scholarly journals Costs and benefits of a superinfection of facultative symbionts in aphids

2006 ◽  
Vol 273 (1591) ◽  
pp. 1273-1280 ◽  
Author(s):  
Kerry M Oliver ◽  
Nancy A Moran ◽  
Martha S Hunter

Symbiotic associations between animals and inherited micro-organisms are widespread in nature. In many cases, hosts may be superinfected with multiple inherited symbionts. Acyrthosiphon pisum (the pea aphid) may harbour more than one facultative symbiont (called secondary symbionts) in addition to the obligate primary symbiont, Buchnera aphidicola . Previously we demonstrated that, in a controlled genetic background, A. pisum infected with either Serratia symbiotica or Hamiltonella defensa (called R- and T-type in that study) were more resistant to attack by the parasitoid Aphidius ervi . Here, we examined the consequences of A. pisum superinfected with both resistance-conferring symbionts. We found that an A. pisum line co-infected with both S. symbiotica and H. defensa symbionts exhibits even greater resistance to parasitism by A. ervi than either of the singly infected lines. Despite this added benefit to resistance, superinfections of S. symbiotica and H. defensa symbionts appeared rare in our survey of Utah A. pisum symbionts, which is probably attributable to severe fecundity costs. Quantitative polymerase chain reaction estimates indicate that while the density of H. defensa is similar in singly and superinfected hosts, S. symbiotica densities increased dramatically in superinfected hosts. Over-proliferation of symbionts or antagonistic interactions between symbionts may be harmful to the aphid host. Our results indicate that in addition to host–symbiont interactions, interactions among the symbionts themselves probably play a critical role in determining the distributions of symbionts in natural populations.

PLoS ONE ◽  
2020 ◽  
Vol 15 (11) ◽  
pp. e0242159
Author(s):  
Ailsa H. C. McLean ◽  
Benjamin J. Parker

Evolutionary interactions between parasitoid wasps and insect hosts have been well studied at the organismal level, but little is known about the molecular mechanisms that insects use to resist wasp parasitism. Here we study the interaction between a braconid wasp (Aphidius ervi) and its pea aphid host (Acyrthosiphon pisum). We first identify variation in resistance to wasp parasitism that can be attributed to aphid genotype. We then use transcriptome sequencing to identify genes in the aphid genome that are differentially expressed at an early stage of parasitism, and we compare these patterns in highly resistant and susceptible aphid host lines. We find that resistant genotypes are upregulating genes involved in carbohydrate metabolism and several key innate immune system genes in response to parasitism, but that this response seems to be weaker in susceptible aphid genotypes. Together, our results provide a first look into the complex molecular mechanisms that underlie aphid resistance to wasp parasitism and contribute to a broader understanding of how resistance mechanisms evolve in natural populations.


1984 ◽  
Vol 74 (4) ◽  
pp. 647-656 ◽  
Author(s):  
P. J. Cameron ◽  
W. Powell ◽  
H. D. Loxdale

AbstractAphidius ervi Hal. parasitised natural populations of Acyrthosiphon pisum (Harris), Sitobion avenae (F.) and Microlophium carnosum (Buckt.) in Britain but parasitised few examples of S. avenae placed on trap plants in winter wheat, nettle-grass edge areas or lucerne-wheat strip crops. In laboratory experiments, Aphidius ervi reared from Acyrthosiphon pisum did not parasitise M. carnosum, and significantly fewer mummies were formed on S. avenae than on A. pisum. After rearing Aphidius ervi for 4–5 generations on S. avenae, similar numbers of mummies were formed on both hosts. The switch of hosts from Acyrthosiphon pisum to S. avenae was associated with the loss of certain parasitoid esterase enzyme bands revealed following electrophoretic separation of parasitoid proteins. Slow adaptation to new aphid hosts by polyphagous parasitoids such as Aphidius ervi may reduce the usefulness of reservoirs as a source of beneficial species.


