4.7 Article

Probable role of Cutibacterium acnes in the gut of the polychaete Capitella teleta

Journal

SCIENCE OF THE TOTAL ENVIRONMENT
Volume 809, Issue -, Pages -

Publisher

ELSEVIER
DOI: 10.1016/j.scitotenv.2021.151127

Keywords

Marine worm; Polychaete; Cutibacterium acnes; Gut symbiont; Short chain fatty acids; Vitamin B-12

Funding

  1. University of Minnesota
  2. Jeonbuk National University, Republic of Korea

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This study discovered the presence of Cutibacterium acnes strains in the gut microbiota of the marine polychaete Capitella teleta. These strains produce propionate and vitamin B-12, which are essential microbial metabolites for the host. C. acnes, as a member of the worm's core functional microbiota, is likely favored by the host gut environment.
Capitella teleta, a marine polychaete that feeds on a refractory diet consisting of sediment, was shown to contain unique gut microbiota comprised of microbial functional groups involved in fermentation. Results of our previous studies showed that C. teleta's core gut microbiota were dominated by propionibacteria, and that these bacteria were more abundant in worms than in sediment and feces. In order to test the hypothesis that the worm nutritionally benefits from its gut microbiota, we identified, and genetically and biochemically characterized Cutibacterium acnes strains (formerly Propionibacterium acnes) that were isolated from the gut of C. teleta. Here we show that 13 worm-isolated Cutibacterium acnes strains primarily belonged to phylotype group IB, likely as a clonal population. We also provide evidence that all tested strains produced propionate and vitamin B-12, which are essential host-requiring microbial metabolites. The presence of C. acnes in C. teleta was not unique to our worm culture and was also found in those obtained from geographically distant laboratories located in the U.S. and Europe. Moreover, populations of worm gut-associated C. acnes increased following antibiotic treatment. Collectively, results of this study demonstrated that C. acnes is a member of theworm's core functional microbiota and is likely selectively favored by the physiology and chemistry of the host gut environment. To our knowledge, this is the first report of the presence of C. acnes in the C. teleta gut. Our data strongly suggest that C. acnes, a bacterium previously studied as an opportunistic pathogen, can likely act as a symbiont in C. teleta providing the host essential nutrients for survival, growth, and reproduction. (C) 2021 The Authors. Published by Elsevier B.V.

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