Nutritional Interactions between Bacterial Species Colonising the Human Nasal Cavity: Current Knowledge and Future Prospects

Adolf, Lea Antje; Heilbronner, Simon

doi:10.3390/metabo12060489

Cited by 9 publications

(4 citation statements)

References 124 publications

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“…It is possible the increase of C. propinquum when grown together with S. aureus at higher temperatures is due to changes in available nutrients in the airway surface liquid due to metabolites produced either by S. aureus or from epithelial cells, which could result either from altered secretion due to the presence of staphylococcal proteins or increased S. aureus -induced cytotoxicity. Of note, previous studies have found metabolic interactions between URT microbionts, and many of these interspecies interactions have been documented showing synergism, which may explain the interactions seen for C. propinquum in the presence of S. aureus ( 60 , 61 ). The differences observed for S. aureus interactions with C. propinquum compared to C. pseudodiphtheriticum underscore that we know relatively little about species of commensal Corynebacterium , and further studies are warranted to uncover diverse mechanisms by which members of this genera interact with microbial constituents in the URT.…”

Section: Discussionmentioning

confidence: 82%

Temperature influences commensal-pathogen dynamics in a nasal epithelial cell co-culture model

Huffines,

Boone,

Kiedrowski

2024

mSphere

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Chronic rhinosinusitis (CRS) is an inflammatory disease of the paranasal sinuses, and microbial dysbiosis associated with CRS is thought to be a key driver of host inflammation that contributes to disease progression. Staphylococcus aureus is a common upper respiratory tract (URT) pathobiont associated with higher carriage rates in CRS populations, where S. aureus -secreted toxins can be identified in CRS tissues. Although many genera of bacteria colonize the URT, few account for the majority of sequencing reads. These include S. aureus and several species belonging to the genus Corynebacterium , including Corynebacterium propinquum and Corynebacterium pseudodiphtheriticum , which are observed at high relative abundance in the healthy URT. Studies have examined bacterial interactions between major microbionts of the URT and S. aureus , but few have done so in the context of a healthy versus diseased URT environment. Here, we examine the role of temperature in commensal, pathogen, and epithelial dynamics using an air-liquid interface cell culture model mimicking the nasal epithelial environment. Healthy URT temperatures change from the nares to the nasopharynx and are increased during disease. Temperatures representative of the healthy URT increase persistence and aggregate formation of commensal C. propinquum and C. pseudodiphtheriticum , reduce S. aureus growth, and lower epithelial cytotoxicity compared to higher temperatures correlating with the diseased CRS sinus. Dual-species colonization revealed species-specific interactions between Corynebacterium species and S. aureus dependent on temperature. Our findings suggest URT mucosal temperature plays a significant role in mediating polymicrobial and host-bacterial interactions that may exacerbate microbial dysbiosis in chronic URT diseases. IMPORTANCE Chronic rhinosinusitis is a complex inflammatory disease with a significant healthcare burden. Although presence of S. aureus and microbial dysbiosis are considered mediators of inflammation in CRS, no studies have examined the influence of temperature on S. aureus interactions with the nasal epithelium and the dominant genus of the healthy URT, Corynebacterium . Interactions between Corynebacterium species and S. aureus have been documented in several studies, but none to date have examined how environmental changes in the URT may alter their interactions with the epithelium or each other. This study utilizes a polarized epithelial cell culture model at air-liquid interface to study the colonization and spatial dynamics of S. aureus and clinical isolates of Corynebacterium from people with CRS to characterize the role temperature has in single- and dual-species dynamics on the nasal epithelium.

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Section: Discussionmentioning

confidence: 82%

Temperature influences commensal-pathogen dynamics in a nasal epithelial cell co-culture model

Huffines,

Boone,

Kiedrowski

2024

mSphere

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Section: Discussionmentioning

confidence: 82%

Temperature Influences Commensal-Pathogen Dynamics in a Nasal Epithelial Cell Co-culture Model

