Metaphenotypes associated with recurrent genomic lineages of Campylobacter jejuni responsible for human infections in Luxembourg
Campylobacter jejuni is a leading cause of foodborne illnesses worldwide. Although considered fragile, this microaerophilic bacterium is able to survive in various challenging environments, which subsequently constitutes multiple sources of transmission for human infection. To test the assumption of...
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| Format: | Article |
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Frontiers Media S.A.
2022-09-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2022.901192/full |
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| author | Morgane Nennig Morgane Nennig Arnaud Clément Emmanuelle Longueval Thierry Bernardi Catherine Ragimbeau Odile Tresse |
| author_facet | Morgane Nennig Morgane Nennig Arnaud Clément Emmanuelle Longueval Thierry Bernardi Catherine Ragimbeau Odile Tresse |
| author_sort | Morgane Nennig |
| collection | DOAJ |
| description | Campylobacter jejuni is a leading cause of foodborne illnesses worldwide. Although considered fragile, this microaerophilic bacterium is able to survive in various challenging environments, which subsequently constitutes multiple sources of transmission for human infection. To test the assumption of acquiring specific features for adaptation and survival, we established a workflow of phenotypic tests related to the survival and the persistence of recurrent and sporadic strains. A representative collection of 83 strains isolated over 13 years from human, mammal, poultry, and environmental sources in Luxembourg, representing different spreading patterns (endemic, epidemic, and sporadic), was screened for survival to oxidative stresses, for acclimating to aerobic conditions (AC), and for persistence on abiotic surfaces. Using the cgMLST Oxford typing scheme for WGS data, the collection was classified into genomic lineages corresponding to host-generalist strains (lineages A and D, CC ST-21), host-specific strains (lineage B, CC ST-257 and lineage C, CC ST-464) and sporadic strains. We established that when a strain survives concentrations beyond 0.25 mM superoxide stress, it is six times more likely to survive hyperoxide stress and that a highly adherent strain is 14 times more likely to develop a biofilm. Surprisingly, more than half of the strains could acclimate to AC but this capacity does not explain the difference between recurrent genomic lineages and sporadic strains and the survival to oxidative stresses, while recurrent strains have a significantly higher adhesion/biofilm formation capacity than sporadic ones. From this work, the genomic lineages with more stable genomes could be characterized by a specific combination of phenotypes, called metaphenotypes. From the functional genomic analyses, the presence of a potentially functional T6SS in the strains of lineage D might explain the propensity of these strains to be strong biofilm producers. Our findings support the hypothesis that phenotypical abilities contribute to the spatio-temporal adaptation and survival of stable genomic lineages. It suggests a selection of better-adapted and persistent strains in challenging stress environments, which could explain the prevalence of these lineages in human infections. |
| first_indexed | 2024-04-11T21:21:58Z |
| format | Article |
| id | doaj.art-24a29586ff0f4274a23a737788799029 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-04-11T21:21:58Z |
| publishDate | 2022-09-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-24a29586ff0f4274a23a7377887990292022-12-22T04:02:36ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-09-011310.3389/fmicb.2022.901192901192Metaphenotypes associated with recurrent genomic lineages of Campylobacter jejuni responsible for human infections in LuxembourgMorgane Nennig0Morgane Nennig1Arnaud Clément2Emmanuelle Longueval3Thierry Bernardi4Catherine Ragimbeau5Odile Tresse6Epidemiology and Microbial Genomics, Laboratoire National de Santé, Dudelange, LuxembourgUMR-1280 PhAN, INRAE, Nantes, FranceBioFilm Control, Biopôle Clermont-Limagne, Saint-Beauzire, FranceEpidemiology and Microbial Genomics, Laboratoire National de Santé, Dudelange, LuxembourgBioFilm Control, Biopôle Clermont-Limagne, Saint-Beauzire, FranceEpidemiology and Microbial Genomics, Laboratoire National de Santé, Dudelange, LuxembourgUMR-1280 PhAN, INRAE, Nantes, FranceCampylobacter jejuni is a leading cause of foodborne illnesses worldwide. Although considered fragile, this microaerophilic bacterium is able to survive in various challenging environments, which subsequently constitutes multiple sources of transmission for human infection. To test the assumption of acquiring specific features for adaptation and survival, we established a workflow of phenotypic tests related to the survival and the persistence of recurrent and sporadic strains. A representative collection of 83 strains isolated over 13 years from human, mammal, poultry, and environmental sources in Luxembourg, representing different spreading patterns (endemic, epidemic, and sporadic), was screened for survival to oxidative stresses, for acclimating to aerobic conditions (AC), and for persistence on abiotic surfaces. Using the cgMLST Oxford typing scheme for WGS data, the collection was classified into genomic lineages corresponding to host-generalist strains (lineages A and D, CC ST-21), host-specific strains (lineage B, CC ST-257 and lineage C, CC ST-464) and sporadic strains. We established that when a strain survives concentrations beyond 0.25 mM superoxide stress, it is six times more likely to survive hyperoxide stress and that a highly adherent strain is 14 times more likely to develop a biofilm. Surprisingly, more than half of the strains could acclimate to AC but this capacity does not explain the difference between recurrent genomic lineages and sporadic strains and the survival to oxidative stresses, while recurrent strains have a significantly higher adhesion/biofilm formation capacity than sporadic ones. From this work, the genomic lineages with more stable genomes could be characterized by a specific combination of phenotypes, called metaphenotypes. From the functional genomic analyses, the presence of a potentially functional T6SS in the strains of lineage D might explain the propensity of these strains to be strong biofilm producers. Our findings support the hypothesis that phenotypical abilities contribute to the spatio-temporal adaptation and survival of stable genomic lineages. It suggests a selection of better-adapted and persistent strains in challenging stress environments, which could explain the prevalence of these lineages in human infections.https://www.frontiersin.org/articles/10.3389/fmicb.2022.901192/fullCampylobacter jejuniaerobic acclimationadhesion capacitybiofilm formationoxidative stressesrecurring lineages |
| spellingShingle | Morgane Nennig Morgane Nennig Arnaud Clément Emmanuelle Longueval Thierry Bernardi Catherine Ragimbeau Odile Tresse Metaphenotypes associated with recurrent genomic lineages of Campylobacter jejuni responsible for human infections in Luxembourg Frontiers in Microbiology Campylobacter jejuni aerobic acclimation adhesion capacity biofilm formation oxidative stresses recurring lineages |
| title | Metaphenotypes associated with recurrent genomic lineages of Campylobacter jejuni responsible for human infections in Luxembourg |
| title_full | Metaphenotypes associated with recurrent genomic lineages of Campylobacter jejuni responsible for human infections in Luxembourg |
| title_fullStr | Metaphenotypes associated with recurrent genomic lineages of Campylobacter jejuni responsible for human infections in Luxembourg |
| title_full_unstemmed | Metaphenotypes associated with recurrent genomic lineages of Campylobacter jejuni responsible for human infections in Luxembourg |
| title_short | Metaphenotypes associated with recurrent genomic lineages of Campylobacter jejuni responsible for human infections in Luxembourg |
| title_sort | metaphenotypes associated with recurrent genomic lineages of campylobacter jejuni responsible for human infections in luxembourg |
| topic | Campylobacter jejuni aerobic acclimation adhesion capacity biofilm formation oxidative stresses recurring lineages |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2022.901192/full |
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