Corynebacterium accolens Releases Antipneumococcal Free Fatty Acids from Human Nostril and Skin Surface Triacylglycerols

Author:

Bomar Lindsey12,Brugger Silvio D.12,Yost Brian H.1,Davies Sean S.3,Lemon Katherine P.14

Affiliation:

1. Department of Microbiology, The Forsyth Institute, Cambridge, Massachusetts, USA

2. Department of Oral Medicine, Infection and Immunity, Harvard School of Dental Medicine, Boston, Massachusetts, USA

3. Department of Pharmacology, Division of Clinical Pharmacology, Vanderbilt University, Nashville, Tennessee, USA

4. Division of Infectious Diseases, Boston Children’s Hospital, Harvard Medical School, Boston, Massachusetts, USA

Abstract

ABSTRACT Bacterial interspecies interactions play clinically important roles in shaping microbial community composition. We observed that Corynebacterium spp. are overrepresented in children free of Streptococcus pneumoniae (pneumococcus), a common pediatric nasal colonizer and an important infectious agent. Corynebacterium accolens , a benign lipid-requiring species, inhibits pneumococcal growth during in vitro cocultivation on medium supplemented with human skin surface triacylglycerols (TAGs) that are likely present in the nostrils. This inhibition depends on LipS1, a TAG lipase necessary for C. accolens growth on TAGs such as triolein. We determined that C. accolens hydrolysis of triolein releases oleic acid, which inhibits pneumococcus, as do other free fatty acids (FFAs) that might be released by LipS1 from human skin surface TAGs. Our results support a model in which C. accolens hydrolyzes skin surface TAGS in vivo releasing antipneumococcal FFAs. These data indicate that C. accolens may play a beneficial role in sculpting the human microbiome. IMPORTANCE Little is known about how harmless Corynebacterium species that colonize the human nose and skin might impact pathogen colonization and proliferation at these sites . We show that Corynebacterium accolens , a common benign nasal bacterium, modifies its local habitat in vitro as it inhibits growth of Streptococcus pneumoniae by releasing antibacterial free fatty acids from host skin surface triacylglycerols. We further identify the primary C. accolens lipase required for this activity. We postulate a model in which higher numbers of C. accolens cells deter/limit S. pneumoniae nostril colonization, which might partly explain why children without S. pneumoniae colonization have higher levels of nasal Corynebacterium . This work narrows the gap between descriptive studies and the needed in-depth understanding of the molecular mechanisms of microbe-microbe interactions that help shape the human microbiome. It also lays the foundation for future in vivo studies to determine whether habitat modification by C. accolens could be promoted to control pathogen colonization.

Funder

Swiss Society for Microbiology Encouragement Award

The Swiss National Science Foundation and Swiss Foundation for Grants in Biology and Medicine

Boston Children's Hospital Career Development Grant

HHS | NIH | National Institute of Allergy and Infectious Diseases

HHS | NIH | National Institute of Dental and Craniofacial Research

HHS | NIH | National Center for Complementary and Integrative Health

Publisher

American Society for Microbiology

Subject

Virology,Microbiology

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