Genome sequence-based identification of Enterobacter strains and description of Enterobacter pasteurii sp. nov.

ABSTRACT Members of the Enterobacter cloacae complex (ECC) are almost ubiquitous in nature and can act as pathogens. In this study, we used a polyphasic taxonomy approach to establish the accurate taxonomic position of six strains within the ECC. Notably, the 16S rRNA gene-based phylogeny failed to...

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Main Authors: Praveen Rahi, Estelle Mühle, Cyril Scandola, Gerald Touak, Dominique Clermont
Format: Article
Language:English
Published: American Society for Microbiology 2024-01-01
Series:Microbiology Spectrum
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/spectrum.03150-23
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author Praveen Rahi
Estelle Mühle
Cyril Scandola
Gerald Touak
Dominique Clermont
author_facet Praveen Rahi
Estelle Mühle
Cyril Scandola
Gerald Touak
Dominique Clermont
author_sort Praveen Rahi
collection DOAJ
description ABSTRACT Members of the Enterobacter cloacae complex (ECC) are almost ubiquitous in nature and can act as pathogens. In this study, we used a polyphasic taxonomy approach to establish the accurate taxonomic position of six strains within the ECC. Notably, the 16S rRNA gene-based phylogeny failed to group all Enterobacter species into a monophyletic cluster. As an alternative to this, we explored genome sequence-based phylogenetic approaches. The bac120 gene-based phylogeny successfully grouped all Enterobacter species into a monophyletic cluster, although some species-level clustering conflicted with average nucleotide identity (ANI) values. Furthermore, the Enterobacter-specific core gene phylogeny resolved all species, aligning with ANI results. Three strains were identified as Enterobacter asburiae, while strain P99 was classified as “Enterobacter xiangfangensis” and strain C45 as Enterobacter quasihormaechei. Conversely, strain A-8T formed a distinct cluster in all phylogenies, with ANI and digital DNA-DNA hybridization (dDDH) values below the species threshold (<92% and <44%, respectively) with all known Enterobacter species. Matrix-assisted laser desorption/ionization time-of-flight mass spectrometry biotyper results confirmed that all strains belonged to the ECC. However, the comparison of mean spectrum profile of strain A-8T with those of other strains revealed the presence of 18 unique peaks, highlighting its distinct protein profile. Based on comprehensive genotypic and phenotypic characterizations, we propose that strain A-8T is a new species of the genus Enterobacter, which is named Enterobacter pasteurii sp. nov. The type strain is A-8T (CIP 103550T; ATCC 23355T; DSM 26481T; and WDCM 00082T). This study advances our understanding of the ECC, emphasizing the need for multidimensional taxonomic techniques and contributing to the better management of microbial resource centers. IMPORTANCE Accurate taxonomy is essential for microbial biological resource centers, since the microbial resources are often used to support new discoveries and subsequent research. Here, we used genome sequence data, alongside matrix-assisted laser desorption/ionization time-of-flight mass spectrometer biotyper-based protein profiling, to accurately identify six Enterobacter cloacae complex strains. This approach effectively identified distinct species within the E. cloacae complex, including Enterobacter asburiae, “Enterobacter xiangfangensis,” and Enterobacter quasihormaechei. Moreover, the study revealed the existence of a novel species within the Enterobacter genus, for which we proposed the name Enterobacter pasteurii sp. nov. In summary, this study demonstrates the significance of adopting a genome sequence-driven taxonomy approach for the precise identification of bacterial strains in a biological resource center and expands our understanding of the E. cloacae complex.
