White feces syndrome of shrimp arises from transformation, sloughing and aggregation of hepatopancreatic microvilli into vermiform bodies superficially resembling gregarines

PLoS One. 2014 Jun 9;9(6):e99170. doi: 10.1371/journal.pone.0099170. eCollection 2014.

Abstract

Accompanying acute hepatopancreatic necrosis disease (AHPND) in cultivated Asian shrimp has been an increasing prevalence of vermiform, gregarine-like bodies within the shrimp hepatopancreas (HP) and midgut. In high quantity they result in white fecal strings and a phenomenon called white feces syndrome (WFS). Light microscopy (LM) of squash mounts and stained smears from fresh HP tissue revealed that the vermiform bodies are almost transparent with widths and diameters proportional to the HP tubule lumens in which they occur. Despite vermiform appearance, they show no cellular structure. At high magnification (LM with 40-100x objectives), they appear to consist of a thin, outer membrane enclosing a complex of thicker, inter-folded membranes. Transmission electron microscopy (TEM) revealed that the outer non-laminar membrane of the vermiform bodies bore no resemblance to a plasma membrane or to the outer layer of any known gregarine, other protozoan or metazoan. Sub-cellular organelles such as mitochondria, nuclei, endoplasmic reticulum and ribosomes were absent. The internal membranes had a tubular sub-structure and occasionally enclosed whole B-cells, sloughed from the HP tubule epithelium. These internal membranes were shown to arise from transformed microvilli that peeled away from HP tubule epithelial cells and then aggregated in the tubule lumen. Stripped of microvilli, the originating cells underwent lysis. By contrast, B-cells remained intact or were sloughed independently and whole from the tubule epithelium. When sometimes engulfed by the aggregated, transformed microvilli (ATM) they could be misinterpreted as cyst-like structures by light microscopy, contributing to gregarine-like appearance. The cause of ATM is currently unknown, but formation by loss of microvilli and subsequent cell lysis indicate that their formation is a pathological process. If sufficiently severe, they may retard shrimp growth and may predispose shrimp to opportunistic pathogens. Thus, the cause of ATM and their relationship (if any) to AHPND should be determined.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apicomplexa / physiology*
  • Digestive System / parasitology
  • Digestive System / pathology*
  • Digestive System / ultrastructure
  • Epithelial Cells / parasitology
  • Epithelial Cells / pathology
  • Epithelial Cells / ultrastructure
  • Feces / parasitology*
  • Hepatopancreas / parasitology
  • Hepatopancreas / pathology*
  • Hepatopancreas / ultrastructure
  • Microscopy, Electron
  • Microscopy, Electron, Transmission
  • Microvilli / parasitology
  • Microvilli / pathology*
  • Penaeidae / parasitology*
  • Protozoan Infections / parasitology
  • Syndrome

Grants and funding

Partial funding for this work was obtained from the Surathani Shrimp Farmers Club, the Frozen Food Association of Thailand, Charoen Pokphand Company Ltd., the Thai Commission for Higher Education, the National Research Council of Thailand and Mahidol University. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.