16S rRNA gene profiling and genome reconstruction reveal community metabolic interactions and prebiotic potential of medicinal herbs used in neurodegenerative disease and as nootropics

PLoS One. 2019 Mar 19;14(3):e0213869. doi: 10.1371/journal.pone.0213869. eCollection 2019.

Abstract

The prebiotic potential of nervine herbal medicines has been scarcely studied. We therefore used anaerobic human fecal cultivation to investigate whether medicinal herbs commonly used as treatment in neurological health and disease in Ayurveda and other traditional systems of medicine modulate gut microbiota. Profiling of fecal cultures supplemented with either Kapikacchu, Gotu Kola, Bacopa/Brahmi, Shankhapushpi, Boswellia/Frankincense, Jatamansi, Bhringaraj, Guduchi, Ashwagandha or Shatavari by 16S rRNA sequencing revealed profound changes in diverse taxa. Principal coordinate analysis highlights that each herb drives the formation of unique microbial communities predicted to display unique metabolic potential. The relative abundance of approximately one-third of the 243 enumerated species was altered by all herbs. Additional species were impacted in an herb-specific manner. In this study, we combine genome reconstruction of sugar utilization and short chain fatty acid (SCFA) pathways encoded in the genomes of 216 profiled taxa with monosaccharide composition analysis of each medicinal herb by quantitative mass spectrometry to enhance the interpretation of resulting microbial communities and discern potential drivers of microbiota restructuring. Collectively, our results indicate that gut microbiota engage in both protein and glycan catabolism, providing amino acid and sugar substrates that are consumed by fermentative species. We identified taxa that are efficient amino acid fermenters and those capable of both amino acid and sugar fermentation. Herb-induced microbial communities are predicted to alter the relative abundance of taxa encoding SCFA (butyrate and propionate) pathways. Co-occurrence network analyses identified a large number of taxa pairs in medicinal herb cultures. Some of these pairs displayed related culture growth relationships in replicate cultures highlighting potential functional interactions among medicinal herb-induced taxa.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Amino Acids / metabolism
  • Bacteria / genetics*
  • Bacteria / metabolism
  • Diet, Vegetarian
  • Fatty Acids, Volatile / metabolism
  • Feces / microbiology
  • Female
  • Gastrointestinal Microbiome / drug effects*
  • Genome, Bacterial
  • Humans
  • Male
  • Middle Aged
  • Monosaccharides / analysis
  • Neurodegenerative Diseases / microbiology
  • Neurodegenerative Diseases / pathology
  • Nootropic Agents / chemistry
  • Nootropic Agents / pharmacology*
  • Plants, Medicinal / chemistry
  • Plants, Medicinal / metabolism*
  • Principal Component Analysis
  • RNA, Ribosomal, 16S / metabolism*

Substances

  • Amino Acids
  • Fatty Acids, Volatile
  • Monosaccharides
  • Nootropic Agents
  • RNA, Ribosomal, 16S

Grants and funding

This work was supported by a research grant from the Samuel Lawrence Foundation and a fellowship grant from the Chopra Foundation awarded to CP. DR and SI were supported by the Russian Science Foundation (grant #14-14-00289). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. The funders web sites are: http://rscf.ru/en/; https://www.samuellawrencefoundation.org/; https://www.choprafoundation.org/.