Dynamics of Wolbachia pipientis Gene Expression Across the Drosophila melanogaster Life Cycle.
Symbiotic interactions between microbes and their multicellular hosts have manifold biological consequences. To better understand how bacteria maintain symbiotic associations with animal hosts, we analyzed genome-wide gene expression for the endosymbiotic α-proteobacteria Wolbachia pipientis across the entire life cycle of Drosophila melanogaster. We found that the majority of Wolbachia genes are expressed stably across the D. melanogaster life cycle, but that 7.8% of Wolbachia genes exhibit robust stage- or sex-specific expression differences when studied in the whole-organism context. Differentially-expressed Wolbachia genes are typically up-regulated after Drosophila embryogenesis and include many bacterial membrane, secretion system, and ankyrin repeat-containing proteins. Sex-biased genes are often organized as small operons of uncharacterized genes and are mainly up-regulated in adult Drosophila males in an age-dependent manner. We also systematically investigated expression levels of previously-reported candidate genes thought to be involved in host-microbe interaction, including those in the WO-A and WO-B prophages and in the Octomom region, which has been implicated in regulating bacterial titer and pathogenicity. Our work provides comprehensive insight into the developmental dynamics of gene expression for a widespread endosymbiont in its natural host context, and shows that public gene expression data harbor rich resources to probe the functional basis of the Wolbachia-Drosophila symbiosis and annotate the transcriptional outputs of the Wolbachia genome.
Faculty of Life Sciences, University of Manchester, M13 9PT Manchester, United Kingdom.
Florence
F
Gutzwiller
Instituto Gulbenkian de Ciência, P-2780-156 Oeiras, Portugal.
Catarina R
http://orcid.org/0000-0001-9717-6667
CR
Carmo
Stowers Institute for Medical Research, Kansas City, Missouri 64110 Department of Molecular and Integrative Physiology, University of Kansas Medical Center, Kansas City, Kansas 66160.
Danny E
DE
Miller
Department of Biology, Indiana University, Bloomington, Indiana 47405.
Danny W
http://orcid.org/0000-0002-1123-4617
DW
Rice
Department of Biology, Indiana University, Bloomington, Indiana 47405.
Irene L G
IL
Newton
Stowers Institute for Medical Research, Kansas City, Missouri 64110 Department of Molecular and Integrative Physiology, University of Kansas Medical Center, Kansas City, Kansas 66160.
R Scott
RS
Hawley
Instituto Gulbenkian de Ciência, P-2780-156 Oeiras, Portugal.
Luis
http://orcid.org/0000-0001-8326-6645
L
Teixeira
Faculty of Life Sciences, University of Manchester, M13 9PT Manchester, United Kingdom casey.bergman@manchester.ac.uk.
Casey M
http://orcid.org/0000-0002-5462-9854
CM
Bergman
D000818:Animals; D016000:Cluster Analysis; D019295:Computational Biology; D004331:Drosophila melanogaster / Q000254:growth & development* / Q000382:microbiology; D020869:Gene Expression Profiling; D015964:Gene Expression Regulation, Bacterial; D016680:Genome, Bacterial; D059014:High-Throughput Nucleotide Sequencing; D054884:Host-Pathogen Interactions / Q000235:genetics; D008018:Life Cycle Stages; D010802:Phylogeny; D013312:Stress, Physiological / Q000235:genetics; D013559:Symbiosis; D059467:Transcriptome; D020577:Wolbachia / Q000235:genetics*
Drosophila; Wolbachia; cytoplasmic incompatibility; development; symbiosis