microRNA regulation in an ancient obligate endosymbiosis

Abstract

Although many insects are associated with obligate bacterial endosymbionts, the mechanisms by which these host/endosymbiont associations are regulated remain mysterious. While microRNAs (miRNAs) have been recently identified as regulators of host/microbe interactions, including host/pathogen and host/facultative endosymbiont interactions, the role miRNAs may play in mediating host/obligate endosymbiont interactions is virtually unknown. Here, we identified conserved miRNAs that potentially mediate symbiotic interactions between aphids and their obligate endosymbiont, Buchnera aphidicola. Using small RNA sequence data from Myzus persicae and Acyrthosiphon pisum, we annotated 93 M. persicae and 89 A. pisum miRNAs, among which 69 were shared. We found 14 miRNAs that were either highly expressed in aphid bacteriome, the Buchnera-housing tissue, or differentially expressed in bacteriome vs. gut, a non-Buchnera-housing tissue. Strikingly, 10 of these 14 miRNAs have been implicated previously in other host/microbe interaction studies. Investigating the interaction networks of these miRNAs using a custom computational pipeline, we identified 103 miRNA::mRNA interactions shared between M. persicae and A. pisum. Functional annotation of the shared mRNA targets revealed only two over-represented cluster of orthologous group categories: amino acid transport and metabolism, and signal transduction mechanisms. Our work supports a role for miRNAs in mediating host/symbiont interactions between aphids and their obligate endosymbiont Buchnera. In addition, our results highlight the probable importance of signal transduction mechanisms to host/endosymbiont coevolution.

mTOR Complex 1 Implicated in Aphid/Buchnera Host/Symbiont Integration

“…In addition, A. pisum has two Rag A/B, and Skp2 orthologs, and M. persicae two Nup44A orthologs. All of these duplicated genes with the exception of the two RHEB orthologs unique to A. pisum are detected in wingless parthenogenetic female aphid transcriptomes (Feng et al 2018; NCBI BioProject PRJNA315109). The two RHEB orthologs unique to A. pisum were not detected in the transcriptomes associated with this study but are found in an alate male aphid transcriptome (data from Jaquiéry et al , 2018.…”

“…This evidence for a host-catalyzed final step of branched chain amino acid biosynthesis supports intimate coordination between the aphid and Buchnera in completion of amino acid biosynthesis pathways (Hansen and Moran 2011), but also opens the metabolic pathway to host control. Recent work identifying microRNA (miRNA) targets in aphid bacteriocytes suggests that expression of BCAT is miRNA regulated, thereby implicating host regulatory checks in the production of the branched-chain amino acids (Feng et al 2018). With respect to symbiont control, it is of interest that the genes for leucine biosynthesis are located on a plasmid within Buchnera from M. persicae and A. pisum , a genomic location that potentially uncouples leucine production rates from Buchnera genome copy number, a feature of symbiont genome evolution that possibly reveals some level of endosymbiont control of leucine production (Baumann et al 1999; Jiang et al 2013; Shigenobu et al 2000).…”

“…persicae genotypes based on M. persicae G006 v1.0 official gene set from aphidbase (bipaa.genouest.org/is/aphidbase). We used RNAseq generated in Feng et al 2018 and Jaquiéry et al 2018 to produce reference transcriptomes for A . pisum based on the 2.1b official gene set on aphidbase.…”

“…In particular, life-stage dependent differential expression of amino acid biosynthesis pathways within Buchnera has been hypothesized to result from post-transcriptional small RNA regulation within Buchnera (Hansen and Degnan 2014). Third, microRNAs (miRNAs) encoded in aphid genomes have been found to show bacteriocyte-specific expression (Feng et al 2018). Remarkably, of the 14 miRNAs highly or differentially expressed within aphid bacteriocytes, ten have previously been characterized to play roles in host/microbe interactions (Feng et al 2018).…”

“…Third, microRNAs (miRNAs) encoded in aphid genomes have been found to show bacteriocyte-specific expression (Feng et al 2018). Remarkably, of the 14 miRNAs highly or differentially expressed within aphid bacteriocytes, ten have previously been characterized to play roles in host/microbe interactions (Feng et al 2018). The emerging picture of host/endosymbiont regulation is one of multiple concurrent and overlapping mechanisms of integration.…”