2015 ◽  
Vol 282 (1811) ◽  
pp. 20150977 ◽  
Author(s):  
Ailsa H. C. McLean ◽  
H. Charles J. Godfray

Many insects harbour facultative symbiotic bacteria, some of which have been shown to provide resistance against natural enemies. One of the best-known protective symbionts is Hamiltonella defensa , which in pea aphid ( Acyrthosiphon pisum ) confers resistance against attack by parasitoid wasps in the genus Aphidius (Braconidae). We asked (i) whether this symbiont also confers protection against a phylogenetically distant group of parasitoids (Aphelinidae) and (ii) whether there are consistent differences in the effects of bacteria found in pea aphid biotypes adapted to different host plants. We found that some H. defensa strains do provide protection against an aphelinid parasitoid Aphelinus abdominalis. Hamiltonella defensa from the Lotus biotype provided high resistance to A. abdominalis and moderate to low resistance to Aphidius ervi , while the reverse was seen from Medicago biotype isolates. Aphids from Ononis showed no evidence of symbiont-mediated protection against either wasp species and were relatively vulnerable to both. Our results may reflect the different selection pressures exerted by the parasitoid community on aphids feeding on different host plants, and could help explain the maintenance of genetic diversity in bacterial symbionts.


2017 ◽  
Vol 284 (1866) ◽  
pp. 20171925 ◽  
Author(s):  
Jayce W. Brandt ◽  
Germain Chevignon ◽  
Kerry M. Oliver ◽  
Michael R. Strand

Heritable symbionts are common in insects with many contributing to host defence. Hamiltonella defensa is a facultative, bacterial symbiont of the pea aphid, Acyrthosiphon pisum that provides protection against the endoparasitoid wasp Aphidius ervi . Protection levels vary among strains of H. defensa that are differentially infected by bacteriophages named APSEs. By contrast, little is known about mechanism(s) of resistance owing to the intractability of host-restricted microbes for functional study. Here, we developed methods for culturing strains of H. defensa that varied in the presence and type of APSE. Most H. defensa strains proliferated at 27°C in co-cultures with the TN5 cell line or as pure cultures with no insect cells. The strain infected by APSE3, which provides high levels of protection in vivo , produced a soluble factor(s) that disabled development of A. ervi embryos independent of any aphid factors. Experimental transfer of APSE3 also conferred the ability to disable A. ervi development to a phage-free strain of H. defensa . Altogether, these results provide a critical foundation for characterizing symbiont-derived factor(s) involved in host protection and other functions. Our results also demonstrate that phage-mediated transfer of traits provides a mechanism for innovation in host restricted symbionts.


2021 ◽  
Vol 9 ◽  
Author(s):  
Mélanie Leclair ◽  
Christelle Buchard ◽  
Frédérique Mahéo ◽  
Jean-Christophe Simon ◽  
Yannick Outreman

In the last decade, the influence of microbial symbionts on ecological and physiological traits of their hosts has been increasingly recognized. However, most of these effects have been revealed under laboratory conditions, which oversimplifies the complexity of the factors involved in the dynamics of symbiotic associations in nature. The pea aphid, Acyrthosiphon pisum, forms a complex of plant-adapted biotypes, which strongly differ in the prevalence of their facultative endosymbionts. Some of the facultative endosymbionts of A. pisum have been shown to confer protection against natural enemies, among which Hamiltonella defensa is known to protect its host from parasitoid wasps. Here, we tested under natural conditions whether the endosymbiont communities of different A. pisum biotypes had a protective effect on their hosts and whether endosymbiotic associations and parasitoid communities associated with the pea aphid complex were linked. A space-time monitoring of symbiotic associations, parasitoid pressure and parasitoid communities was carried out in three A. pisum biotypes respectively specialized on Medicago sativa (alfalfa), Pisum sativum (pea), and Trifolium sp. (clover) throughout the whole cropping season. While symbiotic associations, and to a lesser extent, parasitoid communities were stable over time and structured mainly by the A. pisum biotypes, the parasitoid pressure strongly varied during the season and differed among the three biotypes. This suggests a limited influence of parasitoid pressure on the dynamics of facultative endosymbionts at a seasonal scale. However, we found a positive correlation between the α and β diversities of the endosymbiont and parasitoid communities, indicating interactions between these two guilds. Also, we revealed a negative correlation between the prevalence of H. defensa and Fukatsuia symbiotica in co-infection and the intensity of parasitoid pressure in the alfalfa biotype, confirming in field conditions the protective effect of this symbiotic combination.