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spelling doaj.art-e290e5258689466d9ce8ae4dc8a812182024-01-11T14:04:36ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972024-01-0112110.1128/spectrum.03150-23Genome sequence-based identification of Enterobacter strains and description of Enterobacter pasteurii sp. nov.Praveen Rahi0Estelle Mühle1Cyril Scandola2Gerald Touak3Dominique Clermont4Collection of Institut Pasteur (CIP), Institut Pasteur, Université Paris Cité , Paris, FranceCollection of Institut Pasteur (CIP), Institut Pasteur, Université Paris Cité , Paris, FranceUltrastructural Bioimaging Unit, Institut Pasteur, Université Paris Cité , Paris, FranceCollection of Institut Pasteur (CIP), Institut Pasteur, Université Paris Cité , Paris, FranceCollection of Institut Pasteur (CIP), Institut Pasteur, Université Paris Cité , Paris, FranceABSTRACT Members of the Enterobacter cloacae complex (ECC) are almost ubiquitous in nature and can act as pathogens. In this study, we used a polyphasic taxonomy approach to establish the accurate taxonomic position of six strains within the ECC. Notably, the 16S rRNA gene-based phylogeny failed to group all Enterobacter species into a monophyletic cluster. As an alternative to this, we explored genome sequence-based phylogenetic approaches. The bac120 gene-based phylogeny successfully grouped all Enterobacter species into a monophyletic cluster, although some species-level clustering conflicted with average nucleotide identity (ANI) values. Furthermore, the Enterobacter-specific core gene phylogeny resolved all species, aligning with ANI results. Three strains were identified as Enterobacter asburiae, while strain P99 was classified as “Enterobacter xiangfangensis” and strain C45 as Enterobacter quasihormaechei. Conversely, strain A-8T formed a distinct cluster in all phylogenies, with ANI and digital DNA-DNA hybridization (dDDH) values below the species threshold (<92% and <44%, respectively) with all known Enterobacter species. Matrix-assisted laser desorption/ionization time-of-flight mass spectrometry biotyper results confirmed that all strains belonged to the ECC. However, the comparison of mean spectrum profile of strain A-8T with those of other strains revealed the presence of 18 unique peaks, highlighting its distinct protein profile. Based on comprehensive genotypic and phenotypic characterizations, we propose that strain A-8T is a new species of the genus Enterobacter, which is named Enterobacter pasteurii sp. nov. The type strain is A-8T (CIP 103550T; ATCC 23355T; DSM 26481T; and WDCM 00082T). This study advances our understanding of the ECC, emphasizing the need for multidimensional taxonomic techniques and contributing to the better management of microbial resource centers. IMPORTANCE Accurate taxonomy is essential for microbial biological resource centers, since the microbial resources are often used to support new discoveries and subsequent research. Here, we used genome sequence data, alongside matrix-assisted laser desorption/ionization time-of-flight mass spectrometer biotyper-based protein profiling, to accurately identify six Enterobacter cloacae complex strains. This approach effectively identified distinct species within the E. cloacae complex, including Enterobacter asburiae, “Enterobacter xiangfangensis,” and Enterobacter quasihormaechei. Moreover, the study revealed the existence of a novel species within the Enterobacter genus, for which we proposed the name Enterobacter pasteurii sp. nov. In summary, this study demonstrates the significance of adopting a genome sequence-driven taxonomy approach for the precise identification of bacterial strains in a biological resource center and expands our understanding of the E. cloacae complex.https://journals.asm.org/doi/10.1128/spectrum.03150-23EnterobacterEnterobacteriaceaeMALDI-TOF MSphylogenomictaxonomy
spellingShingle Praveen Rahi
Estelle Mühle
Cyril Scandola
Gerald Touak
Dominique Clermont
Genome sequence-based identification of Enterobacter strains and description of Enterobacter pasteurii sp. nov.
Microbiology Spectrum
Enterobacter
Enterobacteriaceae
MALDI-TOF MS
phylogenomic
taxonomy
title Genome sequence-based identification of Enterobacter strains and description of Enterobacter pasteurii sp. nov.
title_full Genome sequence-based identification of Enterobacter strains and description of Enterobacter pasteurii sp. nov.
title_fullStr Genome sequence-based identification of Enterobacter strains and description of Enterobacter pasteurii sp. nov.
title_full_unstemmed Genome sequence-based identification of Enterobacter strains and description of Enterobacter pasteurii sp. nov.
title_short Genome sequence-based identification of Enterobacter strains and description of Enterobacter pasteurii sp. nov.
title_sort genome sequence based identification of enterobacter strains and description of enterobacter pasteurii sp nov
topic Enterobacter
Enterobacteriaceae
MALDI-TOF MS
phylogenomic
taxonomy
url https://journals.asm.org/doi/10.1128/spectrum.03150-23
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