Metabolic capabilities are highly conserved among human nasal-associated
Corynebacterium
species in pangenomic analyses
Authors: Tran Tommy H. , F. Escapa Isabel , Roberts Ari Q. , Gao Wei , Obawemimo Abiola C. , Segre Julia A. , Kong Heidi H. , Conlan Sean , Kelly Matthew S. , Lemon Katherine P. 
Published: November 2024

ABSTRACT

Corynebact
e
rium
species are globally ubiquitous in human nasal microbiota across the lifespan. Moreover, nasal microbiota profiles typified by higher relative abundances of
Corynebacterium
are often positively associated with health. Among the most common human nasal
Corynebacterium
species are
C. propinquum
,
C. pseudodiphtheriticum, C. accolens
, and
C. tuberculostearicum
. To gain insight into the functions of these four species, we identified genomic, phylogenomic, and pangenomic properties and estimated the metabolic capabilities of 87 distinct human nasal
Corynebacterium
strain genomes: 31 from Botswana and 56 from the United States.
C. pseudodiphtheriticum
had geographically distinct clades consistent with localized strain circulation, whereas some strains from the other species had wide geographic distribution spanning Africa and North America. All species had similar genomic and pangenomic structures. Gene clusters assigned to all COG metabolic categories were overrepresented in the persistent versus accessory genome of each species indicating limited strain-level variability in metabolic capacity. Based on prevalence data, at least two
Corynebacterium
species likely coexist in the nasal microbiota of 82% of adults. So, it was surprising that core metabolic capabilities were highly conserved among the four species indicating limited species-level metabolic variation. Strikingly, strains in the U.S. clade of
C. pseudodiphtheriticum
lacked genes for assimilatory sulfate reduction present in most of the strains in the Botswana 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.

IMPORTANCE

Pangenomic analysis with estimation of functional capabilities facilitates our understanding of the full biologic diversity of bacterial species. We performed systematic genomic, phylogenomic, and pangenomic analyses with qualitative estimation of the metabolic capabilities of four common human nasal
Corynebacterium
species, along with focused experimental validations, generating a foundational resource. The prevalence of each species in human nasal microbiota is consistent with the common coexistence of at least two species. We identified a notably high level of metabolic conservation within and among species indicating limited options for species to occupy distinct metabolic niches, highlighting the importance of investigating interactions among nasal
Corynebacterium
species. Comparing strains from two continents,
C. pseudodiphtheriticum
had restricted geographic strain distribution characterized by an evolutionarily recent loss of assimilatory sulfate reduction in U.S. strains. Our findings contribute to understanding the functions of
Corynebacterium
within human nasal microbiota and to evaluating their potential for future use as biotherapeutics.