Abstract

Heterorhabditis bacteriophora are entomopathogenic nematodes that have evolved a mutualism with Photorhabdus luminescens bacteria to function as highly virulent insect pathogens. The nematode provides a safe harbor for intestinal symbionts in soil and delivers the symbiotic bacteria into the insect blood. The symbiont provides virulence and toxins, metabolites essential for nematode reproduction, and antibiotic preservation of the insect cadaver. Approximately half of the 21,250 putative protein coding genes identified in the 77 Mbp high quality draft H. bacteriophora genome sequence were novel proteins of unknown function lacking homologs in Caenorhabditis elegans or any other sequenced organisms. Similarly, 317 of the 603 predicted secreted proteins are novel with unknown function in addition to 19 putative peptidases, 9 peptidase inhibitors and 7 C-type lectins that may function in interactions with insect hosts or bacterial symbionts. The 134 proteins contained mariner transposase domains, of which there are none in C. elegans, suggesting an invasion and expansion of mariner transposons in H. bacteriophora. Fewer Kyoto Encyclopedia of Genes and Genomes Orthologies in almost all metabolic categories were detected in the genome compared with 9 other sequenced nematode genomes, which may reflect dependence on the symbiont or insect host for these functions. The H. bacteriophora genome sequence will greatly facilitate genetics, genomics and evolutionary studies to gain fundamental knowledge of nematode parasitism and mutualism. It also elevates the utility of H. bacteriophora as a bridge species between vertebrate parasitic nematodes and the C. elegans model.

Highlights

  • Nematodes are the most abundant multicellular animals on the planet [1], and exhibit remarkably diverse lifestyles to impact all life [2]

  • H. bacteriophora is an entomopathogenic nematode, which is mutually associated with symbiotic bacteria to function as an insect parasite

  • H. bacteriophora is well-known of symbiosis compared to the C. elegans and represent a simple and tractable model of animal-bacteria gut symbiosis

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Summary

Introduction

Nematodes are the most abundant multicellular animals on the planet [1], and exhibit remarkably diverse lifestyles to impact all life [2]. A specialized stage of the nematode, analogous to the C. elegans dauer, called the infective juvenile (IJ) harbors the mutualistic bacteria in its intestine while in search of an insect host [9]. The bacteria produce exoenzymes to degrade the insect tissues and produce unknown metabolites essential for nematode reproduction. Unlike C. elegans and other bacteria-feeding nematodes, H. bacteriophora reproduces only when associated with specific Photorhabdus bacteria both in insects and nutrient rich media [17,18]. The bacteria produce potent secondary metabolites that are antibiotics [20] and which deter scavenging arthropods [21], enabling the nematode proliferation to nearly 500,000 IJs from a single infected insect, which disperse in search of new insect hosts [19,22]

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