Does the host drive Wolbachia gene expression?

Wolbachia pipientis is an endosymbiont bacterium commonly found in association with arthropods and filarial nematodes. Several studies disclosed the main role of Wolbachia in host physiology. Reasonably, the maintenance of a strict symbiosis requires coordination between Wolbachia and host gene expressions. Experimental studies show Wolbachia gene expression varies during host development or after environmental stresses. Despite this, the mechanism behind the regulation of Wolbachia gene expression is still not clear, since their genomes have lost most promoters during genome reduction. The first published RNA-Seq study on Wolbachia showed the differential expression of a DNA methyltransferase, an enzyme able to methylate adenine or cytosine on specific patterns and often involved in the regulation of bacteria gene expression. In this work, we tested the hypothesis that DNA methylation can affect gene expression in Wolbachia. We experimentally characterised the Wolbachia DNA methyltransferase and re-analysed RNA-Seq data from six studies on four hosts. We surprisingly found that the Wolbachia DNA methyltransferase is the only so far described able to methylate both adenine and cytosine without highly specific patterns. We also found that the nucleotide content of the genes correlates with their expressions, with a pattern compatible to be a consequence of DNA methylation. Lastly, we found a conserved eukaryotic-like promoter upstream of the Wolbachia DNA methyltransferase gene. Overall, these results may suggest a cascade mechanism in which the host induces the Wolbachia DNA methyltransferase expression, which in turn affects the bacterium gene expression.