Lowe TM (2005) The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Res 33:W686–W689. https://doi.org/10.1093/nar/gki366(Web Server issue)
Bailly-Bechet M, Vergassola M, Rocha E (2007) Causes for the intriguing presence of tRNAs in phages. Genome Res 17(10):1486–1495. https://doi.org/10.1101/gr.6649807
Kawasaki T, Narulita E, Matsunami M, Ishikawa H, Shimizu M, Fujie M, Bhunchoth A, Phironrit N, Chatchawankanphanich O, Yamada T (2016) Genomic diversity of large-plaque-forming podoviruses infecting the phytopathogen Ralstonia solanacearum. Virology 492:73–81. https://doi.org/10.1016/j.virol.2016.02.011
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. https://doi.org/10.1128/JB.01441-07
Essoh C, Latino L, Midoux C, Blouin Y, Loukou G, Nguetta SP, Lathro S, Cablanmian A, Kouassi AK, Vergnaud G, Pourcel C (2015) Investigation of a large collection of Pseudomonas aeruginosa bacteriophages collected from a single environmental source in Abidjan, Côte d’Ivoire. PLoS One 10(6):e0130548. https://doi.org/10.1371/journal.pone.0130548
Kutter E (2009) Phage host range and efficiency of plating. Methods Mol Biol 501:141–149. https://doi.org/10.1007/978-1-60327-164-6_14
We thank Pr. Sylvain Godreuil from the CHU de Montpellier, France, for providing the Achromobacter xylosoxidans isolates. This research was funded by a grant from Direction Générale de l’Armement (DGA) and Agence Nationale de la Recherche (ANR, France) “Resisphage” ANR-13-ASTRID-0011-01. This work was also supported by Programme d’Appui Statégique à la Recherche Scientifique (PASRES) of Côte d’Ivoire. The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication. This work has benefited from facilities and expertise of the high-throughput sequencing core facility of I2BC (Centre de Recherche de Gif—http://www.i2bc.paris-saclay.fr/) and of Imagerie‐Gif core facility supported by l’Agence Nationale de la Recherche (ANR-11-EQPX-0029/Morphoscope, ANR-10-INBS-04/FranceBioImaging; ANR‐11‐IDEX‐0003‐02/ Saclay Plant Sciences. This publication made use of the PubMLST website (https://pubmlst.org/) developed by Keith Jolley (Jolley et al. Wellcome Open Res 2018, 3:124), funded by the Wellcome Trust and located at the University of Oxford.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Handling Editor: Johannes Wittmann.
Electronic supplementary material
Below is the link to the electronic supplementary material.
About this article
Cite this article
Essoh, C., Vernadet, J., Vergnaud, G. et al. Characterization of sixteen Achromobacter xylosoxidans phages from Abidjan, Côte d’Ivoire, isolated on a single clinical strain. Arch Virol 165, 725–730 (2020). https://doi.org/10.1007/s00705-019-04511-7