The Endosymbiont Wolbachia pipientis Induces the Expression of Host Antioxidant Proteins in an Aedes albopictus Cell Line

Brennan, Lesley; Keddie, B. A.; Braig, Henk R.; Harris, Harriet L.

doi:10.1371/journal.pone.0002083

Cited by 139 publications

(127 citation statements)

References 78 publications

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“…We note that in plantmicroorganism interactions, oxidative stress commonly occurs, for example, in rhizobial symbiosis (56) and also in phytopathogenic infections (35). More generally, it could be a common and fundamental mechanism occurring widely in many prokaryote-eukaryote interactions, as it has been described recently in the Aedes albopictus-Wolbachia symbiosis (11).…”

Section: Discussionmentioning

confidence: 67%

Differential Effects of Rare Specific Flavonoids on Compatible and Incompatible Strains in the Myrica gale - Frankia Actinorhizal Symbiosis

Popovici

Comte

Bagnarol

et al. 2010

Appl Environ Microbiol

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Plant secondary metabolites, and specifically phenolics, play important roles when plants interact with their environment and can act as weapons or positive signals during biotic interactions. One such interaction, the establishment of mutualistic nitrogen-fixing symbioses, typically involves phenolic-based recognition mechanisms between host plants and bacterial symbionts during the early stages of interaction. While these mechanisms are well studied in the rhizobia-legume symbiosis, little is known about the role of plant phenolics in the symbiosis between actinorhizal plants and Frankia genus strains. In this study, the responsiveness of Frankia strains to plant phenolics was correlated with their symbiotic compatibility. We used Myrica gale, a host species with narrow symbiont specificity, and a set of compatible and noncompatible Frankia strains. M. gale fruit exudate phenolics were extracted, and 8 dominant molecules were purified and identified as flavonoids by high-resolution spectroscopic techniques. Total fruit exudates, along with two purified dihydrochalcone molecules, induced modifications of bacterial growth and nitrogen fixation according to the symbiotic specificity of strains, enhancing compatible strains and inhibiting incompatible ones. Candidate genes involved in these effects were identified by a global transcriptomic approach using ACN14a strain whole-genome microarrays. Fruit exudates induced differential expression of 22 genes involved mostly in oxidative stress response and drug resistance, along with the overexpression of a whiB transcriptional regulator. This work provides evidence for the involvement of plant secondary metabolites in determining symbiotic specificity and expands our understanding of the mechanisms, leading to the establishment of actinorhizal symbioses.Over the course of evolution, plants have developed many strategies to adapt to their environment and manage their biotic interactions. The production of secondary metabolites is an important tool in many of these strategies. In particular, secondary metabolites are involved in plant-microbe interactions both as weapons in plant defense mechanisms and as early signals in mutualistic as well as pathogenic relationships (22). For example, sesquiterpenes and flavonoids are involved in the early steps of arbuscular mycorrhizal symbiosis (1, 62). Similarly, in the early stages of the rhizobia-legume symbiosis, recognition of host flavonoids enhances rhizospheric competitiveness and root colonization and is the basic mechanism through which rhizobia induce the transcription of nod genes, leading to root hair deformation and nodulation in the plant tissues (13,49,55).Actinorhizal symbiosis is a less well-known nitrogen-fixing interaction, resulting from the association between the actinobacterium Frankia and plants belonging to eight dicotyledonous families collectively called "actinorhizal": Betulaceae, Myricaceae, Rosaceae, Datiscaceae, Elaeagnaceae, Coriariaceae, Casuarinaceae, and Rhamnaceae (8). Due to the nitrogen-fixing...

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Section: Discussionmentioning

confidence: 67%

Differential Effects of Rare Specific Flavonoids on Compatible and Incompatible Strains in the Myrica gale - Frankia Actinorhizal Symbiosis

Popovici

Comte

Bagnarol

et al. 2010

Appl Environ Microbiol

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“…The maternally transmitted intracellular bacteria Wolbachia pipientis, which can reach a high prevalence in host populations as a result of reproductive manipulations-even when they are physiologically costly- [57], are interesting model systems to understand the maintenance of symbiosis through the evolution of tolerance mechanisms. In cultured cells from the mosquito Aedes albopictus, the infection by Wolbachia is associated with a higher level of ROS (H 2 O 2 ) and the synthesis of anti-oxidant proteins [58]. The artificial infection of Wolbachia in Ae.…”

Section: (C) Evolution Of Tolerance In Wolbachia-insect Symbiosesmentioning

confidence: 99%

The oxidative environment: a mediator of interspecies communication that drives symbiosis evolution

2014

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Symbiotic interactions are ubiquitous in nature and play a major role in driving the evolution of life. Interactions between partners are often mediated by shared signalling pathways, which strongly influence both partners' biology and the evolution of the association in various environments. As an example of 'common language', the regulation of the oxidative environment plays an important role in driving the evolution of symbiotic associations. Such processes have been occurring for billions of years, including the increase in Earth's atmospheric oxygen and the subsequent evolution of mitochondria. The effect of reactive oxygen species and reactive nitrogen species (RONS) has been characterized functionally, but the molecular dialogue between partners has not been integrated within a broader evolutionary context yet. Given the pleiotropic role of RONS in cell-cell communication, development and immunity, but also their associated physiological costs, we discuss here how their regulation can influence the establishment, the maintenance and the breakdown of various symbiotic associations. By synthesizing recent developments in redox biology, we aim to provide an interdisciplinary understanding of the influence of such mediators of interspecies communication on the evolution and stability of symbioses, which in turn can shape ecosystems and play a role in health and disease.

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“…Recent studies on diverse insect-microbe symbiotic associations have revealed that the host organisms regulate infection densities of their symbionts by means of phagocytosis, antimicrobial peptides, lysozymes, reactive oxygen species, etc. (39)(40)(41)(42). These innate immune mechanisms may also comprise host-related stress factors for the symbionts.…”

Section: Host Fitness Is Negatively Affected By Infection With Symbiontmentioning

confidence: 99%

Polyester synthesis genes associated with stress resistance are involved in an insect–bacterium symbiosis

Kim

Won

Nikoh

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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Significance This study reports a previously unrecognized involvement of polyhydroxyalkanoate (PHA), known as a bacterial endocellular storage polymer, in an insect–bacterium symbiosis. Many bacteria in the environment accumulate PHA granules within their cells, which provide resistance to nutritional depletion and other environmental stresses. Here we demonstrate that synthesis and accumulation of PHA in the symbiont cells are required for normal symbiotic association with, and, consequently, positive fitness effects for the host insect. The requirement of PHA for symbiosis suggests that, contrary to the general expectation, the within-host environment may be, at least in some aspects, stressful for the symbiotic bacteria.

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The Endosymbiont Wolbachia pipientis Induces the Expression of Host Antioxidant Proteins in an Aedes albopictus Cell Line

Cited by 139 publications

References 78 publications

Differential Effects of Rare Specific Flavonoids on Compatible and Incompatible Strains in the Myrica gale - Frankia Actinorhizal Symbiosis

Differential Effects of Rare Specific Flavonoids on Compatible and Incompatible Strains in the Myrica gale - Frankia Actinorhizal Symbiosis

The oxidative environment: a mediator of interspecies communication that drives symbiosis evolution

Polyester synthesis genes associated with stress resistance are involved in an insect–bacterium symbiosis

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