2020 ◽  
Vol 19 ◽  
pp. 153303382096558
Author(s):  
Lixia Shan ◽  
Tao Zhao ◽  
Yu Wang

Objective: Long non-coding RNAs (lncRNAs) play a critical role in tumorigenesis. Upregulation of lncRNA deleted in lymphocytic leukemia 1 (DLEU1) has been reported in endometrial cancer (EC) tissues. This prospective study aimed to determine the potential clinical significance of serum lncRNA DLEU1 in EC. Methods: The serum lncRNA DLEU1 level was detected in EC patients, patients with endometrial hyperplasia and healthy controls by reverse transcription-quantitative polymerase chain reaction (RT-qPCR). Then its clinical value in EC was further evaluated. Results: Our results demonstrated that serum lncRNA DLEU1 levels were significantly increased in patients with EC, and serum lncRNA DLEU1 showed good performance for discriminating EC patients from patients with endometrial hyperplasia and healthy controls. In addition, EC patients with advanced clinicopathological features had higher circulating lncRNA DLEU1 level than those with favorable clinical characteristics. Moreover, EC patients in the high serum lncRNA DLEU1 group suffered worse overall survival and disease-free survival than those in the low serum lncRNA DLEU1 group. Furthermore, multivariate cox regression analysis displayed that the serum lncRNA DLEU1 served as an independent prognostic factor for EC. Conclusions: Collectively, our study suggests that serum lncRNA DLEU1 is a novel and promising biomarker for prognostic estimation of EC.


EvoDevo ◽  
2020 ◽  
Vol 11 (1) ◽  
Author(s):  
Celeste R. Banfill ◽  
Alex C. C. Wilson ◽  
Hsiao-ling Lu

Abstract Background Host/symbiont integration is a signature of evolutionarily ancient, obligate endosymbioses. However, little is known about the cellular and developmental mechanisms of host/symbiont integration at the molecular level. Many insects possess obligate bacterial endosymbionts that provide essential nutrients. To advance understanding of the developmental and metabolic integration of hosts and endosymbionts, we track the localization of a non-essential amino acid transporter, ApNEAAT1, across asexual embryogenesis in the aphid, Acyrthosiphon pisum. Previous work in adult bacteriomes revealed that ApNEAAT1 functions to exchange non-essential amino acids at the A. pisum/Buchnera aphidicola symbiotic interface. Driven by amino acid concentration gradients, ApNEAAT1 moves proline, serine, and alanine from A. pisum to Buchnera and cysteine from Buchnera to A. pisum. Here, we test the hypothesis that ApNEAAT1 is localized to the symbiotic interface during asexual embryogenesis. Results During A. pisum asexual embryogenesis, ApNEAAT1 does not localize to the symbiotic interface. We observed ApNEAAT1 localization to the maternal follicular epithelium, the germline, and, in late-stage embryos, to anterior neural structures and insect immune cells (hemocytes). We predict that ApNEAAT1 provisions non-essential amino acids to developing oocytes and embryos, as well as to the brain and related neural structures. Additionally, ApNEAAT1 may perform roles related to host immunity. Conclusions Our work provides further evidence that the embryonic and adult bacteriomes of asexual A. pisum are not equivalent. Future research is needed to elucidate the developmental time point at which the bacteriome reaches maturity.


