Although many insects are associated with obligate bacterial endosymbionts, the mechanisms by which these host/endosymbiont associations are regulated remain mysterious. While micro
Like all organisms, aphids, plant sap-sucking insects that house a bacterial endosymbiont called
- NSF-PAR ID:
- 10153885
- Publisher / Repository:
- Nature Publishing Group
- Date Published:
- Journal Name:
- Scientific Reports
- Volume:
- 9
- Issue:
- 1
- ISSN:
- 2045-2322
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract RNA s (miRNA s) have been recently identified as regulators of host/microbe interactions, including host/pathogen and host/facultative endosymbiont interactions, the role miRNA s may play in mediating host/obligate endosymbiont interactions is virtually unknown. Here, we identified conserved miRNA s that potentially mediate symbiotic interactions between aphids and their obligate endosymbiont,Buchnera aphidicola . Using smallRNA sequence data fromMyzus persicae andAcyrthosiphon pisum , we annotated 93M. persicae and 89A. pisum miRNA s, among which 69 were shared. We found 14 miRNA s that were either highly expressed in aphid bacteriome, theBuchnera ‐housing tissue, or differentially expressed in bacteriome vs. gut, a non‐Buchnera ‐housing tissue. Strikingly, 10 of these 14 miRNA s have been implicated previously in other host/microbe interaction studies. Investigating the interaction networks of these miRNA s using a custom computational pipeline, we identified 103 miRNA ::mRNA interactions shared betweenM. persicae andA. pisum . Functional annotation of the sharedmRNA 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 miRNA s in mediating host/symbiont interactions between aphids and their obligate endosymbiontBuchnera . In addition, our results highlight the probable importance of signal transduction mechanisms to host/endosymbiont coevolution. -
Abstract Heritable symbionts are common in terrestrial arthropods and often provide beneficial services to hosts. Unlike obligate, nutritional symbionts that largely persist under strict host control within specialized host cells, heritable facultative symbionts exhibit large variation in within-host lifestyles and services rendered with many retaining the capacity to transition among roles. One enigmatic symbiont, Candidatus Fukatsuia symbiotica, frequently infects aphids with reported roles ranging from pathogen, defensive symbiont, mutualism exploiter and nutritional co-obligate symbiont. Here we used an in vitro culture-assisted protocol to sequence the genome of a facultative strain of Fukatsuia from pea aphids (Acyrthosiphon pisum). Phylogenetic and genomic comparisons indicate that Fukatsuia is an aerobic heterotroph, which together with Regiella insecticola and Hamiltonella defensa form a clade of heritable facultative symbionts within the Yersiniaceae (Enterobacteriales). These three heritable facultative symbionts largely share overlapping inventories of genes associated with housekeeping functions, metabolism, and nutrient acquisition, while varying in complements of mobile DNA. One unusual feature of Fukatsuia is its strong tendency to occur as a co-infection with H. defensa. However, the overall similarity of gene inventories among aphid heritable facultative symbionts suggest that metabolic complementarity is not the basis for co-infection, unless playing out on a H. defensa strain-specific basis. We also compared the pea aphid Fukatsuia with a strain from the aphid Cinara confinis (Lachninae) where it is reported to have transitioned to co-obligate status to support decaying Buchnera function. Overall the two genomes are very similar with no clear genomic signatures consistent with such a transition, which suggests co-obligate status in C. confinis was a recent event.more » « less
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Symbioses between animals and microbes are often described as mutualistic, but are subject to tradeoffs that may manifest as shifts in host and symbiont metabolism, cellular processes, or symbiont density. In pea aphids, the bacterial symbiont
