Fitness costs of infection with <i>Serratia symbiotica</i> are associated with greater susceptibility to insecticides in the pea aphid <scp><i>Acyrthosiphon pisum</i></scp>

Škaljac, Marisa; Kirfel, Phillipp; Grotmann, Jens; Vilcinskas, Andreas

doi:10.1002/ps.4881

Cited by 63 publications

(87 citation statements)

References 76 publications

(210 reference statements)

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“…Our results demonstrated that, once in the gut, cultivable S. symbiotica infections have negative effects on some A. fabae host life history traits in the absence of environmental stressors. These effects are similar to those found in previous studies that emphasize the costs associated with the presence of facultative endosymbionts for aphids, including the defensive endosymbiont Hamiltonella defensa (23,(27)(28)(29)(30)48). There may be several potential causes of virulence of cultivable S. symbiotica strains.…”

Section: Discussionsupporting

confidence: 86%

“…More erratically distributed in aphid populations than obligate partners, facultative partners are not essential for aphid host growth and reproduction but may lead to the acquisition of ecologically important traits by aphids (4,(23)(24)(25)(26). However, while facultative symbionts can have beneficial fitness consequences for aphid hosts, they can also impose a fitness cost on their host that makes them parasitic (22,(27)(28)(29)(30).…”

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confidence: 99%

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New Insights into the Nature of Symbiotic Associations in Aphids: Infection Process, Biological Effects, and Transmission Mode of Cultivable Serratia symbiotica Bacteria

Pons

Renoz

Noël

et al. 2019

Appl Environ Microbiol

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Symbiotic microorganisms are widespread in nature and can play a major role in the ecology and evolution of animals. The aphid-Serratia symbiotica bacterium interaction provides a valuable model to study the mechanisms behind these symbiotic associations. The recent discovery of cultivable S. symbiotica strains with a free-living lifestyle allowed us to simulate their environmental acquisition by aphids to examine the mechanisms involved in this infection pathway. Here, after oral ingestion, we analyzed the infection dynamics of cultivable S. symbiotica during the host's lifetime using quantitative PCR and fluorescence techniques and determined the immediate fitness consequences of these bacteria on their new host. We further examined the transmission behavior and phylogenetic position of cultivable strains. Our study revealed that cultivable S. symbiotica bacteria are predisposed to establish a symbiotic association with a new aphid host, settling in its gut. We show that cultivable S. symbiotica bacteria colonize the entire aphid digestive tract following infection, after which the bacteria multiply exponentially during aphid development.Our results further reveal that gut colonization by the bacteria induces a fitness cost to their hosts. Nevertheless, it appeared that the bacteria also offer an immediate protection against parasitoids. Interestingly, cultivable S. symbiotica strains seem to be extracellularly transmitted, possibly through the honeydew, while S. symbiotica is generally considered a maternally transmitted bacterium living within the aphid body cavity and bringing some benefits to its hosts, despite its costs. These findings provide new insights into the nature of symbiosis in aphids and the mechanisms underpinning these interactions. IMPORTANCE S. symbiotica is one of the most common symbionts among aphid populations and includes a wide variety of strains whose degree of interdependence on the host may vary considerably. S. symbiotica strains with a free-living capacity have recently been isolated from aphids. By using these strains, we established artificial associations by simulating new bacterial acquisitions involved in aphid gut infections to decipher their infection processes and biological effects on their new hosts. Our results showed the early stages involved in this route of infection. So far, S. symbiotica has been considered a maternally transmitted aphid endosymbiont. Nevertheless, we show that our cultivable S. symbiotica strains occupy and replicate in the aphid gut and seem to be transmitted over generations through an environmental transmission mechanism. Moreover, cultivable S. symbiotica bacteria are both parasites and mutualists given the context, as are many aphid endosymbionts. Our findings give new perception of the associations involved in bacterial mutualism in aphids.

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Section: Discussionsupporting

confidence: 86%

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confidence: 99%

New Insights into the Nature of Symbiotic Associations in Aphids: Infection Process, Biological Effects, and Transmission Mode of Cultivable Serratia symbiotica Bacteria

Pons

Renoz

Noël

et al. 2019

Appl Environ Microbiol

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“…were also eliminated using microinjections of ampicillin (Leonardo, 2004;Sakurai et al, 2005;Simon et al, 2011), but this method failed to remove Hamiltonella defensa (Leonardo, 2004). One study also selectively eliminated S. symbiotica with ampicillin using an artificial medium supplemented with the antibiotic to feed A. pisum (Skaljac et al, 2018). Other methods using a cocktail of ampicillin, cefotaxime, and gentamicin instead of ampicillin solely allowed elimination of Fukatsuia symbiotica (also known as PAXS or Pea aphid X-type), H. defensa, R. insecticola, and S. symbiotica (Douglas et al, 2006;McLean et al, 2011;Simon et al, 2011) but failed to eliminate Rickettsia sp., Rickettsiella viridis, and Spiroplasma sp.…”

