The Steinernema carpocapsae intestinal vesicle contains a subcellular structure with which Xenorhabdus nematophila associates during colonization initiation

Cell Microbiol. 2005 Dec;7(12):1723-35. doi: 10.1111/j.1462-5822.2005.00585.x.

Abstract

Steinernema carpocapsae infective juvenile (IJ) nematodes are intestinally colonized by mutualistic Xenorhabdus nematophila bacteria. During IJ development, a small number of ingested X. nematophila cells initiate colonization in an anterior region of the intestine termed the vesicle and subsequently multiply within this host niche. We hypothesize that efficient colonization of a high percentage of S. carpocapsae individuals (typically>85%) is facilitated by bacterial adherence to a site(s) in the nematode intestine. We provide evidence that the adherence site is a structure in the lumen of the IJ vesicle that we have termed the intravesicular structure (IVS). The IVS is an untethered cluster of anucleate spherical bodies that co-localizes with colonizing X. nematophila cells, but does not require X. nematophila for its formation. Colocalization with the IVS is readily apparent in IJs colonized by X. nematophila mutants that initiate intestinal colonization but fail to proliferate normally, suggesting that bacterial-IVS interaction occurs early in the colonization process. Treatment with insect haemolymph induces anal release of X. nematophila from colonized IJs and induces release of the IVS from uncolonized S. carpocapsae IJs. Released IVS were probed with several carbohydrate-specific lectins. One lectin, wheat-germ agglutinin, reacts strongly with a mucus-like substance that is present around individual spheres in the aggregate IVS. Potential roles for the IVS in mediating X. nematophila colonization of the nematode intestine are discussed.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Bacterial Adhesion
  • Cytoplasmic Vesicles / metabolism
  • Cytoplasmic Vesicles / microbiology*
  • Cytoplasmic Vesicles / ultrastructure
  • Hemolymph / metabolism
  • Intestinal Mucosa / cytology
  • Intestinal Mucosa / metabolism
  • Intestinal Mucosa / microbiology*
  • Nematoda / cytology
  • Nematoda / microbiology*
  • Species Specificity
  • Wheat Germ Agglutinins / metabolism
  • Xenorhabdus / pathogenicity
  • Xenorhabdus / physiology*

Substances

  • Wheat Germ Agglutinins