A metagenomic approach from aphid’s hemolymph sheds light on the potential roles of co-existing endosymbionts

Abstract

BackgroundAphids are known to live in symbiosis with specific bacteria, called endosymbionts which can be classified as obligate or accessory. Buchnera aphidicola is generally the only obligatory symbiont present in aphids, supplying essential nutrients that are missing in the plants phloem to its host. Pentalonia nigronervosa is the main vector of the banana bunchy top virus, one of the most damageable viruses in banana. This aphid is carrying two symbionts: B. aphidicola (BPn) and Wolbachia sp. (wPn). The high occurrence of Wolbachia in the banana aphid raises questions about the role it plays in this insect. The goal of this study was to go further in the understanding of the role played by the two symbionts in P. nigronervosa. To do so, microinjection tests were made to see the effect of wPn elimination on the host, and then, high-throughput sequencing of the haemolymph was used to analyze the gene content of the symbionts.ResultsWe observed that the elimination of wPn systematically led to the death of aphids, suggesting that the bacterium could play a mutualistic role. In addition, we identify and annotate 587 and 250 genes for wPn and BPn, respectively, through high-throughput sequencing. Analysis of these genes suggests that the two bacteria are working together for the production of several essential nutrients. The most striking cases are for lysin and riboflavin which are usually provided by B. aphidicola alone to the host. In the banana aphid, the genes involved in the production pathways of these metabolites are shared between the two bacteria making them both essential for the survival of the aphid host.ConclusionsOur results suggest that a co-obligatory symbiosis between B. aphidicola and Wolbachia occurs in the banana aphid, the two bacteria acting together to supply essential nutrients to the host. This is, to our knowledge, the first time Wolbachia is reported to play an essential role in aphids.Electronic supplementary materialThe online version of this article (doi:10.1186/s40168-015-0130-5) contains supplementary material, which is available to authorized users.

The price of protection: a defensive endosymbiont impairs nymph growth in the bird cherry‐oat aphid, Rhopalosiphum padi

“…Additional coobligatory symbioses with B. aphidiciola have been described in other aphid species, including cosymbiosis with Wolbachia sp. in the banana aphid, Pentalonia nigronervosa (Coquerel) (De Clerck et al ., ), and Serratia symbiotica in Cinara species (Meseguer et al ., ). The most frequently detected facultative endosymbionts of aphids are Hamiltonella defensa , Regiella insecticola , S. symbiotica , Rickettsia sp., Ricketsiella sp., Spiroplasma sp., the Pea Aphid X‐type Symbiont ( PAXS ) and Wolbachia sp.…”

Plant Virus–Insect Vector Interactions: Current and Potential Future Research Directions

“…Although Wolbachia has not been identified in the vast majority of aphid species, Wolbachia is known to be present in at least some plant feeding insect vectors including the whitefly [135,163,164,165]. Using a metagenomic approach, Wolbachia was recently shown to play a role in the supply of essential nutrients to the banana aphid [166]. Antibiotic removal of these symbionts may have detrimental effects on aphid vector survival.…”

No evidence forWolbachiaas a nutritional co-obligate endosymbiont in the aphidPentalonia nigronervosa

“…In this study I re-analyse previously published sequencing data from the banana aphid Pentalonia nigronervosa. I show that the metabolic inference results from De Clerck et al (2015) are incorrect and possibly arise from the use of inadequate methods. Additionally, I discuss how the biased interpretation of their antibiotic treatment analyses together with the incorrect metabolic inference resulted in the erroneous suggestion "that a co-obligatory symbiosis between B. aphidicola and Wolbachia occurs in the banana aphid".…”

“…I find that this Buchnera has equivalent biosynthetic capabilities; concerning essential amino acids, B-vitamins, and co-factors; to all published Buchnera strains from "mono-symbiotic" aphids (only harbouring Buchnera as the nutritional co-obligate symbiont), and thus should not need an additional partner to fulfil its nutritional role. I also critically discuss the interpretation of the experimental results presented by De Clerck et al (2015) and conclude that their suggestion of the nutritional-based co-obligate nature of Wolbachia in P. nigronervosa derives from inadequate analyses of their data as well as a biased interpretation of their experimental results.…”

“…In a previous study, De Clerck et al (2015) claimed to present evidence for a potential co-obligate association of Buchnera and Wolbachia in the aphid Pentalonia nigronervosa. They reach these conclusions mainly based on 4 lines of evidence:…”