Protein tyrosine phosphatase-induced hyperactivity is a conserved strategy of a subset of baculoviruses to manipulate lepidopteran host behavior

PLoS One. 2012;7(10):e46933. doi: 10.1371/journal.pone.0046933. Epub 2012 Oct 15.

Abstract

Many parasites manipulate host behavior to increase the probability of transmission. To date, direct evidence for parasitic genes underlying such behavioral manipulations is scarce. Here we show that the baculovirus Autographa californica nuclear polyhedrovirus (AcMNPV) induces hyperactive behavior in Spodoptera exigua larvae at three days after infection. Furthermore, we identify the viral protein tyrosine phosphatase (ptp) gene as a key player in the induction of hyperactivity in larvae, and show that mutating the catalytic site of the encoded phosphatase enzyme prevents this induced behavior. Phylogenetic inference points at a lepidopteran origin of the ptp gene and shows that this gene is well-conserved in a group of related baculoviruses. Our study suggests that ptp-induced behavioral manipulation is an evolutionarily conserved strategy of this group of baculoviruses to enhance virus transmission, and represents an example of the extended phenotype concept. Overall, these data provide a firm base for a deeper understanding of the mechanisms behind baculovirus-induced insect behavior.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Baculoviridae / enzymology
  • Baculoviridae / genetics
  • Baculoviridae / physiology*
  • Cell Line
  • Enzyme Activation
  • Gene Deletion
  • Genes, Viral
  • Host-Parasite Interactions*
  • Lepidoptera / physiology
  • Lepidoptera / virology*
  • Mutation
  • Phylogeny
  • Protein Tyrosine Phosphatases / genetics*
  • Protein Tyrosine Phosphatases / metabolism
  • Viral Proteins / genetics*
  • Viral Proteins / metabolism

Substances

  • Viral Proteins
  • Protein Tyrosine Phosphatases

Grants and funding

SVH and VIDR were both supported by the Program Strategic Alliances of the Royal Dutch Academy of Sciences (project 08-PSA-BD-01). MVO was supported by a MEERVOUD grant from the Netherlands Organization for Scientific Research (project ALW2PJ/11051). KH was supported by a visiting scientist grant from the C.T. de Wit Graduate School for Production Ecology and Resource Conservation. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.