Draft Genomes, Phylogenetic Reconstruction, and Comparative Genomics of Two Novel Cohabiting Bacterial Symbionts Isolated from<i>Frankliniella occidentalis</i>

Facey, Paul D.; Méric, Guillaume; Hitchings, Matthew D.; Pachebat, Justin A.; Hegarty, Matthew J.; Chen, Hong; Morgan, Laura V.A.; Hoeppner, James E.; Whitten, Miranda M. A.; Kirk, William D. J.; Dyson, Paul; Sheppard, Samuel K.; Sol, Ricardo Del

doi:10.1093/gbe/evv136

Cited by 37 publications

(46 citation statements)

References 61 publications

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“…With regards to orthotospovirus-thrips interactions, global expression analyses of whole bodies of F. occidentalis [18, 19] and other thrips vectors [20, 21] indicated the occurrence of insect innate immune responses to virus infection. In addition to serving as crop disease vectors, thrips support vertically transmitted, facultative bacterial symbionts that reside in the hindgut [22, 23].…”

Section: Introductionmentioning

confidence: 99%

Genome-enabled insights into the biology of thrips as crop pests

Rotenberg

Baumann

Ben-Mahmoud

et al. 2020

Preprint

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54Background: The western flower thrips, Frankliniella occidentalis (Pergande), is a globally 55 invasive pest and plant virus vector on a wide array of food, fiber and ornamental crops. While 56 there are numerous studies centered on thrips pest and vector biology, feeding behaviors, ecology, 57 and insecticide resistance, the underlying genetic mechanisms of the processes governing these 58 areas of research are largely unknown. To address this gap, we present the F. occidentalis draft 59 genome assembly and official gene set. 60Results: We report on the first genome sequence for any member of the insect order Thysanoptera. 61 Benchmarking Universal Single-Copy Ortholog (BUSCO) assessments of the genome assembly 62 (size = 415.8 Mb, scaffold N50 = 948.9 Kb) revealed a relatively complete and well-annotated 63 assembly in comparison to other insect genomes. The genome is unusually GC-rich (50%) 64 compared to other insect genomes to date. The official gene set (OGS v1.0) contains 16,859 genes, 65 of which ~10% were manually verified and corrected by our consortium. We focused on manual 66 annotation, phylogenetic and expression evidence analyses for gene sets centered on primary 67 themes in the life histories and activities of plant-colonizing insects. Highlights include: 1) 68 divergent clades and large expansions in genes associated with environmental sensing 69 (chemosensory receptors) and detoxification (CYP4, CYP6 and CCE enzymes) of substances 70 encountered in agricultural environments; 2) a comprehensive set of salivary gland-associated 71 genes supported by enriched expression; 3) apparent absence of members of the IMD innate 72 3 immune defense pathway; and 4) developmental-and sex-specific expression analyses of genes 73 associated with progression from larvae to adulthood through neometaboly, a distinct form of 74 maturation compared to complete metamorphosis in the Holometabola. 75 Conclusions: Analysis of the F. occidentalis genome offers insights into the polyphagous behavior 76 of this insect pest to find, colonize and survive on a widely diverse array of plants. The genomic 77 resources presented here enable a more complete analysis of insect evolution and biology, 78 providing a missing taxon for contemporary insect genomics-based analyses. Our study also offers 79 a genomic benchmark for molecular and evolutionary investigations of other thysanopteran 80 species. 81 KEY WORDS 82 Thysanoptera, western flower thrips, hemipteroid assemblage, insect genomics, tospovirus, 83 virus-vector interactions, salivary glands, chemosensory receptors, opsins, detoxification, innate 84 immunity 85 86 BACKGROUND 87Thrips are small, polyphagous and cosmopolitan insects that comprise the order Thysanoptera. 88Thysanoptera lies within the Paraneoptera, also commonly called the "hemipteroid assemblage" 89 which also includes the orders Hemiptera, Psocoptera, and Phthiraptera. Among the over 7,000 90 reported thrips species classified into nine families with an additional five identified from fossil 91 species [1]...

