Analysis of gene expression from the Wolbachia genome of a filarial nematode supports both metabolic and defensive roles within the symbiosis.
The α-proteobacterium Wolbachia is probably the most prevalent, vertically transmitted symbiont on Earth. In contrast with its wide distribution in arthropods, Wolbachia is restricted to one family of animal-parasitic nematodes, the Onchocercidae. This includes filarial pathogens such as Onchocerca volvulus, the cause of human onchocerciasis, or river blindness. The symbiosis between filariae and Wolbachia is obligate, although the basis of this dependency is not fully understood. Previous studies suggested that Wolbachia may provision metabolites (e.g., haem, riboflavin, and nucleotides) and/or contribute to immune defense. Importantly, Wolbachia is restricted to somatic tissues in adult male worms, whereas females also harbor bacteria in the germline. We sought to characterize the nature of the symbiosis between Wolbachia and O. ochengi, a bovine parasite representing the closest relative of O. volvulus. First, we sequenced the complete genome of Wolbachia strain wOo, which revealed an inability to synthesize riboflavin de novo. Using RNA-seq, we also generated endobacterial transcriptomes from male soma and female germline. In the soma, transcripts for membrane transport and respiration were up-regulated, while the gonad exhibited enrichment for DNA replication and translation. The most abundant Wolbachia proteins, as determined by geLC-MS, included ligands for mammalian Toll-like receptors. Enzymes involved in nucleotide synthesis were dominant among metabolism-related proteins, whereas the haem biosynthetic pathway was poorly represented. We conclude that Wolbachia may have a mitochondrion-like function in the soma, generating ATP for its host. Moreover, the abundance of immunogenic proteins in wOo suggests a role in diverting the immune system toward an ineffective antibacterial response.
Institute of Integrative Biology and the Centre for Genomic Research, Biosciences Building, University of Liverpool, Liverpool, Merseyside L69 7ZB, United Kingdom.
Alistair C
AC
Darby
Stuart D
SD
Armstrong
Germanus S
GS
Bah
Gaganjot
G
Kaur
Margaret A
MA
Hughes
Suzanne M
SM
Kay
Pia
P
Koldkjær
Lucille
L
Rainbow
Alan D
AD
Radford
Mark L
ML
Blaxter
Vincent N
VN
Tanya
Alexander J
AJ
Trees
Richard
R
Cordaux
Jonathan M
JM
Wastling
Benjamin L
BL
Makepeace
D000818:Animals; D000900:Anti-Bacterial Agents / Q000378:metabolism; D002853:Chromatography, Liquid; D004261:DNA Replication; D018509:DNA, Helminth / Q000235:genetics; D005260:Female; D015964:Gene Expression Regulation, Bacterial; D016680:Genome, Bacterial; D008297:Male; D017181:Onchocerca volvulus / Q000382:microbiology*; D040901:Proteomics / Q000379:methods; D012256:Riboflavin / Q000378:metabolism; D017423:Sequence Analysis, RNA; D013559:Symbiosis / Q000235:genetics*; D053719:Tandem Mass Spectrometry; D051193:Toll-Like Receptors / Q000235:genetics / Q000378:metabolism; D059467:Transcriptome; D015854:Up-Regulation; D020577:Wolbachia / Q000235:genetics* / Q000276:immunology
D000900:Anti-Bacterial Agents; D018509:DNA, Helminth; D051193:Toll-Like Receptors; D012256:Riboflavin