The transcriptome of Listeria monocytogenes during co-cultivation with cheese rind bacteria suggests adaptation by induction of ethanolamine and 1,2-propanediol catabolism pathway genes

PLoS One. 2020 Jul 23;15(7):e0233945. doi: 10.1371/journal.pone.0233945. eCollection 2020.

Abstract

The survival of Listeria (L.) monocytogenes in foods and food production environments (FPE) is dependent on several genes that increase tolerance to stressors; this includes competing with intrinsic bacteria. We aimed to uncover genes that are differentially expressed (DE) in L. monocytogenes sequence type (ST) 121 strain 6179 when co-cultured with cheese rind bacteria. L. monocytogenes was cultivated in broth or on plates with either a Psychrobacter or Brevibacterium isolate from cheese rinds. RNA was extracted from co-cultures in broth after two or 12 hours and from plates after 24 and 72 hours. Broth co-cultivations with Brevibacterium or Psychrobacter yielded up to 392 and 601 DE genes, while plate co-cultivations significantly affected the expression of up to 190 and 485 L. monocytogenes genes, respectively. Notably, the transcription of virulence genes encoding the Listeria adhesion protein and Listeriolysin O were induced during plate and broth co-cultivations. The expression of several systems under the control of the global stress gene regulator, σB, increased during co-cultivation. A cobalamin-dependent gene cluster, responsible for the catabolism of ethanolamine and 1,2-propanediol, was upregulated in both broth and plate co-cultures conditions. Finally, a small non-coding (nc)RNA, Rli47, was induced after 72 hours of co-cultivation on plates and accounted for 50-90% of the total reads mapped to L. monocytogenes. A recent study has shown that Rli47 may contribute to L. monocytogenes stress survival by slowing growth during stress conditions through the suppression of branch-chained amino acid biosynthesis. We hypothesize that Rli47 may have an impactful role in the response of L. monocytogenes to co-cultivation by regulating a complex network of metabolic and virulence mechanisms.

Publication types

  • Comparative Study
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Acclimatization
  • Agar
  • Bacterial Proteins / biosynthesis
  • Bacterial Proteins / genetics
  • Brevibacterium / metabolism*
  • Cheese / microbiology*
  • Coculture Techniques
  • Culture Media
  • Electron Transport / genetics
  • Ethanolamine / metabolism*
  • Fermentation / genetics
  • Food Microbiology*
  • Gene Expression Regulation, Bacterial*
  • Listeria monocytogenes / genetics*
  • Listeria monocytogenes / metabolism
  • Listeria monocytogenes / pathogenicity
  • Plasmids
  • Propylene Glycol / metabolism*
  • Psychrobacter / metabolism*
  • RNA, Bacterial / biosynthesis
  • RNA, Bacterial / genetics
  • RNA, Messenger / biosynthesis
  • RNA, Messenger / genetics
  • RNA, Small Untranslated / biosynthesis
  • RNA, Small Untranslated / genetics
  • Transcriptome*
  • Virulence / genetics

Substances

  • Bacterial Proteins
  • Culture Media
  • RNA, Bacterial
  • RNA, Messenger
  • RNA, Small Untranslated
  • Ethanolamine
  • Propylene Glycol
  • Agar

Grants and funding

SSE and JMA are supported by the USDA National Institute of Food and Agriculture Hatch projects no. 1011114 and 1018898 and by the USDA National Institute of Food and Agriculture, Agricultural and Food Research Initiative Competitive Program, grant number: 2019-67017-29687.