How the insect immune system interacts with an obligate symbiotic bacterium

Douglas, Angela E.; Bouvaine, Sophie; Russell, Robert B.

doi:10.1098/rspb.2010.1563

Cited by 55 publications

(49 citation statements)

References 40 publications

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“…In particular, questions concerning host tolerance to long-term symbiotic bacteria and the impacts of host-symbiont coevolution on the development and adaptation of the host immune system remained unanswered [9,11,13,31,32,33]. Remarkably, insects have selected a unique compartmentalization strategy that consists of secluding endosymbionts within the bacteriome.…”

Section: Discussionmentioning

confidence: 99%

Systemic Infection Generates a Local-Like Immune Response of the Bacteriome Organ in Insect Symbiosis

Masson¹,

Vallier²,

Vigneron³

et al. 2015

J Innate Immun

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Endosymbiosis is common in insects thriving in nutritionally unbalanced habitats. The cereal weevil, Sitophilus oryzae, houses Sodalis pierantonius, a Gram-negative intracellular symbiotic bacterium (endosymbiont), within a dedicated organ called a bacteriome. Recent data have shown that the bacteriome expresses certain immune genes that result in local symbiont tolerance and control. Here, we address the question of whether and how the bacteriome responds to insect infections involving exogenous bacteria. We have established an infection model by challenging weevil larvae with the Gram-negative bacterium Dickeya dadantii. We showed that D. dadantii infects host tissues and triggers a systemic immune response. Gene transcript analysis indicated that the bacteriome is also immune responsive, but it expresses immune effector genes to a lesser extent than the systemic and intestinal responses. Most genes putatively involved in immune pathways remain weakly expressed in the bacteriome following D. dadantii infection. Moreover, quantitative PCR experiments showed that the endosymbiont load is not affected by insect infection or the resulting bacteriome immune activation. Thus, the contained immune effector gene expression in the bacteriome may prevent potentially harmful effects of the immune response on endosymbionts, whilst efficiently protecting them from bacterial intruders.

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Section: Discussionmentioning

confidence: 99%

Systemic Infection Generates a Local-Like Immune Response of the Bacteriome Organ in Insect Symbiosis

Masson¹,

Vallier²,

Vigneron³

et al. 2015

J Innate Immun

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“…Buchnera growth is inferred to require 33 host-derived metabolites (11,16), and there is no reasonable prospect of culturing this bacterium. Despite this, viable and metabolically active Buchnera cells persist in defined medium for some hours (17)(18)(19), facilitating direct investigation of their metabolic capabilities. In this study, we probed the metabolic functions of isolated Buchnera preparations and obtained direct evidence that metabolic pathways are shared between host and symbiont.…”

Section: Discussionmentioning

confidence: 99%

Shared Metabolic Pathways in a Coevolved Insect-Bacterial Symbiosis

Russell

Bouvaine

Newell

et al. 2013

Appl Environ Microbiol

104

112

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The symbiotic bacterium Buchnera aphidicola lacks key genes in the biosynthesis of five essential amino acids (EAAs), and yet its animal hosts (aphids) depend on the symbiosis for the synthesis of these EAAs (isoleucine, leucine, methionine, phenylalanine, and valine). We tested the hypothesis, derived from genome annotation, that the missing Buchnera reactions are mediated by host enzymes, with the exchange of metabolic intermediates between the partners. The specialized host cells bearing Buchnera were separated into a Buchnera fraction and a Buchnera-free host cell fraction (HF). Addition of HF to isolated Buchnera preparations significantly increased the production of leucine and phenylalanine, and recombinant enzymes mediating the final reactions in branched-chain amino acid and phenylalanine synthesis rescued the production of these EAAs by Buchnera preparations without HF. The likely precursors for the missing proximal reactions in isoleucine and methionine synthesis were identified, and they differed from predictions based on genome annotations: synthesis of 2-oxobutanoate, the aphid-derived precursor of isoleucine synthesis, was stimulated by homoserine and not threonine via threonine dehydratase, and production of the homocysteine precursor of methionine was driven by cystathionine, not cysteine, via reversal of the transsulfuration pathway. The evolution of shared metabolic pathways in this symbiosis can be attributed to host compensation for genomic deterioration in the symbiont, involving changes in host gene expression networks to recruit specific enzymes to the host cell.

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“…The same has been observed during the later stages of development of Acyrthosiphon pisum (Hemiptera: Aphididae) [36] and Camponotus floridanus (Hymenoptera: Formicidae) [40], in which part of the symbiont population is destroyed due to the host nutritional demand. Adaptive changes in the regulation of the host immune response to control the density of obligate and facultative symbionts may also explain changes in symbiont density during host development [36,39,[66][67][68].…”

Section: Discussionmentioning

confidence: 99%

Population Dynamics and Growth Rates of Endosymbionts During Diaphorina citri (Hemiptera, Liviidae) Ontogeny

2014

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The infection density of symbionts is among the major parameters to understand their biological effects in host-endosymbionts interactions. Diaphorina citri harbors two bacteriome-associated bacterial endosymbionts (Candidatus Carsonella ruddii and Candidatus Profftella armatura), besides the intracellular reproductive parasite Wolbachia. In this study, the density dynamics of the three endosymbionts associated with the psyllid D. citri was investigated by real-time quantitative PCR (qPCR) at different developmental stages. Bacterial density was estimated by assessing the copy number of the 16S rRNA gene for Carsonella and Profftella, and of the ftsZ gene for Wolbachia. Analysis revealed a continuous growth of the symbionts during host development. Symbiont growth and rate curves were estimated by the Gompertz equation, which indicated a negative correlation between the degree of symbiont-host specialization and the time to achieve the maximum growth rate (t*). Carsonella densities were significantly lower than those of Profftella at all host developmental stages analyzed, even though they both displayed a similar trend. The growth rates of Wolbachia were similar to those of Carsonella, but Wolbachia was not as abundant. Adult males displayed higher symbiont densities than females. However, females showed a much more pronounced increase in symbiont density as they aged if compared to males, regardless of the incorporation of symbionts into female oocytes and egg laying. The increased density of endosymbionts in aged adults differs from the usual decrease observed during host aging in other insect-symbiont systems.

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How the insect immune system interacts with an obligate symbiotic bacterium

Cited by 55 publications

References 40 publications

Systemic Infection Generates a Local-Like Immune Response of the Bacteriome Organ in Insect Symbiosis

Systemic Infection Generates a Local-Like Immune Response of the Bacteriome Organ in Insect Symbiosis

Shared Metabolic Pathways in a Coevolved Insect-Bacterial Symbiosis

Population Dynamics and Growth Rates of Endosymbionts During Diaphorina citri (Hemiptera, Liviidae) Ontogeny

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