Aphid facultative symbionts confer no protection against the fungal entomopathogen Batkoa apiculata

Inchauregui, Rose A.; Tallapragada, Keertana; Parker, Benjamin J.

doi:10.1371/journal.pone.0286095

Cited by 7 publications

(4 citation statements)

References 31 publications

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“…No plates from control aphids grew bacterial colonies; however, Pandora spores from infected aphids successfully transferred the transformed Serratia to plates at varying CFUs (Figure 4). Aphid facultative symbionts confer protection against specialist fungal pathogens in the family Entomophthorales (30)(31)(32)(33). We found that when a fungal pathogen is able to overcome this protection and infect a host (which occurs in both the lab and field (34,35,39)), the pathogen suffers reduced virulence against subsequent hosts.…”

Section: Resultsmentioning

confidence: 88%

“…These microbes include several species of 'facultative' bacteria that are not required for host survival but have different phenotypic effects on hosts (29). Several distantly related species of bacterial symbionts, including Regiella insecticola, confer protection to aphids against Pandora (30)(31)(32) (but not against a generalist species in the order Entomophthorales (33)). However, the protection is not perfect and pathogens are able to overcome symbiont-mediated protection in both lab infections and in the field (34).…”

Section: Introductionmentioning

confidence: 99%

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Pathogen-microbiome interactions and the virulence of an entomopathogenic fungus

Kolp,

de Anda Acosta,

Brewer

et al. 2023

Preprint

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Bacteria shape interactions between hosts and fungal pathogens. In some cases, bacteria associated with fungi are essential for pathogen virulence. In other systems, host associated microbiomes confer resistance against fungal pathogens. We studied an aphid-specific entomopathogenic fungus calledPandora neoaphidisin the context of both host and pathogen microbiomes. Aphids host several species of heritable bacteria, some of which confer resistance againstPandora. We first found that spores that emerged from aphids that harbored protective bacteria were less virulent against subsequent hosts and did not grow on plate media. We then used 16S amplicon sequencing to study the bacterial microbiome of fungal mycelia and spores during plate culturing and host infection. We found that the bacterial community is remarkably stable in culture despite dramatic changes in pathogen virulence. Last, we used an experimentally transformed symbiont of aphids to show thatPandoracan acquire hostassociated bacteria during infection. Our results uncover new roles for bacteria in the dynamics of aphidpathogen interactions and illustrate the importance of the broader microbiological context in studies of fungal pathogenesis.

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Section: Resultsmentioning

confidence: 88%

Section: Introductionmentioning

confidence: 99%

Pathogen-microbiome interactions and the virulence of an entomopathogenic fungus

Kolp,

de Anda Acosta,

Brewer

et al. 2023

Preprint

Self Cite

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“…As a conseqiuence, such symbionts are found to be directly involved in symbiont -aphid -parasitoid/predator interaction (Purkiss et al 2022). In contrast, the presence of the facultative symbiont R.insecticola in the body of A. pisum does not provide protection against the pathogenic fungus Batkoa apiculate (Inchauregui et al 2023).…”

Section: Mechanisms Of Symbiont Acquisition Via Nematode Infectionmentioning

confidence: 99%

Aphid adaptation in a changing environment through their bacterial endosymbionts: an overview, including a new major cereal pest (Rhopalosiphum maidis (Fitch) scenario

Csorba,

Dinescu,

Pircalabioru

et al. 2024

Symbiosis

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Aphids (Hemiptera: Aphididae) are small, phloem-feeding insects that exhibit remarkable adaptability and resilience to various environmental conditions, including heat stress. Recent research has shed light on the role of bacterial symbionts in influencing the heat tolerance of aphids. Additionally, an intriguing avenue of investigation has explored how aphids can acquire bacterial symbionts through a unique mechanism involving soil nematodes. In this paper, we provide an in-depth overview of the interplay between heat stress, bacterial symbionts, and soil nematodes in the context of aphid biology. In reviewing the existing literature and collating available knowledge, we highlight the mechanisms by which bacterial symbionts contribute to aphid heat stress tolerance and examine the symbiont acquisition process facilitated by soil nematodes. Furthermore, we discuss the implications of these symbiotic associations in relation to the ecology, evolution, and agricultural management of a major globally expanding pest aphid, the corn leaf aphid, Rhopalosiphum maidis (Fitch). Overall, it may be concluded that both primary and secondary bacterial endosymbionts play a significant role in aphid biology with evolutionary consequences. These include adaptations through bacterial symbionts in terms of longevity and fecundity, heat shock tolerance, and resistance to fungal pathogens and primary hymenopterous wasp parasitoids.

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“…Several other aphid endosymbionts, including Candidatus Regiella insecticola , have been reported to protect against the distantly related aphid specialist Pandora neoaphidis ( 35 ). However, to our knowledge, no studies have shown pea aphid-associated heritable endosymbionts protecting against generalist entomopathogens, within Entomophthorales or Ascomycota ( 36 , 37 ). Although Ca .…”

Section: Discussionmentioning

confidence: 97%

Intracellular defensive symbiont is culturable and capable of transovarial, vertical transmission

Maeda,

Kelly,

Sundar

et al. 2024

mBio

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Insects frequently form heritable associations with beneficial bacteria that are vertically transmitted from parent to offspring. Long-term vertical transmission has repeatedly resulted in genome reduction and gene loss, rendering many such bacteria incapable of establishment in axenic culture. Among aphids, heritable endosymbionts often provide context-specific benefits to their hosts. Although these associations have large impacts on host phenotypes, experimental approaches are often limited by an inability to cultivate these microbes. Here, we report the axenic culture of Candidatus Fukatsuia symbiotica strain WIR, a heritable bacterial endosymbiont of the pea aphid, Acyrthosiphon pisum . Whole-genome sequencing revealed similar genomic features and high sequence similarity to previously described strains, suggesting that the cultivation techniques used here may be applicable to Ca . F. symbiotica strains from distantly related aphids. Microinjection of cultured Ca . F. symbiotica into uninfected aphids revealed that it can reinfect developing embryos and that infections are maintained in subsequent generations via transovarial maternal transmission. Artificially infected aphids exhibit phenotypic and life history traits similar to those observed for native infections. Our results show that Ca . F. symbiotica may be a useful tool for experimentally probing the molecular mechanisms underlying host-symbiont interactions in a heritable symbiosis. IMPORTANCE Diverse eukaryotic organisms form stable, symbiotic relationships with bacteria that provide benefits to their hosts. While these associations are often biologically important, they can be difficult to probe experimentally because intimately host-associated bacteria are difficult to access within host tissues, and most cannot be cultured. This is especially true for the intracellular, maternally inherited bacteria associated with many insects, including aphids. Here, we demonstrate that a pea aphid-associated strain of the heritable endosymbiont, Candidatus Fukatsuia symbiotica, can be grown outside of its host using standard microbiology techniques and can readily re-establish infection that is maintained across host generations. These artificial infections recapitulate the effects of native infections, making this host-symbiont pair a useful experimental system.

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Aphid facultative symbionts confer no protection against the fungal entomopathogen Batkoa apiculata

Cited by 7 publications

References 31 publications

Pathogen-microbiome interactions and the virulence of an entomopathogenic fungus

Pathogen-microbiome interactions and the virulence of an entomopathogenic fungus

Aphid adaptation in a changing environment through their bacterial endosymbionts: an overview, including a new major cereal pest (Rhopalosiphum maidis (Fitch) scenario

Intracellular defensive symbiont is culturable and capable of transovarial, vertical transmission

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