<named-content content-type="genus-species">Acinetobacter baumannii</named-content> NCIMB8209: a Rare Environmental Strain Displaying Extensive Insertion Sequence-Mediated Genome Remodeling Resulting in the Loss of Exposed Cell Structures and Defensive Mechanisms

ABSTRACT Acinetobacter baumannii represents nowadays an important nosocomial pathogen of poorly defined reservoirs outside the clinical setting. Here, we conducted whole-genome sequencing analysis of the Acinetobacter sp. NCIMB8209 collection strain, isolated in 1943 from the aerobic degradation (re...

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Autores principales:	Guillermo D. Repizo, Martín Espariz, Joana L. Seravalle, Juan Ignacio Díaz Miloslavich, Bruno A. Steimbrüch, Howard A. Shuman, Alejandro M. Viale
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	environmental Acinetobacter baumannii preantibiotic-era Acinetobacter baumannii environmental reservoirs comparative genomics insertion sequences virulence factors Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/fa65870e34484a95ab9d03bb89425d30
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spelling	oai:doaj.org-article:fa65870e34484a95ab9d03bb89425d302021-11-15T15:30:50Z<named-content content-type="genus-species">Acinetobacter baumannii</named-content> NCIMB8209: a Rare Environmental Strain Displaying Extensive Insertion Sequence-Mediated Genome Remodeling Resulting in the Loss of Exposed Cell Structures and Defensive Mechanisms10.1128/mSphere.00404-202379-5042https://doaj.org/article/fa65870e34484a95ab9d03bb89425d302020-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00404-20https://doaj.org/toc/2379-5042ABSTRACT Acinetobacter baumannii represents nowadays an important nosocomial pathogen of poorly defined reservoirs outside the clinical setting. Here, we conducted whole-genome sequencing analysis of the Acinetobacter sp. NCIMB8209 collection strain, isolated in 1943 from the aerobic degradation (retting) of desert guayule shrubs. Strain NCIMB8209 contained a 3.75-Mb chromosome and a plasmid of 134 kb. Phylogenetic analysis based on core genes indicated NCIMB8209 affiliation to A. baumannii, a result supported by the identification of a chromosomal blaOXA-51-like gene. Seven genomic islands lacking antimicrobial resistance determinants, 5 regions encompassing phage-related genes, and notably, 93 insertion sequences (IS) were found in this genome. NCIMB8209 harbors most genes linked to persistence and virulence described in contemporary A. baumannii clinical strains, but many of the genes encoding components of surface structures are interrupted by IS. Moreover, defense genetic islands against biological aggressors such as type 6 secretion systems or CRISPR-cas are absent from this genome. These findings correlate with a low capacity of NCIMB8209 to form biofilm and pellicle, low motility on semisolid medium, and low virulence toward Galleria mellonella and Caenorhabditis elegans. Searching for catabolic genes and concomitant metabolic assays revealed the ability of NCIMB8209 to grow on a wide range of substances produced by plants, including aromatic acids and defense compounds against external aggressors. All the above features strongly suggest that NCIMB8209 has evolved specific adaptive features to a particular environmental niche. Moreover, they also revealed that the remarkable genetic plasticity identified in contemporary A. baumannii clinical strains represents an intrinsic characteristic of the species. IMPORTANCE Acinetobacter baumannii is an ESKAPE (Enterococcus faecium, Staphylococcus aureus, Klebsiella pneumoniae, Acinetobacter baumannii, Pseudomonas aeruginosa, and Enterobacter species) opportunistic pathogen, with poorly defined natural habitats/reservoirs outside the clinical setting. A. baumannii arose from the Acinetobacter calcoaceticus-A. baumannii complex as the result of a population bottleneck, followed by a recent population expansion from a few clinically relevant clones endowed with an arsenal of resistance and virulence genes. Still, the identification of virulence traits and the evolutionary paths leading to a pathogenic lifestyle has remained elusive, and thus, the study of nonclinical (“environmental”) A. baumannii isolates is necessary. We conducted here comparative genomic and virulence studies on A. baumannii NCMBI8209 isolated in 1943 from the microbiota responsible for the decomposition of guayule, and therefore well differentiated both temporally and epidemiologically from the multidrug-resistant strains that are predominant nowadays. Our work provides insights on the adaptive strategies used by A. baumannii to escape from host defenses and may help the adoption of measures aimed to limit its further dissemination.Guillermo D. RepizoMartín EsparizJoana L. SeravalleJuan Ignacio Díaz MiloslavichBruno A. SteimbrüchHoward A. ShumanAlejandro M. VialeAmerican Society for Microbiologyarticleenvironmental Acinetobacter baumanniipreantibiotic-era Acinetobacter baumanniienvironmental reservoirscomparative genomicsinsertion sequencesvirulence factorsMicrobiologyQR1-502ENmSphere, Vol 5, Iss 4 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	environmental Acinetobacter baumannii preantibiotic-era Acinetobacter baumannii environmental reservoirs comparative genomics insertion sequences virulence factors Microbiology QR1-502
spellingShingle	environmental Acinetobacter baumannii preantibiotic-era Acinetobacter baumannii environmental reservoirs comparative genomics insertion sequences virulence factors Microbiology QR1-502 Guillermo D. Repizo Martín Espariz Joana L. Seravalle Juan Ignacio Díaz Miloslavich Bruno A. Steimbrüch Howard A. Shuman Alejandro M. Viale <named-content content-type="genus-species">Acinetobacter baumannii</named-content> NCIMB8209: a Rare Environmental Strain Displaying Extensive Insertion Sequence-Mediated Genome Remodeling Resulting in the Loss of Exposed Cell Structures and Defensive Mechanisms
