The evolutionary development of plant‐feeding insects and their nutritional endosymbionts

Skidmore, Isabel H.; Hansen, Allison K.

doi:10.1111/1744-7917.12463

Cited by 45 publications

(41 citation statements)

References 93 publications

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“…Our experimental data provide tangential evidence for this hypothesis. It is also interesting to note that the majority of sRNAs (this study) and proteins (Hansen & Degnan, 2014) were upregulated in aphid embryos compared to maternal (Skidmore & Hansen, 2017).…”

Section: Discussionmentioning

confidence: 69%

“…It is also interesting to note that the majority of sRNAs (this study) and proteins (Hansen & Degnan, ) were upregulated in aphid embryos compared to maternal bacteriocytes. Potentially if some of these sRNA candidates are regulatory, the enrichment of Buchnera proteins may be more important in the embryonic stage of insect development where host control is not yet possible, because bacteriocytes have not fully formed yet around Buchnera cells (Skidmore & Hansen, ).…”

Section: Discussionmentioning

confidence: 99%

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A sRNA in a reduced mutualistic symbiont genome regulates its own gene expression

2017

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Similar to other nutritional endosymbionts that are obligate for host survival, the mutualistic aphid endosymbiont, Buchnera, has a highly reduced genome with few regulatory elements. Until recently, it was thought that aphid hosts were primarily responsible for regulating their symbiotic relationship. However, we recently revealed that Buchnera displays differential protein regulation, but not mRNA expression. We also identified a number of conserved small RNAs (sRNAs) that are expressed among Buchnera taxa. In this study, we investigate whether differential protein regulation in Buchnera is the result of post-transcriptional gene regulation via sRNAs. We characterize the sRNA profile of two Buchnera life stages: (i) when Buchnera is transitioning from an extracellular proliferating state in aphid embryos and (ii) when Buchnera is in an intracellular nonproliferating state in aphid bacteriocytes (specialized symbiont cells). Overall, we identified 90 differentially expressed sRNAs, 97% of which were upregulated in aphid embryos. Of these sRNAs, the majority were predicted to be involved in the regulation of various metabolic processes, including arginine biosynthesis. Using a heterologous dual expression vector, we reveal for the first time that a Buchnera antisense sRNA can post-transcriptionally interact with its cognate Buchnera coding sequence, carB, a gene involved in arginine biosynthesis. These results corroborate our in vivo RNAseq and proteomic data, where the candidate antisense sRNA carB and the protein CarB are significantly upregulated in aphid embryos. Overall, we demonstrate that Buchnera may regulate gene expression independently from its host by utilizing sRNAs.

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Section: Discussionmentioning

confidence: 69%

Section: Discussionmentioning

confidence: 99%

A sRNA in a reduced mutualistic symbiont genome regulates its own gene expression

2017

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“…The microbiomes harbored by insects play important roles in mediating their host health and fitness, and hence have captured more and more attention by entomologists (Oliver et al ., ; Engel & Moran, ; Skidmore & Hansen, ; Blow & Douglas, ). Nowadays, accumulating studies have described the microbial diversity and its variations across different developmental stages in insects, especially for the holometabolous insects, such as Acromyrmex echinatior , Ceratitis capitata and Bactrocera dorsalis (Zhukova et al ., ; Malacrinò et al ., ; Zhao et al ., ).…”

Section: Discussionmentioning

confidence: 99%

Diversity and dynamics of microbial communities in brown planthopper at different developmental stages revealed by high‐throughput amplicon sequencing

et al. 2019

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The microbiome associated with brown planthopper (BPH) plays an important role in mediating host health and fitness. Characterization of the microbial community and its structure is prerequisite for understanding the intricate symbiotic relationships between microbes and host insect. Here, we investigated the bacterial and fungal communities of BPH at different developmental stages using high‐throughput amplicon sequencing. Our results revealed that both the bacterial and fungal communities were diverse and dynamic during BPH development. The bacterial communities were generally richer than fungi in each developmental stage. At 97% similarly, 19 phyla and 278 genera of bacteria were annotated, while five fungal phyla comprising 80 genera were assigned. The highest species richness for the bacterial communities was detected in the nymphal stage. The taxonomic diversity of the fungal communities in female adults was generally at a relatively higher level when compared to other developmental stages. The most dominant phylum of bacteria and fungi at each developmental stage all belonged to Proteobacteria and Ascomycota, respectively. A significantly lower abundance of bacterial genus Acinetobacter was recorded in the egg stage when compared to other developmental stages, while the dominant fungal genus Wallemia was more abundant in the nymph and adult stages than in the egg stage. Additionally, the microbial composition differed between male and female adults, suggesting that the microbial communities in BPH were gender‐dependent. Overall, our study enriches our knowledge on the microbial communities associated with BPH and will provide clues to develop potential biocontrol techniques against this rice pest.

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“…2012 ; Rosas-Pérez etal. 2014 ; Skidmore and Hansen 2017 ). Since flavobacteria and enterobacteria are not found in Dactylopius, Dactylopiibacterium , which has all genes for essential amino acid biosynthesis, might in turn provide essential amino acids to the host.…”

Section: Discussionmentioning

confidence: 99%

Candidatus Dactylopiibacterium carminicum, a Nitrogen-Fixing Symbiont of Dactylopius Cochineal Insects (Hemiptera: Coccoidea: Dactylopiidae)

León

Ormeño‐Orrillo

Ramírez-Puebla

et al. 2017

Genome Biology and Evolution

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The domesticated carmine cochineal Dactylopius coccus (scale insect) has commercial value and has been used for more than 500 years for natural red pigment production. Besides the domesticated cochineal, other wild Dactylopius species such as Dactylopius opuntiae are found in the Americas, all feeding on nutrient poor sap from native cacti. To compensate nutritional deficiencies, many insects harbor symbiotic bacteria which provide essential amino acids or vitamins to their hosts. Here, we characterized a symbiont from the carmine cochineal insects, Candidatus Dactylopiibacterium carminicum (betaproteobacterium, Rhodocyclaceae family) and found it in D. coccus and in D. opuntiae ovaries by fluorescent in situ hybridization, suggesting maternal inheritance. Bacterial genomes recovered from metagenomic data derived from whole insects or tissues both from D. coccus and from D. opuntiae were around 3.6 Mb in size. Phylogenomics showed that dactylopiibacteria constituted a closely related clade neighbor to nitrogen fixing bacteria from soil or from various plants including rice and other grass endophytes. Metabolic capabilities were inferred from genomic analyses, showing a complete operon for nitrogen fixation, biosynthesis of amino acids and vitamins and putative traits of anaerobic or microoxic metabolism as well as genes for plant interaction. Dactylopiibacterium nif gene expression and acetylene reduction activity detecting nitrogen fixation were evidenced in D. coccus hemolymph and ovaries, in congruence with the endosymbiont fluorescent in situ hybridization location. Dactylopiibacterium symbionts may compensate for the nitrogen deficiency in the cochineal diet. In addition, this symbiont may provide essential amino acids, recycle uric acid, and increase the cochineal life span.

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The evolutionary development of plant‐feeding insects and their nutritional endosymbionts

Cited by 45 publications

References 93 publications

A sRNA in a reduced mutualistic symbiont genome regulates its own gene expression

A sRNA in a reduced mutualistic symbiont genome regulates its own gene expression

Diversity and dynamics of microbial communities in brown planthopper at different developmental stages revealed by high‐throughput amplicon sequencing

Candidatus Dactylopiibacterium carminicum, a Nitrogen-Fixing Symbiont of Dactylopius Cochineal Insects (Hemiptera: Coccoidea: Dactylopiidae)

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