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

Wang GH, Niu LM, Ma GC, Xiao JH, Huang DW - BMC Genomics (2014)

Bottom Line: In 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).A 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.

View Article: PubMed Central - PubMed

Affiliation: Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China. xiaojh@ioz.ac.cn.

ABSTRACT

Background: Cryptic 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.

Results: In 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.

Conclusions: A 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.

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Related in: MedlinePlus

The correlation between the abundance of prophage WOSol and that ofWolbachia wSol in females (A) and males (B) ofC. solmsi. Each circle on the charts denotes the absolute copy number of a single-copy gene (orf7) of prophage WOSol (according to the vertical axis) and a single-copy gene (groEL) of Wolbachia wSol (according to the horizontal axis) in an adult female or male C. solmsi individual infected with Wolbachia. Altogether, 31 female and 35 male wasps were investigated. Correlation coefficients (rho values) and significances (P values) were calculated according to the nonparametric method of Spearman’s rho.
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Fig1: The correlation between the abundance of prophage WOSol and that ofWolbachia wSol in females (A) and males (B) ofC. solmsi. Each circle on the charts denotes the absolute copy number of a single-copy gene (orf7) of prophage WOSol (according to the vertical axis) and a single-copy gene (groEL) of Wolbachia wSol (according to the horizontal axis) in an adult female or male C. solmsi individual infected with Wolbachia. Altogether, 31 female and 35 male wasps were investigated. Correlation coefficients (rho values) and significances (P values) were calculated according to the nonparametric method of Spearman’s rho.

Mentions: The total bacteriophage WOSol abundance correlated strongly with the total bacterial abundance in both females (rho = 0.8756, P <0.0001; Figure 1A) and males (rho = 0.8064, P <0.0001; Figure 1B), as expected for a cryptic prophage with which a lysogenic phage is co-transmitted in the bacterial host.Figure 1


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

Wang GH, Niu LM, Ma GC, Xiao JH, Huang DW - BMC Genomics (2014)

The correlation between the abundance of prophage WOSol and that ofWolbachia wSol in females (A) and males (B) ofC. solmsi. Each circle on the charts denotes the absolute copy number of a single-copy gene (orf7) of prophage WOSol (according to the vertical axis) and a single-copy gene (groEL) of Wolbachia wSol (according to the horizontal axis) in an adult female or male C. solmsi individual infected with Wolbachia. Altogether, 31 female and 35 male wasps were investigated. Correlation coefficients (rho values) and significances (P values) were calculated according to the nonparametric method of Spearman’s rho.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4201733&req=5

Fig1: The correlation between the abundance of prophage WOSol and that ofWolbachia wSol in females (A) and males (B) ofC. solmsi. Each circle on the charts denotes the absolute copy number of a single-copy gene (orf7) of prophage WOSol (according to the vertical axis) and a single-copy gene (groEL) of Wolbachia wSol (according to the horizontal axis) in an adult female or male C. solmsi individual infected with Wolbachia. Altogether, 31 female and 35 male wasps were investigated. Correlation coefficients (rho values) and significances (P values) were calculated according to the nonparametric method of Spearman’s rho.
Mentions: The total bacteriophage WOSol abundance correlated strongly with the total bacterial abundance in both females (rho = 0.8756, P <0.0001; Figure 1A) and males (rho = 0.8064, P <0.0001; Figure 1B), as expected for a cryptic prophage with which a lysogenic phage is co-transmitted in the bacterial host.Figure 1

Bottom Line: In 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).A 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.

View Article: PubMed Central - PubMed

Affiliation: Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China. xiaojh@ioz.ac.cn.

ABSTRACT

Background: Cryptic 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.

Results: In 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.

Conclusions: A 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.

Show MeSH
Related in: MedlinePlus