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Genetic and Phenotypic Diversity of Morganella morganii Isolated From Cheese
Lorenz Timo Ryser1,2, Emmanuelle Arias-Roth2, Vincent Perreten3
1Interfaculty Bioinformatics Unit and Swiss Institute of Bioinformatics, University of Bern, Bern, Switzerland.
Abstract:
The bacterium Morganella morganii can produce the biogenic amines (BA) cadaverine, putrescine, and histamine in vitro and is responsible for high histamine concentrations in fish products. These BA can have toxic effects upon ingestion and are undesired in food. The purpose of this study was to characterize the phenotype and genotype of 11 M. morganii isolated from cheese in regard to the BA formation. In addition, we investigated the phylogeny, trehalose fermentation ability, and antibiotic resistance of the cheese isolates. To do so, we sequenced their genomes using both long and short read technologies. Due to the presence of the trehalose operon and the ability to ferment trehalose, the cheese isolates can be assigned to the subsp. sibonii. Comparative genomics with public available M. morganii genomes shows that the genomes of the cheese isolates cluster together with other subsp. sibonii genomes. All genomes between subsp. morganii and subsp. sibonii are separated by an average nucleotide identity (ANI) of less than 95.0%. Therefore, the subspecies could represent two distinct species. Nine of the strains decarboxylated lysine yielding cadaverine in vitro. This metabolic activity is linked to a previously unknown gene cluster comprising genes encoding a lysine-tRNA ligase (lysS), an HTH-transcriptional regulator (argP), a cadaverine-lysine antiporter (cadB), and a lysine decarboxylase (cadA). The formation of putrescine is linked to the speF gene encoding an ornithine decarboxylase. The gene is disrupted in five strains by an insertion sequence, and these strains only exhibit a weak putrescine production. Antimicrobial susceptibility profiling revealed that all cheese strains are resistant to tetracycline, chloramphenicol, tigecycline, colistin, and ampicillin. These phenotypes, except for colistin which is intrinsic, could be linked to antimicrobial resistance genes located on the chromosome.
Insights
This study characterizes cheese-isolated Morganella morganii, identifying a new gene cluster for cadaverine production and confirming subspecies sibonii classification. The findings highlight potential food safety concerns due to biogenic amine formation and antibiotic resistance.
Area of Science:
- Microbiology
- Food Safety
- Genomics
Background:
- Morganella morganii produces biogenic amines (BA), including histamine, cadaverine, and putrescine, which are toxic and undesirable in food.
- M. morganii is implicated in high histamine levels in fish products, posing a food safety risk.
Purpose of the Study:
- To phenotypically and genotypically characterize 11 M. morganii strains isolated from cheese regarding biogenic amine formation.
- To investigate the phylogeny, trehalose fermentation, and antibiotic resistance of these cheese isolates.
- To identify genetic determinants responsible for BA production in M. morganii.
Main Methods:
- Whole-genome sequencing using long and short read technologies.
- Comparative genomics with public M. morganii genomes.
- Phenotypic characterization including trehalose fermentation and antimicrobial susceptibility profiling.
Main Results:
- Cheese isolates were assigned to M. morganii subsp. sibonii based on the trehalose operon and fermentation ability.
- Comparative genomics revealed distinct clustering of subsp. morganii and subsp. sibonii, suggesting they may be separate species.
- A novel gene cluster (lysS, argP, cadB, cadA) associated with cadaverine production was identified.
- Putrescine production is linked to the speF gene, with disruptions observed in some strains.
- All cheese strains exhibited resistance to tetracycline, chloramphenicol, tigecycline, colistin, and ampicillin, potentially due to chromosomal antimicrobial resistance genes.
Conclusions:
- M. morganii subsp. sibonii represents a distinct phylogenetic and genomic lineage within M. morganii.
- The identified gene cluster provides insight into the mechanism of cadaverine production.
- The observed antibiotic resistance profiles in cheese isolates warrant further investigation for food safety implications.
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