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

Jeonghwan Jang, Valery E. Forbes, Michael J. Sadowsky

Research output: Contribution to journalArticlepeer-review

Abstract

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 B12, 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 the worm'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.

Original languageEnglish (US)
Article number151127
JournalScience of the Total Environment
Volume809
DOIs
StatePublished - Feb 25 2022

Bibliographical note

Funding Information:
This work was partially supported by funds from the University of Minnesota and by research funds for newly appointed professors (for JJ) from Jeonbuk National University, Republic of Korea. We would like to thank Dr. Glenn Lopez for help in collecting marine sediment in the field and Drs. Elaine Seaver (University of Florida, USA) and Henriette Selck (Roskilde University, Denmark) for providing Capitella teleta cultured in their laboratories.

Funding Information:
This work was partially supported by funds from the University of Minnesota and by research funds for newly appointed professors (for JJ) from Jeonbuk National University, Republic of Korea .

Publisher Copyright:
© 2021 The Authors

Keywords

  • Cutibacterium acnes
  • Gut symbiont
  • Marine worm
  • Polychaete
  • Short chain fatty acids
  • Vitamin B

PubMed: MeSH publication types

  • Journal Article

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