Section: Introductionmentioning

confidence: 99%

Examination of the success rate of secondary symbiont manipulation by microinjection methods in the pea aphid system

Sochard

Morlière

Toussaint

et al. 2020

Entomologia Exp Applicata

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Insects harbor a wide range of microbial symbionts, but their influence on host phenotypes is described in a limited number of biological models. One experimental approach to gain knowledge on the effects of symbionts to their hosts is to create insect lines with and without symbionts and examine their phenotypes. However, the success rate of symbiont elimination and introduction methods is dependent on several parameters that are scarcely tested or described. The pea aphid, Acyrthosiphon pisum Harris (Hemiptera: Aphididae), is a model insect of symbiosis studies. It harbors a primary symbiont that supplies the host with essential amino acids, and an array of secondary symbionts whose effects have been assessed by manipulating their presence/absence in the insect. Here, we describe the influence of key parameters on the success rate of symbiont manipulation using the pea aphid–secondary symbiont system. We compared two elimination methods differing in antibiotic treatment using several aphid–symbiont combinations. We also created new aphid host–symbiont combinations by secondary symbiont introduction and examined the effects of larval stage of recipient aphids on introduction success. Our study revealed that the aphid–symbiont combination has strong influence on both symbiont introduction and elimination success rates, and that the type of antibiotics and the larval stage of recipient aphids influence the elimination and introduction success rate, respectively.

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“…symbiotica ; Chen et al (2000); Mathé-Hubert et al (2019)), lower adult mass ( S . symbiotica; Skaljac et al (2018)), and increased susceptibility to insecticide ( S . symbiotica; Skaljac et al (2018)).…”

Section: Introductionmentioning

confidence: 99%

“…symbiotica; Skaljac et al (2018)), and increased susceptibility to insecticide ( S . symbiotica; Skaljac et al (2018)).…”

Section: Introductionmentioning

confidence: 99%

A fitness cost resulting fromHamiltonella defensainfection is associated with altered probing and feeding behaviour inRhopalosiphum padi

Leybourne

Valentine

Bos

et al. 2019

Preprint

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Aphids frequently associate with facultative endosymbiotic bacteria which influence aphid physiology in myriad ways. Endosymbiont infection can increase aphid resistance against parasitoids and pathogens, modulate plant responses to aphid feeding, and promote aphid virulence. These endosymbiotic relationships can also decrease aphid fitness in the absence of natural enemies or when feeding on less suitable plant types. Here, we use the Electrical Penetration Graph (EPG) technique to monitor feeding behaviour of four genetically-similar clonal lines of a cereal-feeding aphid, Rhopalosiphum padi, differentially infected (+/−) with the facultative protective endosymbiont, Hamiltonella defensa, to understand how physiological processes at the aphid-plant interface are affected by endosymbiont infection. Endosymbiont-infected aphids exhibited altered probing and feeding patterns compared with uninfected aphids, characterised by a two-fold increase in the number of plant cell punctures, a 50% reduction in the duration of each cellular puncture, and a greater probability of achieving sustained ingestion of plant phloem. Feeding behaviour was altered further by host plant identity: endosymbiont-infected aphids spent less time probing into plant tissue, required twice as many probes into plant tissue to reach plant phloem, and showed a 44% reduction in phloem ingestion when feeding on the partially-resistant wild relative of barley, Hordeum spontaneum 5, compared with a commercial barley cultivar. These observations might explain reduced growth of H. defensa-infected aphids on the former host plant. This study is the first to demonstrate a physiological mechanism at the aphid-plant interface contributing to endosymbiont effects on aphid fitness on different quality plants through altered aphid feeding behaviour.SummaryReduced performance of aphids infected with a common facultative endosymbiont on poor quality plants may be explained by changes in aphid probing behaviour and decreased phloem sap ingestion.

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Fitness costs of infection with Serratia symbiotica are associated with greater susceptibility to insecticides in the pea aphid Acyrthosiphon pisum

Cited by 63 publications

References 76 publications

New Insights into the Nature of Symbiotic Associations in Aphids: Infection Process, Biological Effects, and Transmission Mode of Cultivable Serratia symbiotica Bacteria

New Insights into the Nature of Symbiotic Associations in Aphids: Infection Process, Biological Effects, and Transmission Mode of Cultivable Serratia symbiotica Bacteria

Examination of the success rate of secondary symbiont manipulation by microinjection methods in the pea aphid system

A fitness cost resulting fromHamiltonella defensainfection is associated with altered probing and feeding behaviour inRhopalosiphum padi

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