Rickettsia parkeri infection modulates the sialome and ovariome of the Gulf coast tick, Amblyomma maculatum

Abstract

The Gulf Coast tick, <i>Amblyomma maculatum</i>, is a vector of several tick-borne pathogens, including <i>Rickettsia parkeri</i>. The ability of <i>R</i>. <i>parkeri</i> to persist within the tick population through transovarial and transstadial transmission, without apparently harming the ticks, contributes to the pathogen's perpetuation in the tick population. Previous studies have shown that the <i>R</i>. <i>parkeri</i> load in <i>A</i>. <i>maculatum</i> is regulated by the tick tissues' oxidant/antioxidant balance and the non-pathogenic tick microbiome. To obtain further insights into the interaction between tick and pathogen, we performed a bulk RNA-Seq for differential transcriptomic analysis of ovaries and salivary glands from <i>R</i>. <i>parkeri</i>-infected and uninfected ticks over the feeding course on a host. The most differentially expressed functional category was of bacterial origin, exhibiting a massive overexpression of bacterial transcripts in response to the <i>R</i>. <i>parkeri</i> infection. <i>Candidatus</i> Midichloria mitochondrii and bacteria from the genus Rickettsia were mainly responsible for the overexpression of bacterial transcripts. Host genes were also modulated in <i>R</i>. <i>parkeri</i>-infected tick organs. A similar number of host transcripts from all analyzed functional categories was negatively and positively modulated, revealing a global alteration of the <i>A</i>. <i>maculatum</i> transcriptome in response to pathogen infection. <i>R</i>. <i>parkeri</i> infection led to an increase in salivary transcripts involved in blood feeding success as well as a decrease in ovarian immune transcripts. We hypothesize that these transcriptional alterations facilitate pathogen persistence and transmission within tick population.