Exoelectrogenic capacity of host microbiota predicts lymphocyte recruitment to the gut

Physiol Genomics. 2015 Jul;47(7):243-52. doi: 10.1152/physiolgenomics.00010.2015. Epub 2015 Apr 7.

Abstract

Electrotaxis, directional cell movement in response to an electric potential, has been demonstrated in a wide range of cell types including lymphocytes. Exoelectrogens, microorganisms capable of generating electrical currents, have been identified in microbial fuel cells. However, no studies have investigated exoelectrogenic microbes in fresh feces or the effects of an exoelectrogenic microbiota on the host organism. Here we show that commensal gut microbial populations differ in their capacity for electrical current production by exoelectrogens and that those differences are predictive of increased lymphocyte trafficking to the gut in vivo, despite the lack of increased production of canonical lymphocyte-specific chemokines. Additionally, we demonstrate that the difference in current production between mice purchased from different commercial sources correlates reproducibly with the presence or absence of segmented filamentous bacteria, and while our data do not support a direct role for segmented filamentous bacteria in ex vivo current production, an exoelectrogenic microbiota can be transferred in vivo via mucosa-associated bacteria present in the ileum. Moreover, we detect upregulation of microbial genes associated with extracellular electron transfer in feces of mice colonized with exoelectrogenic microbiota containing segmented filamentous bacteria. While still correlative, these results suggest a novel means by which the gut microbiota modulates the recruitment of cells of the immune system to the gut.

Keywords: electrotaxis; exoelectrogen; microbiota; segmented filamentous bacteria.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Adoptive Transfer
  • Animals
  • Base Sequence
  • Cell Movement / physiology*
  • Computational Biology
  • Electrolysis
  • Electrophysiological Phenomena / physiology*
  • Enzyme-Linked Immunosorbent Assay
  • Feces / chemistry
  • Fluorometry
  • Gastric Mucosa / physiology*
  • Gastrointestinal Microbiome / physiology*
  • Gastrointestinal Tract / cytology
  • Gastrointestinal Tract / microbiology
  • Gastrointestinal Tract / physiology*
  • Gene Expression Regulation / physiology*
  • Gene Library
  • Immunohistochemistry
  • Lymphocytes / physiology*
  • Mice
  • Mice, Inbred C57BL
  • Microscopy, Confocal
  • Microscopy, Electron, Scanning
  • Microscopy, Electron, Transmission
  • Molecular Sequence Data
  • Proteobacteria / metabolism
  • Real-Time Polymerase Chain Reaction
  • Reverse Transcriptase Polymerase Chain Reaction
  • Sequence Analysis, DNA
  • Statistics, Nonparametric