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Scandinavium Goeteborgense Gen. Nov., Sp. Nov., a New Member of the Family Enterobacteriaceae Isolated from a Wound Infection, C

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Scandinavium Goeteborgense Gen. Nov., Sp. Nov., a New Member of the Family Enterobacteriaceae Isolated from a Wound Infection, C fmicb-10-02511 November 2, 2019 Time: 13:9 # 1 ORIGINAL RESEARCH published: 05 November 2019 doi: 10.3389/fmicb.2019.02511 Scandinavium goeteborgense gen. nov., sp. nov., a New Member of the Family Enterobacteriaceae Isolated From a Wound Infection, Carries a Novel Quinolone Resistance Gene Variant Edited by: 1,2,3† 2,3,4,5† 2,3,6 Iain Sutcliffe, Nachiket P. Marathe , Francisco Salvà-Serra , Roger Karlsson , 2,3 2,3,4 2,3 Northumbria University, D. G. Joakim Larsson , Edward R. B. Moore , Liselott Svensson-Stadler and United Kingdom Hedvig E. Jakobsson2,3* Reviewed by: 1 Institute of Marine Research, Bergen, Norway, 2 Department of Infectious Diseases, Sahlgrenska Academy, University Aharon Oren, of Gothenburg, Gothenburg, Sweden, 3 Centre for Antibiotic Resistance Research, University of Gothenburg, Gothenburg, Hebrew University of Jerusalem, Israel Sweden, 4 Department of Clinical Microbiology, Culture Collection University of Gothenburg, Sahlgrenska University Hospital Marike Palmer, and Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden, 5 Microbiology, Department of Biology, University of Nevada, Las Vegas, University of the Balearic Islands, Palma de Mallorca, Spain, 6 Nanoxis Consulting AB, Gothenburg, Sweden United States *Correspondence: Hedvig E. Jakobsson The family Enterobacteriaceae is a taxonomically diverse and widely distributed family [email protected] containing many human commensal and pathogenic species that are known to †These authors have contributed carry transferable antibiotic resistance determinants. Characterization of novel taxa equally to this work within this family is of great importance in order to understand the associated health Specialty section: risk and provide better treatment options. The aim of the present study was to This article was submitted to characterize a Gram-negative bacterial strain (CCUG 66741) belonging to the family Evolutionary and Genomic Enterobacteriaceae, isolated from a wound infection of an adult patient, in Sweden. Microbiology, a section of the journal Initial phenotypic and genotypic analyses identified the strain as a member of the family Frontiers in Microbiology Enterobacteriaceae but could not assign it to any previously described species. The Received: 07 August 2019 complete 16S rRNA gene sequence showed highest similarity (98.8%) to four species. Accepted: 18 October 2019 Published: 05 November 2019 Whole genome sequencing followed by in silico DNA-DNA similarity analysis and Citation: average nucleotide identity (ANI) analysis confirmed that strain CCUG 66741 represents Marathe NP, Salvà-Serra F, a novel taxon. Sequence comparisons of six house-keeping genes (16S rRNA, atpD, Karlsson R, Larsson DGJ, dnaJ, gyrB, infB, rpoB) with those of the type strains of the type species of related Moore ERB, Svensson-Stadler L and Jakobsson HE (2019) Scandinavium genera within the family Enterobacteriaceae indicated that the strain embodies a novel goeteborgense gen. nov., sp. nov., species within the family. Phylogenomic analyses (ANI-based and core genome-based a New Member of the Family Enterobacteriaceae Isolated From phylogeny) showed that strain CCUG 66741 forms a distinct clade, representing a a Wound Infection, Carries a Novel novel species of a distinct, new genus within the family Enterobacteriaceae, for which Quinolone Resistance Gene Variant. the name Scandinavium goeteborgense gen. nov., sp. nov. is proposed, with CCUG Front. Microbiol. 10:2511. T T T doi: 10.3389/fmicb.2019.02511 66741 as the type strain (= CECT 9823 = NCTC 14286 ). S. goeteborgense CCUG Frontiers in Microbiology| www.frontiersin.org 1 November 2019| Volume 10| Article 2511 fmicb-10-02511 November 2, 2019 Time: 13:9 # 2 Marathe et al. Scandinavium goeteborgense gen. nov., sp., nov., a New Member of the Family Enterobacteriaceae 66741T carries a novel variant of a chromosomally-encoded quinolone resistance gene (proposed qnrB96). When expressed in Escherichia coli, the qnrB96 gene conferred five-fold increase in minimum inhibitory concentration against ciprofloxacin. This study highlights the importance and the utility of whole genome sequencing for pathogen identification in clinical settings. Keywords: novel genus, novel species, Enterobacteriaceae, quinolone resistance, wound infection, antibiotic resistance, phylogenomics, taxonomy INTRODUCTION RESULTS The family Enterobacteriaceae is a large and taxonomically Strain Isolation and Characterization diverse group of Gram-negative rod-shaped bacteria within Strain CCUG 66741T was isolated from a wound infection of the class Gammaproteobacteria and order Enterobacteriales