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Section: Introductionmentioning

confidence: 99%

Genome-enabled insights into the biology of thrips as crop pests

Rotenberg

Baumann

Ben-Mahmoud

et al. 2020

Preprint

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“…[Corrections added on November 23, 2016, after first online publication: Multiple reference citations were corrected throughout the article. On page 7, “[…] symbiont of the pigeon louse fly),” was changed to “[…] symbiont of the pigeon louse fly),”; on page 8, “[…] relative to DNA deletion …”

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confidence: 99%

Dissecting genome reduction and trait loss in insect endosymbionts

Latorre

Manzano-Marı́n

2016

Annals of the New York Academy of Sciences

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Symbiosis has played a major role in eukaryotic evolution beyond the origin of the eukaryotic cell. Thus, organisms across the tree of life are associated with diverse microbial partners, conferring to the host new adaptive traits that enable it to explore new niches. This is the case for insects thriving on unbalanced diets, which harbor mutualistic intracellular microorganisms, mostly bacteria that supply them with the required nutrients. As a consequence of the lifestyle change, from free-living to host-associated mutualist, a bacterium undergoes many structural and metabolic changes, of which genome shrinkage is the most dramatic. The trend toward genome size reduction in endosymbiotic bacteria is associated with large-scale gene loss, reflecting the lack of an effective selection mechanism to maintain genes that are rendered superfluous by the constant and rich environment provided by the host. This genome-reduction syndrome is so strong that it has generated the smallest bacterial genomes found to date, whose gene contents are so limited that their status as cellular entities is questionable. The recent availability of data on several endosymbiotic bacteria is enabling us to form a comprehensive picture of the genome-reduction process and the phenotypic consequences for the dwindling symbiont.

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“…Thus, aphid feeding is a likely source for the presence and persistence of Erwinia bacteria inside the aphid digestive tract. It is important to note that the aforementioned Erwinia symbionts described for F. occidentalis (Facey et al, 2015) (INSDC accessions JMSO00000000.1, LAGQ00000000.1, and LAGP00000000.1) belong to the E. aphidicola species (AB681773.1; type strain X 001=CIP 106296=IAM 14479=JCM 21238=LMG 24877=NBRC 102417), based on 16S sequence identity (between 99.72-100.00%). This indicates that strains from these bacterial species can actually infect very distantly related insect species such as aphids and thrips.…”

Section: Discussionmentioning

confidence: 99%

Serial horizontal transfer of vitamin-biosynthetic genes enables the establishment of new nutritional symbionts in aphids’ di-symbiotic systems

Manzano-Marı́n

d’Acier

Clamens

et al. 2019

Preprint

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Many insects with a nutrient-restricted diet depend on obligate mutualistic bacteria for the provisioning of essential nutrients lacking from their food source, namely essential amino acids and B vitamins. Most aphids (Hemiptera: Aphididae), whose diet consists of phloem, rely on the bacterial endosymbiont Buchnera for the supply of the aforementioned compounds. However, in some aphid lineages Buchnera have lost the capability of producing these nutrients and thus the symbiotic consortium has accommodated an extra bacterial partner to supplement Buchnera's deficiencies. In this work, we explore the di-symbiotic nutritional endosymbiosis of a group of Cinara aphids which has been found to harbour both Buchnera and an Erwinia-related symbiont. Using fluorescence in situ hybridisation, we have located this symbiont to the bacteriome where it inhabits its own bacteriocytes. Through whole-genome sequencing of the endosymbionts of 9 species of Erwinia-associated Cinara aphids, we have found that Ewrinia genomes are highly syntenic and all show significant genome reduction. Additionally, Erwinia symbionts display phylogenetic congruency with Buchnera, suggesting long-term co-divergence. Most significantly, we found that not only is Erwinia capable of complementing Buchnera's auxotrophies, but that the genes involved in the biosynthesis of two B vitamins have actually been horizontally acquired from a Sodalis-related bacterium. Finally, this B-vitamin biosynthetic genes have been further transferred to a new Hamiltonella co-obligate symbiont in a specific Cinara lineage, thus displaying a tri-symbiotic system. These results highlight the important role horizontal gene transfer plays in the establishment of new obligate nutritional symbionts.

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Draft Genomes, Phylogenetic Reconstruction, and Comparative Genomics of Two Novel Cohabiting Bacterial Symbionts Isolated fromFrankliniella occidentalis

Cited by 37 publications

References 61 publications

Genome-enabled insights into the biology of thrips as crop pests

Genome-enabled insights into the biology of thrips as crop pests

Dissecting genome reduction and trait loss in insect endosymbionts

Serial horizontal transfer of vitamin-biosynthetic genes enables the establishment of new nutritional symbionts in aphids’ di-symbiotic systems

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