Huffines,

Boone,

Kiedrowski

2023

Preprint

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Chronic rhinosinusitis (CRS) is an inflammatory disease of the paranasal sinuses, and microbial dysbiosis associated with CRS is thought to be a key driver of host inflammation that contributes to disease progression.Staphylococcus aureusis a common upper respiratory tract (URT) pathobiont that is associated with higher carriage rates in CRS populations, whereS. aureussecreted toxins can be identified in CRS tissue samples. Although many genera of bacteria colonize the URT, relatively few account for the majority of sequencing reads. These includeS. aureus, as well as several species belonging to the genusCorynebacterium, includingCorynebacterium propinquumandCorynebacterium pseudodiphtheriticum, which are observed at high relative abundance in the URT of healthy individuals. Studies have examined the bacterial interactions between the major microbionts of the URT andS. aureus, but few have done so in the context of a healthy versus diseased URT environment. Here, we examine the role of temperature in commensal, pathogen, and epithelial dynamics using an air-liquid interface cell culture model mimicking the nasal epithelial environment. The healthy URT temperature changes from the nares to the nasopharynx and is altered during disease. Temperatures representative of the healthy URT increase persistence and aggregate formation of commensalC. propinquum and C. pseudodiphtheriticum, reduceS. aureusgrowth, and lower epithelial cytotoxicity compared to higher temperatures correlating with the diseased CRS sinus. Dual-species colonization revealed species-specific interactions between commensalCorynebacteriumspecies andS. aureusdependent on temperature. Our findings suggest that URT mucosal temperature plays a significant role in mediating polymicrobial and host-bacterial interactions that may exacerbate microbial dysbiosis found in chronic URT disease.IMPORTANCEChronic rhinosinusitis is a complex inflammatory disease with a significant healthcare burden. Although presence ofS. aureusand microbial dysbiosis are considered mediators of inflammation in CRS, no studies have examined the influence of temperature onS. aureusinteractions with the nasal epithelium and the dominant genus of the healthy URT,Corynebacterium. Interactions betweenCorynebacterium speciesandS. aureushave been documented in several studies, but none to date have examined how environmental changes in the URT may alter their interactions with the epithelium or each other. This study utilizes a polarized epithelial cell culture model at air-liquid interface to study the colonization and spatial dynamics ofS. aureusand clinical isolates ofCorynebacteriumfrom people with CRS to characterize the role temperature has in single-and dual-species dynamics on the nasal epithelium.

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“…Lastly, all four species encoded a complete module for UDP-N-acetyl-D-glucosamine biosynthesis (M00909), a precursor of cell wall peptidoglycan (81). Of note, we found 61 hits across 28 D. pigrum genomes and no hits in the Corynebacterium genomes for a sialidase (K01186), which can release sialic acid from sialylated glycans found in mucus providing bacteria with carbon and nitrogen (82).…”

Section: S4a S4bmentioning

confidence: 92%

Metabolic capabilities are highly conserved among human nasal-associatedCorynebacteriumspecies in pangenomic analyses

Tran

Roberts

Escapa

et al. 2023

Preprint

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Corynebacteriumspecies are globally ubiquitous in human nasal microbiota across the lifespan. Moreover, nasal microbiota profiles typified by higher relative abundances ofCorynebacteriumare often positively associated with health. Among the most common human nasalCorynebacteriumspecies areC. propinquum,C. pseudodiphtheriticum,C. accolens, andC. tuberculostearicum. Based on the prevalence of these species, at least two likely coexist in the nasal microbiota of 82% of adults. To gain insight into the functions of these four species, we identified genomic, phylogenomic, and pangenomic properties and estimated the functional protein repertoire and metabolic capabilities of 87 distinct human nasalCorynebacteriumstrain genomes: 31 from Botswana and 56 from the U.S.C. pseudodiphtheriticumhad geographically distinct clades consistent with localized strain circulation, whereas some strains from the other species had wide geographic distribution across Africa and North America. All four species had similar genomic and pangenomic structures. Gene clusters assigned to all COG metabolic categories were overrepresented in the persistent (core) compared to the accessory genome of each species indicating limited strain-level variability in metabolic capacity. Moreover, core metabolic capabilities were highly conserved among the four species indicating limited species-level metabolic variation. Strikingly, strains in the U.S. clade ofC. pseudodiphtheriticumlacked genes for assimilatory sulfate reduction present in the Botswanan clade and in the other studied species, indicating a recent, geographically related loss of assimilatory sulfate reduction. Overall, the minimal species and strain variability in metabolic capacity implies coexisting strains might have limited ability to occupy distinct metabolic niches.

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Nutritional Interactions between Bacterial Species Colonising the Human Nasal Cavity: Current Knowledge and Future Prospects

Cited by 9 publications

References 124 publications

Temperature influences commensal-pathogen dynamics in a nasal epithelial cell co-culture model

Temperature influences commensal-pathogen dynamics in a nasal epithelial cell co-culture model

Temperature Influences Commensal-Pathogen Dynamics in a Nasal Epithelial Cell Co-culture Model

Metabolic capabilities are highly conserved among human nasal-associatedCorynebacteriumspecies in pangenomic analyses

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