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Evolution of Listeria monocytogenes During a Persistent Human Prosthetic Hip Joint Infection.

ABSTRACT: Listeria monocytogenes associated prosthetic joint infections (PJI) are a rare but increasing clinical problem of listeriosis. We characterized two isolates of the same L. monocytogenes strain isolated within five years of each other from a recurrent human prosthetic joint infection. The two isolates although clonally identical were phenotypically distinct confirming that the original infection strain had evolved within the human host PJI environment giving rise to a phenotypically distinct variant. The recurrent PJI isolate displayed various phenotypic differences compared to the parental original PJI isolate including diminished growth and carbon source metabolism, as well as altered morphology and increased stress sensitivity. The PJI isolates were both diminished in virulence due to an identical truncation mutation in the major virulence regulator PrfA. Genome wide sequence comparison provided conclusive evidence that the two isolates were identical clonal descendants of the same L. monocytogenes strain that had evolved through acquisition of various single nucleotide polymorphisms (SNPs) as well as insertion and deletion events (InDels) during a persistent human PJI. Acquired genetic changes included a specific mutation causing premature stop codon (PMSC) and truncation of RNAse J1 protein. Based on analysis of this naturally truncated as well as other complete RNAse J1 deletion mutants we show that the long-term survival of this specific L. monocytogenes strain within the prosthetic joint might in part be explained by the rnjA PMSC mutation that diminishes virulence and activation of the host immune system in a zebrafish embryo localized infection model. Overall our analysis of this special natural case provides insights into random mutation events and molecular mechanisms that might be associated with the adaptation and short-term evolution of this specific L. monocytogenes strain within a persistent human PJI environment.

SUBMITTER: Muchaamba F

PROVIDER: S-EPMC7399150 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description: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.

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Evolution of Listeria monocytogenes During a Persistent Human Prosthetic Hip Joint Infection.

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