Integrating nutrition and immunology: A new frontier

Ponton, Fleur; Wilson, Kenneth; Holmes, Andrew; Cotter, Sheena C.; Raubenheimer, David; Simpson, Stephen J.

doi:10.1016/j.jinsphys.2012.10.011

Cited by 124 publications

(98 citation statements)

References 146 publications

(149 reference statements)

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“…These differences could be explained by the heterogeneous microbiota composition and differing degrees of host immunocompetence, which are influenced by various biotic and abiotic factors. Indeed, the capacity of insects to mount a costly defense reaction is affected by multiple factors, including nutritional status, developmental phase, co-occurrence of multiple pathogens and parasites, as well as by any other competing metabolic response to environmental stress agents (49,50).…”

Section: Discussionmentioning

confidence: 99%

Midgut microbiota and host immunocompetence underlie Bacillus thuringiensis killing mechanism

Caccia¹,

Lelio

Storia

et al. 2016

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

148

128

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Bacillus thuringiensis is a widely used bacterial entomopathogen producing insecticidal toxins, some of which are expressed in insect-resistant transgenic crops. Surprisingly, the killing mechanism of B. thuringiensis remains controversial. In particular, the importance of the septicemia induced by the host midgut microbiota is still debated as a result of the lack of experimental evidence obtained without drastic manipulation of the midgut and its content. Here this key issue is addressed by RNAi-mediated silencing of an immune gene in a lepidopteran host Spodoptera littoralis, leaving the midgut microbiota unaltered. The resulting cellular immunosuppression was characterized by a reduced nodulation response, which was associated with a significant enhancement of host larvae mortality triggered by B. thuringiensis and a Cry toxin. This was determined by an uncontrolled proliferation of midgut bacteria, after entering the body cavity through toxin-induced epithelial lesions. Consequently, the hemolymphatic microbiota dramatically changed upon treatment with Cry1Ca toxin, showing a remarkable predominance of Serratia and Clostridium species, which switched from asymptomatic gut symbionts to hemocoelic pathogens. These experimental results demonstrate the important contribution of host enteric flora in B. thuringiensis-killing activity and provide a sound foundation for developing new insect control strategies aimed at enhancing the impact of biocontrol agents by reducing the immunocompetence of the host.

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Section: Discussionmentioning

confidence: 99%

Midgut microbiota and host immunocompetence underlie Bacillus thuringiensis killing mechanism

Caccia¹,

Lelio

Storia

et al. 2016

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

148

128

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“…6) and mixed effects have been found in other insects (Ponton et al, 2013), including an increase in disease resistance to some pathogens (e.g. D. melanogaster, Ayres and Schneider, 2009; tent caterpillars Malacosoma pluviale californicum, Myers et al, 2011; crickets, Gryllus texensis, Kelly and Tawes, 2013; Galleria mellonella, Kangassalo et al, 2015).…”

Section: Effects On Disease Resistancementioning

confidence: 99%

Reconfiguration of the immune system network during food limitation in the caterpillar Manduca sexta

Adamo

Davies

Easy

et al. 2016

Journal of Experimental Biology

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Dwindling resources might be expected to induce a gradual decline in immune function. However, food limitation has complex and seemingly paradoxical effects on the immune system. Examining these changes from an immune system network perspective may help illuminate the purpose of these fluctuations. We found that food limitation lowered long-term (i.e. lipid) and short-term (i.e. sugars) energy stores in the caterpillar Manduca sexta. Food limitation also: altered immune gene expression, changed the activity of key immune enzymes, depressed the concentration of a major antioxidant (glutathione), reduced resistance to oxidative stress, reduced resistance to bacteria (Grampositive and -negative bacteria) but appeared to have less effect on resistance to a fungus. These results provide evidence that food limitation led to a restructuring of the immune system network. In severely food-limited caterpillars, some immune functions were enhanced. As resources dwindled within the caterpillar, the immune response shifted its emphasis away from inducible immune defenses (i.e. those responses that are activated during an immune challenge) and increased emphasis on constitutive defenses (i.e. immune components that are produced consistently). We also found changes suggesting that the activation threshold for some immune responses (e.g. phenoloxidase) was lowered. Changes in the configuration of the immune system network will lead to different immunological strengths and vulnerabilities for the organism.

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“…For example, desert locusts (Schistocerca gregaria) infected by a fungal pathogen were only able to produce viable offspring when they were permitted to thermoregulate to fever temperatures (Elliot et al, 2002). In addition to illustrating that behavioral alteration of the thermal context for metabolic processes can affect immunity (Anderson et al, 2013;Elliot et al, 2002;Inglis et al, 1996), ecological immunity research also highlights the importance of chemical and nutritional inputs to the system (Adamo et al, 2010;Ayres and Schneider, 2009;Cotter et al, 2011;Lee et al, 2006b;Lefèvre et al, 2010) [nutritional aspects are reviewed in Ponton et al (Ponton et al, 2013) and SivaJothy and Thompson (Siva-Jothy and Thompson, 2002)]. In a transgenerational example, monarch butterflies infected with a protozoan parasite adaptively select host plants that reduce infection in offspring (Lefèvre et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

Reduced consumption of protein-rich foods follows immune challenge in a polyphagous caterpillar

Mason

Smilanich

Singer

2014

Journal of Experimental Biology

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Advances in ecological immunity have illustrated that, like vertebrates, insects exhibit adaptive immunity, including induced changes in feeding behavior that aid the immune system. In particular, recent studies have pointed to the importance of protein intake in mounting an immune response. In this study, we tested the hypothesis that the polyphagous caterpillar Grammia incorrupta (H. Edwards) (Family: Erebidae) would adaptively change its feeding behavior in response to immune challenge, predicting that caterpillars would increase their intake of dietary protein. We further predicted that this response would enhance the melanization response, a component of the immune system that acts against parasitoids. We challenged the immune system using either tachinid fly parasitoids or a bead injection technique that has been used in studies to simulate parasitism, and measured feeding before and after immune challenge on diets varying in their macronutrient content. To evaluate the effects of diet on melanization, we quantified melanization of beads following feeding assays. Contrary to our prediction, we found that parasitized or injected caterpillars given a choice between high-and low-protein foods reduced their intake of the high-protein food. Furthermore, in a no-choice experiment, caterpillars offered food with a protein concentration that is optimal for growth reduced feeding following immune challenge, whereas those offered a low-protein food did not. Although variation in protein intake did not change the caterpillars' melanization response, increased carbohydrate intake did increase melanization, suggesting a prophylactic role for carbohydrates. We discuss alternative mechanisms by which variation in protein intake could negatively or positively affect parasitized caterpillars, including nutritional interactions with the caterpillar's self-medication response.

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Integrating nutrition and immunology: A new frontier

Cited by 124 publications

References 146 publications

Midgut microbiota and host immunocompetence underlie Bacillus thuringiensis killing mechanism

Midgut microbiota and host immunocompetence underlie Bacillus thuringiensis killing mechanism

Reconfiguration of the immune system network during food limitation in the caterpillar Manduca sexta

Reduced consumption of protein-rich foods follows immune challenge in a polyphagous caterpillar

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