description	ABSTRACT Acinetobacter baumannii represents nowadays an important nosocomial pathogen of poorly defined reservoirs outside the clinical setting. Here, we conducted whole-genome sequencing analysis of the Acinetobacter sp. NCIMB8209 collection strain, isolated in 1943 from the aerobic degradation (retting) of desert guayule shrubs. Strain NCIMB8209 contained a 3.75-Mb chromosome and a plasmid of 134 kb. Phylogenetic analysis based on core genes indicated NCIMB8209 affiliation to A. baumannii, a result supported by the identification of a chromosomal blaOXA-51-like gene. Seven genomic islands lacking antimicrobial resistance determinants, 5 regions encompassing phage-related genes, and notably, 93 insertion sequences (IS) were found in this genome. NCIMB8209 harbors most genes linked to persistence and virulence described in contemporary A. baumannii clinical strains, but many of the genes encoding components of surface structures are interrupted by IS. Moreover, defense genetic islands against biological aggressors such as type 6 secretion systems or CRISPR-cas are absent from this genome. These findings correlate with a low capacity of NCIMB8209 to form biofilm and pellicle, low motility on semisolid medium, and low virulence toward Galleria mellonella and Caenorhabditis elegans. Searching for catabolic genes and concomitant metabolic assays revealed the ability of NCIMB8209 to grow on a wide range of substances produced by plants, including aromatic acids and defense compounds against external aggressors. All the above features strongly suggest that NCIMB8209 has evolved specific adaptive features to a particular environmental niche. Moreover, they also revealed that the remarkable genetic plasticity identified in contemporary A. baumannii clinical strains represents an intrinsic characteristic of the species. IMPORTANCE Acinetobacter baumannii is an ESKAPE (Enterococcus faecium, Staphylococcus aureus, Klebsiella pneumoniae, Acinetobacter baumannii, Pseudomonas aeruginosa, and Enterobacter species) opportunistic pathogen, with poorly defined natural habitats/reservoirs outside the clinical setting. A. baumannii arose from the Acinetobacter calcoaceticus-A. baumannii complex as the result of a population bottleneck, followed by a recent population expansion from a few clinically relevant clones endowed with an arsenal of resistance and virulence genes. Still, the identification of virulence traits and the evolutionary paths leading to a pathogenic lifestyle has remained elusive, and thus, the study of nonclinical (“environmental”) A. baumannii isolates is necessary. We conducted here comparative genomic and virulence studies on A. baumannii NCMBI8209 isolated in 1943 from the microbiota responsible for the decomposition of guayule, and therefore well differentiated both temporally and epidemiologically from the multidrug-resistant strains that are predominant nowadays. Our work provides insights on the adaptive strategies used by A. baumannii to escape from host defenses and may help the adoption of measures aimed to limit its further dissemination.
format	article
author	Guillermo D. Repizo Martín Espariz Joana L. Seravalle Juan Ignacio Díaz Miloslavich Bruno A. Steimbrüch Howard A. Shuman Alejandro M. Viale
author_facet	Guillermo D. Repizo Martín Espariz Joana L. Seravalle Juan Ignacio Díaz Miloslavich Bruno A. Steimbrüch Howard A. Shuman Alejandro M. Viale
author_sort	Guillermo D. Repizo
title	<named-content content-type="genus-species">Acinetobacter baumannii</named-content> NCIMB8209: a Rare Environmental Strain Displaying Extensive Insertion Sequence-Mediated Genome Remodeling Resulting in the Loss of Exposed Cell Structures and Defensive Mechanisms
title_short	<named-content content-type="genus-species">Acinetobacter baumannii</named-content> NCIMB8209: a Rare Environmental Strain Displaying Extensive Insertion Sequence-Mediated Genome Remodeling Resulting in the Loss of Exposed Cell Structures and Defensive Mechanisms
title_full	<named-content content-type="genus-species">Acinetobacter baumannii</named-content> NCIMB8209: a Rare Environmental Strain Displaying Extensive Insertion Sequence-Mediated Genome Remodeling Resulting in the Loss of Exposed Cell Structures and Defensive Mechanisms
title_fullStr	<named-content content-type="genus-species">Acinetobacter baumannii</named-content> NCIMB8209: a Rare Environmental Strain Displaying Extensive Insertion Sequence-Mediated Genome Remodeling Resulting in the Loss of Exposed Cell Structures and Defensive Mechanisms
title_full_unstemmed	<named-content content-type="genus-species">Acinetobacter baumannii</named-content> NCIMB8209: a Rare Environmental Strain Displaying Extensive Insertion Sequence-Mediated Genome Remodeling Resulting in the Loss of Exposed Cell Structures and Defensive Mechanisms
title_sort	<named-content content-type="genus-species">acinetobacter baumannii</named-content> ncimb8209: a rare environmental strain displaying extensive insertion sequence-mediated genome remodeling resulting in the loss of exposed cell structures and defensive mechanisms
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/fa65870e34484a95ab9d03bb89425d30
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<named-content content-type="genus-species">Acinetobacter baumannii</named-content> NCIMB8209: a Rare Environmental Strain Displaying Extensive Insertion Sequence-Mediated Genome Remodeling Resulting in the Loss of Exposed Cell Structures and Defensive Mechanisms

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