an adult patient, which was sampled in Kungälv, Sweden. that includes many common human pathogens (Hata et al., The colonies on Columbia Blood Agar, after 24 h of 2016). Numerous genera within the Enterobacteriaceae incubation at 30◦C, were 2–3 mm in size, circular, moist, family are recognized to be polyphyletic, based on the and smooth. Cells were Gram-negative, rod-shaped, around 16S rRNA gene (Brady et al., 2008; Kämpfer et al., 2015; 2 mm in length and around 1 mm in width. The strain Alnajar and Gupta, 2017), hence multilocus sequence analyses was typed using MALDI-TOF MS at the Department of (MLSA) based on several house-keeping gene sequences Clinical Microbiology of the Sahlgrenska University Hospital have been proposed for reliable classification of isolates (Gothenburg, Sweden), using the IVD-Database Knowledge Base and strains within this family (Brady et al., 2013). The v2 (bioMérieux, Marcy-l’Étoile, France). The typing analysis advent of next-generation sequencing and whole genome could not assign strain CCUG 66741T to any species, with sequencing (WGS) analysis has significantly impacted the Escherichia vulneris being identified as the most similar species, taxonomic classification of Enterobacteriaceae members. although with a confidence value of 74.4%, which is below Recently, using whole genome-based phylogeny and taxonomy, the 90% threshold for species identification recommended some members of this family have been reclassified into by the manufacturer. API R ID 32E metabolic profiling with separate and novel families (e.g., Budviciaceae, Erwiniaceae, StrainMatcher, indicated that the most closely-related species Hafniaceae, Morganellaceae, Pectobacteriaceae, Yersiniaceae), (i.e., those with lowest StrainMatcher scores) were Buttiauxella belonging to the order Enterobacterales (Adeolu et al., 2016). warmboldiae, Buttiauxella noackiae, Buttiauxella izardii, and Nevertheless, many species within Enterobacteriaceae are Enterobacter cancerogenus (Table 1). These results did not important human pathogens usually carrying transferable allow reliable assignation of the strain CCUG 66741T to antibiotic resistance markers (Carattoli, 2009). Indeed, the any species. World Health Organization has included carbapenem- Partial sequencing of 16S rRNA gene and dnaJ was resistant and extended-spectrum beta-lactamase-producing performed, which yielded sequences of 621 and 711 bp, Enterobacteriaceae within the Priority 1 (critical) group, in respectively. Comparative sequence analysis of the 16S rRNA the list of priority pathogens for research and development of partial gene sequence with EMBL-EBI Nucleotide Database new antibiotics (World Health Organization [WHO], 2017). and the FASTA search tool (Madeira et al., 2019), showed a Thus, taxonomic description of novel members of the family is highest similarity value of 98.7% with Buttiauxella ferragutiae important in order to understand associated health risks and to DSM 9390T, Buttiauxella agrestis DSM 4586T, Buttiauxella prevent spread of infections. izardii DSM 9397T, and Buttiauxella noackiae DSM 9401T The aim of the current study was to characterize (GenBank accession numbers: AJ233402, AJ233400, AJ233404, a Gram-negative bacterial strain (CCUG 66741) and AJ233405, respectively). The analysis of the dnaJ partial isolated from a wound infection of an adult patient in sequence showed the highest similarity value of 86.3% with Sweden. We here present a novel genus in the family Leclercia adecarboxylata GTC 1267T (GenBank accession Enterobacteriaceae: Scandinavium goeteborgense gen. nov., number: AB272662). Analyses performed by Pham et al.(2007) sp. nov., with reference to taxonomy, genome analysis and identification of a novel variant of quinolone resistance TABLE 1 | Results of the API R ID 32E analysis (bioMérieux). gene (qnrB96). Strain StrainMatcher score Abbreviations: ANI, average nucleotide identity; ANIb, average nucleotide Buttiauxella warmboldiae CCUG 35512T 20 identity based on BLAST; CFA-FAME, cell fatty acid-fatty acid methyl ester; Buttiauxella noackiae CCUG 35511T 22 MALDI-TOF MS, Matrix-Assisted Laser Desorption/Ionization-Time Of Flight T Mass Spectrometry; MLSA, multilocus sequence analysis; qnr, quinolone Buttiauxella izardii CCUG 35510 28 resistance; WGS, whole genome sequencing. Enterobacter cancerogenus CCUG 25231T 38 Frontiers in Microbiology| www.frontiersin.org 2 November 2019| Volume 10| Article 2511 fmicb-10-02511 November 2, 2019 Time: 13:9 # 3 Marathe et al. Scandinavium goeteborgense gen. nov., sp., nov., a New Member of the Family Enterobacteriaceae showed that intraspecific variation of dnaJ within the family Additional Related Strain Genome Enterobacteriaceae ranges from 0 to 8.3%. Therefore, 14% Sequences sequence divergence compared with GTC L. adecarboxylata BLAST analyses, using house-keeping gene sequences of strain 1267T was considered not enough to assign strain CCUG
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