2014 ◽  
Vol 281 (1791) ◽  
pp. 20141163 ◽  
Author(s):  
Calum W. Russell ◽  
Anton Poliakov ◽  
Meena Haribal ◽  
Georg Jander ◽  
Klaas J. van Wijk ◽  
...  

Various animals derive nutrients from symbiotic microorganisms with much-reduced genomes, but it is unknown whether, and how, the supply of these nutrients is regulated. Here, we demonstrate that the production of essential amino acids (EAAs) by the bacterium Buchnera aphidicola in the pea aphid Acyrthosiphon pisum is elevated when aphids are reared on diets from which that EAA are omitted, demonstrating that Buchnera scale EAA production to host demand. Quantitative proteomics of bacteriocytes (host cells bearing Buchnera ) revealed that these metabolic changes are not accompanied by significant change in Buchnera or host proteins, suggesting that EAA production is regulated post-translationally. Bacteriocytes in aphids reared on diet lacking the EAA methionine had elevated concentrations of both methionine and the precursor cystathionine, indicating that methionine production is promoted by precursor supply and is not subject to feedback inhibition by methionine. Furthermore, methionine production by isolated Buchnera increased with increasing cystathionine concentration. We propose that Buchnera metabolism is poised for EAA production at certain maximal rates, and the realized release rate is determined by precursor supply from the host. The incidence of host regulation of symbiont nutritional function via supply of key nutritional inputs in other symbioses remains to be investigated.


BMC Genomics ◽  
2014 ◽  
Vol 15 (1) ◽  
pp. 342 ◽  
Author(s):  
Dominique Colinet ◽  
Caroline Anselme ◽  
Emeline Deleury ◽  
Donato Mancini ◽  
Julie Poulain ◽  
...  

2017 ◽  
Vol 83 (8) ◽  
Author(s):  
Matthew R. Doremus ◽  
Kerry M. Oliver

ABSTRACT Insects and other animals commonly form symbioses with heritable bacteria, which can exert large influences on host biology and ecology. The pea aphid, Acyrthosiphon pisum, is a model for studying effects of infection with heritable facultative symbionts (HFS), and each of its seven common HFS species has been reported to provide resistance to biotic or abiotic stresses. However, one common HFS, called X-type, rarely occurs as a single infection in field populations and instead typically superinfects individual aphids with Hamiltonella defensa, another HFS that protects aphids against attack by parasitic wasps. Using experimental aphid lines comprised of all possible infection combinations in a uniform aphid genotype, we investigated whether the most common strain of X-type provides any of the established benefits associated with aphid HFS as a single infection or superinfection with H. defensa. We found that X-type does not confer protection to any tested threats, including parasitoid wasps, fungal pathogens, or thermal stress. Instead, component fitness assays identified large costs associated with X-type infection, costs which were ameliorated in superinfected aphids. Together these findings suggest that X-type exploits the aphid/H. defensa mutualism and is maintained primarily as a superinfection by “hitchhiking” via the mutualistic benefits provided by another HFS. Exploitative symbionts potentially restrict the functions and distributions of mutualistic symbioses with effects that extend to other community members. IMPORTANCE Maternally transmitted bacterial symbionts are widespread and can have major impacts on the biology of arthropods, including insects of medical and agricultural importance. Given that host fitness and symbiont fitness are tightly linked, inherited symbionts can spread within host populations by providing beneficial services. Many insects, however, are frequently infected with multiple heritable symbiont species, providing potential alternative routes of symbiont maintenance. Here we show that a common pea aphid symbiont called X-type likely employs an exploitative strategy of hitchhiking off the benefits of a protective symbiont, Hamiltonella. Infection with X-type provides none of the benefits conferred by other aphid symbionts and instead results in large fitness costs, costs lessened by superinfection with Hamiltonella. These findings are corroborated by natural infections in field populations, where X-type is mostly found superinfecting aphids with Hamiltonella. Exploitative symbionts may be common in hosts with communities of heritable symbionts and serve to hasten the breakdown of mutualisms.


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