Genomic analysis of a rare recurrent Listeria monocytogenes prosthetic joint infection indicates a protected niche within biofilm on prosthetic materials

Abstract Listeria monocytogenes is a rare cause of prosthetic joint infections (PJI). In this study, we describe a case of recurrent L. monocytogenes infections, 39 months apart, following debridement and retention of a prosthetic hip. Despite numerous studies reporting persistent L. monocytogenes i...

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Autores principales: Chloe Hutchins, Lizbeth Sayavedra, Maria Diaz, Puja Gupta, Elizabeth Tissingh, Chiamaka Elumogo, John Nolan, Ian Charles, Ngozi Elumogo, Arjan Narbad
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Publicado: Nature Portfolio 2021
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spelling oai:doaj.org-article:6f4b766e499a4370b22926a336db1ef52021-11-14T12:24:11ZGenomic analysis of a rare recurrent Listeria monocytogenes prosthetic joint infection indicates a protected niche within biofilm on prosthetic materials10.1038/s41598-021-01376-22045-2322https://doaj.org/article/6f4b766e499a4370b22926a336db1ef52021-11-01T00:00:00Zhttps://doi.org/10.1038/s41598-021-01376-2https://doaj.org/toc/2045-2322Abstract Listeria monocytogenes is a rare cause of prosthetic joint infections (PJI). In this study, we describe a case of recurrent L. monocytogenes infections, 39 months apart, following debridement and retention of a prosthetic hip. Despite numerous studies reporting persistent L. monocytogenes in human infections, the genomic and phenotypic changes that clinically relevant strains undergo in the host are poorly understood. Improved knowledge of how PJI occurs is needed to improve the management of prosthetic infections. We used a combination of long- and short-read sequencing to identify any potential genomic differences between two L. monocytogenes isolates that occurred over 39-month incubation in the host. The isolates, QI0054 and QI0055, showed three single nucleotide polymorphisms and three insertions or deletions, suggesting that the recurrent infection was caused by the same strain. To identify potential differences in the capacity for persistence of these isolates, their biofilm-forming ability and potential to colonize prosthesis-relevant materials was investigated both in microtitre plates and on prosthetic material titanium, stainless steel 316 and ultra-high molecular weight polyethylene. Whilst the L. monocytogenes isolate from the most recent infection (QI0055) was able to form higher biofilm in microtitre plates, this did not lead to an increase in biomass on prosthetic joint materials compared to the initial isolate (QI0054). Both clinical isolates were able to form significantly more biofilm on the two metal prosthetic materials than on the ultra-high molecular weight polyethylene, in contrast to reference strain Scott A. Transcriptomics revealed 41 genes overexpressed in biofilm state and 643 in planktonic state. Moreover, genes with mutations were actively expressed in both isolates. We conclude the isolates are derived from the same strain and hypothesize that L. monocytogenes formed biofilm on the prosthetic joint materials, with minimal exposure to stresses, which permitted their survival and growth.Chloe HutchinsLizbeth SayavedraMaria DiazPuja GuptaElizabeth TissinghChiamaka ElumogoJohn NolanIan CharlesNgozi ElumogoArjan NarbadNature PortfolioarticleMedicineRScienceQENScientific Reports, Vol 11, Iss 1, Pp 1-11 (2021)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
Chloe Hutchins
Lizbeth Sayavedra
Maria Diaz
Puja Gupta
Elizabeth Tissingh
Chiamaka Elumogo
John Nolan
Ian Charles
Ngozi Elumogo
Arjan Narbad
Genomic analysis of a rare recurrent Listeria monocytogenes prosthetic joint infection indicates a protected niche within biofilm on prosthetic materials
description Abstract Listeria monocytogenes is a rare cause of prosthetic joint infections (PJI). In this study, we describe a case of recurrent L. monocytogenes infections, 39 months apart, following debridement and retention of a prosthetic hip. Despite numerous studies reporting persistent L. monocytogenes in human infections, the genomic and phenotypic changes that clinically relevant strains undergo in the host are poorly understood. Improved knowledge of how PJI occurs is needed to improve the management of prosthetic infections. We used a combination of long- and short-read sequencing to identify any potential genomic differences between two L. monocytogenes isolates that occurred over 39-month incubation in the host. The isolates, QI0054 and QI0055, showed three single nucleotide polymorphisms and three insertions or deletions, suggesting that the recurrent infection was caused by the same strain. To identify potential differences in the capacity for persistence of these isolates, their biofilm-forming ability and potential to colonize prosthesis-relevant materials was investigated both in microtitre plates and on prosthetic material titanium, stainless steel 316 and ultra-high molecular weight polyethylene. Whilst the L. monocytogenes isolate from the most recent infection (QI0055) was able to form higher biofilm in microtitre plates, this did not lead to an increase in biomass on prosthetic joint materials compared to the initial isolate (QI0054). Both clinical isolates were able to form significantly more biofilm on the two metal prosthetic materials than on the ultra-high molecular weight polyethylene, in contrast to reference strain Scott A. Transcriptomics revealed 41 genes overexpressed in biofilm state and 643 in planktonic state. Moreover, genes with mutations were actively expressed in both isolates. We conclude the isolates are derived from the same strain and hypothesize that L. monocytogenes formed biofilm on the prosthetic joint materials, with minimal exposure to stresses, which permitted their survival and growth.
format article
author Chloe Hutchins
Lizbeth Sayavedra
Maria Diaz
Puja Gupta
Elizabeth Tissingh
Chiamaka Elumogo
John Nolan
Ian Charles
Ngozi Elumogo
Arjan Narbad
author_facet Chloe Hutchins
Lizbeth Sayavedra
Maria Diaz
Puja Gupta
Elizabeth Tissingh
Chiamaka Elumogo
John Nolan
Ian Charles
Ngozi Elumogo
Arjan Narbad
author_sort Chloe Hutchins
title Genomic analysis of a rare recurrent Listeria monocytogenes prosthetic joint infection indicates a protected niche within biofilm on prosthetic materials
title_short Genomic analysis of a rare recurrent Listeria monocytogenes prosthetic joint infection indicates a protected niche within biofilm on prosthetic materials
title_full Genomic analysis of a rare recurrent Listeria monocytogenes prosthetic joint infection indicates a protected niche within biofilm on prosthetic materials
title_fullStr Genomic analysis of a rare recurrent Listeria monocytogenes prosthetic joint infection indicates a protected niche within biofilm on prosthetic materials
title_full_unstemmed Genomic analysis of a rare recurrent Listeria monocytogenes prosthetic joint infection indicates a protected niche within biofilm on prosthetic materials
title_sort genomic analysis of a rare recurrent listeria monocytogenes prosthetic joint infection indicates a protected niche within biofilm on prosthetic materials
publisher Nature Portfolio
publishDate 2021
url https://doaj.org/article/6f4b766e499a4370b22926a336db1ef5
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