Large proportion of genes in one cryptic WO prophage genome are actively and sex-specifically transcribed in a fig wasp species

Guan-Hong Wang,Da-Wei Huang,Li-Ming Niu,Jin-Hua Xiao,Guang-Chang Ma

doi:10.1186/1471-2164-15-893

Abstract

BackgroundCryptic prophages are genetically defective in their induction and propagation, and are simply regarded as genetic remnants. There are several putative cryptic WO prophages in the sequenced Wolbachia genomes. Whether they are lytic is unclear and their functions are poorly understood. Only three open reading frames (ORFs) in cryptic WO prophages have been reported to be actively transcribed.ResultsIn this study, we comprehensively examined the transcription of the only cryptic WO prophage (WOSol) in a Wolbachia strain that infects a fig wasp, Ceratosolen solmsi (Agaonidae, Chalcidoidea). By analyzing the transcriptions of all the ORFs of WOSol in both sexes of C. solmsi, using qualitative and quantitative methods, we demonstrated that i) a high percentage of ORFs are actively transcribed (59%, 17/29); ii) the expression of these ORFs is highly sex-specific, with a strong male bias (three in females and 15 in males); iii) an ank (ankyrin-domain-containing) gene actively transcribed in both wasp sexes is more highly expressed in males.ConclusionsA large proportion of the genes in the cryptic WO prophage WOSol are expressed, which overturns the concept that cryptic prophages are simply genetically defective. The highly sex-specific expression patterns of these genes in the host suggest that they play important roles in Wolbachia biology and its reproductive manipulation of its insect host, particularly through the males.Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-15-893) contains supplementary material, which is available to authorized users.

Highlights

Cryptic prophages are genetically defective in their induction and propagation, and are regarded as genetic remnants
One cryptic prophage occurred in C. solmsi In our previous study [31], we have demonstrated that the fig wasp species C. solmsi is infected by a single Wolbachia strain that contains only one defective prophage WOSol, which lacks a tail module
Using real-time quantitative PCR, we counted and compared the densities of the Wolbachia genomes, and the phage WOSol genomes to determine whether WOSol was replicated extrachromosomally

Summary

Introduction

Cryptic prophages are genetically defective in their induction and propagation, and are regarded as genetic remnants. Lytic phages are strict pathogens of their bacterial hosts, and their infections culminate in the production of large numbers of new viral particles and lysis of the host cells Temperate phages, such as the WO phages in Wolbachia, have two different forms. A cytoplasmically inherited Rickettsiales, causes a number of reproductive anomalies in its arthropod hosts, including cytoplasmic incompatibility (CI) [9], parthenogenesis [10], feminization of genetic males [11], and male killing [12] These reproductive phenotypes impart a selective advantage on Wolbachia [13,14], facilitating the spread of Wolbachia infections in the host population. Some Wolbachia strains without WO can still manipulate the reproduction of their hosts, indicating the dispensability of WO in the function of Wolbachia [15,17]

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