Buchnera is confined to specialized aphid cells called bacteriocytes, where it produces essential amino acids needed by hosts. This relationship is dynamic;Buchnera titer varies within individual aphids and among different clonal aphid lineages, and is affected by environmental and host genetic factors. We examined how host genotypic variation relates to host and symbiont function among seven aphid clones differing inBuchnera titer. We found that bacteriocyte gene expression varies among individual aphids and among aphid clones, and thatBuchnera gene expression changes in response. By comparing hosts with low and highBuchnera titer, we found that aphids andBuchnera oppositely regulate genes underlying amino acid biosynthesis and cell growth. In high-titer hosts, both bacteriocytes and symbionts show elevated expression of genes underlying energy metabolism. Several eukaryotic cell signaling pathways are differentially expressed in bacteriocytes of low- versus high-titer hosts: Cell-growth pathways are up-regulated in low-titer genotypes, while membrane trafficking, lysosomal processes, and mechanistic target of rapamycin (mTOR) and cytokine pathways are up-regulated in high-titer genotypes. SpecificBuchnera functions are up-regulated within different bacteriocyte environments, with genes underlying flagellar body secretion and flagellar assembly overexpressed in low- and high-titer hosts, respectively. Overall, our results reveal allowances and demands made by both host and symbiont engaged in a metabolic “tug-of-war.” -
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Abstract Most insects harbour influential, yet non‐essential heritable microbes in their hemocoel. Communities of these symbionts exhibit low diversity. But their frequent multi‐species nature raises intriguing questions on roles for symbiont–symbiont synergies in host adaptation, and on the stability of the symbiont communities, themselves. In this study, we build on knowledge of species‐defined symbiont community structure across US populations of the pea aphid,
Acyrthosiphon pisum . Through extensive symbiont genotyping, we show that pea aphids' microbiomes can be more precisely defined at the symbiont strain level, with strain variability shaping five out of nine previously reported co‐infection trends. Field data provide a mixture of evidence for synergistic fitness effects and symbiont hitchhiking, revealing causes and consequences of these co‐infection trends. To test whether within‐host metabolic interactions predict common versus rare strain‐defined communities, we leveraged the high relatedness of our dominant, community‐defined symbiont strains vs. 12 pea aphid‐derived Gammaproteobacteria with sequenced genomes. Genomic inference, using metabolic complementarity indices, revealed high potential for cooperation among one pair of symbionts—Serratia symbiotica andRickettsiella viridis . Applying the expansion network algorithm, through additional use of pea aphid and obligateBuchnera symbiont genomes,Serratia andRickettsiella emerged as the only symbiont community requiring both parties to expand holobiont metabolism. Through their joint expansion of the biotin biosynthesis pathway, these symbionts may span missing gaps, creating a multi‐party mutualism within their nutrient‐limited, phloem‐feeding hosts. Recent, complementary gene inactivation, within the biotin pathways ofSerratia andRickettsiella , raises further questions on the origins of mutualisms and host–symbiont interdependencies. -
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Abstract Background Insects are an important reservoir of viral biodiversity, but the vast majority of viruses associated with insects have not been discovered. Recent studies have employed high-throughput RNA sequencing, which has led to rapid advances in our understanding of insect viral diversity. However, insect genomes frequently contain transcribed endogenous viral elements (EVEs) with significant homology to exogenous viruses, complicating the use of RNAseq for viral discovery.
Methods In this study, we used a multi-pronged sequencing approach to study the virome of an important agricultural pest and prolific vector of plant pathogens, the potato aphid
Macrosiphum euphorbiae . We first used rRNA-depleted RNAseq to characterize the microbes found in individual insects. We then used PCR screening to measure the frequency of two heritable viruses in a local aphid population. Lastly, we generated a quality draft genome assembly forM. euphorbiae using Illumina-corrected Nanopore sequencing to identify transcriptionally active EVEs in the host genome.Results We found reads from two insect-specific viruses (a
Flavivirus and anAmbidensovirus ) in our RNAseq data, as well as a parasitoid virus (Bracovirus ), a plant pathogenic virus (Tombusvirus ), and two phages (Acinetobacter and APSE). However, our genome assembly showed that part of the ‘virome’ of this insect can be attributed to EVEs in the host genome.Conclusion Our work shows that EVEs have led to the misidentification of aphid viruses from RNAseq data, and we argue that this is a widespread challenge for the study of viral diversity in insects.
