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Immune system responses and fitness costs associated with consumption of bacteria in larvae of Trichoplusia ni.

Freitak D, Wheat CW, Heckel DG, Vogel H - BMC Biol. (2007)

Bottom Line: Trichoplusia ni larvae are able to detect and respond to environmental microbes encountered in the diet, possibly even using midgut epithelial tissue as a sensing organ.Potential benefits of this immune system priming may outweigh the observed tradeoffs, as priming based on environmentally sensed bacterial may decrease risk of serious infection.These results show that food plant microbial communities represent a dynamic and unstudied part of the coevolutionary interactions between plants and their insect herbivores.

View Article: PubMed Central - HTML - PubMed

Affiliation: Max Planck Institute for Chemical Ecology, Department of Entomology, Hans-Knoell - Strasse 8, 07745 Jena, Germany. dfreitak@ice.mpg.de

ABSTRACT

Background: Insects helped pioneer, and persist as model organisms for, the study of specific aspects of immunity. Although they lack an adaptive immune system, insects possess an innate immune system that recognizes and destroys intruding microorganisms. Its operation under natural conditions has not been well studied, as most studies have introduced microbes to laboratory-reared insects via artificial mechanical wounding. One of the most common routes of natural exposure and infection, however, is via food; thus, the role of dietary microbial communities in herbivorous insect immune system evolution invites study. Here, we examine the immune system response and consequences of exposing a lepidopteran agricultural pest to non-infectious microorganisms via simple oral consumption.

Results: Immune system response was compared between Trichoplusia ni larvae reared on diets with or without non-pathogenic bacteria (Escherichia coli and Micrococcus luteus). Two major immune response-related enzymatic activities responded to diets differently - phenoloxidase activity was inhibited in the bacteria-fed larvae, whereas general antibacterial activity was enhanced. Eight proteins were highly expressed in the hemolymph of the bacteria fed larvae, among them immune response related proteins arylphorin, apolipophorin III and gloverin. Expression response among 25 putative immune response-related genes were assayed via RT-qPCR. Seven showed more than fivefold up regulation in the presence of bacterial diet, with 22 in total being differentially expressed, among them apolipophorin III, cecropin, gallerimycin, gloverin, lysozyme, and phenoloxidase inhibiting enzyme. Finally, potential life-history trade-offs were studied, with pupation time and pupal mass being negatively affected in bacteria fed larvae.

Conclusion: The presence of bacteria in food, even if non-pathogenic, can trigger an immune response cascade with life history tradeoffs. Trichoplusia ni larvae are able to detect and respond to environmental microbes encountered in the diet, possibly even using midgut epithelial tissue as a sensing organ. Potential benefits of this immune system priming may outweigh the observed tradeoffs, as priming based on environmentally sensed bacterial may decrease risk of serious infection. These results show that food plant microbial communities represent a dynamic and unstudied part of the coevolutionary interactions between plants and their insect herbivores.

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Enzyme activities in the hemolymph of last instar T. ni larva, fed on bacteria-free (-BAC) and bacteria-supplemented diet (+BAC). (A) General antibacterial activity measured as the diameter of the lytic zone on agar plates and transformed into lysozyme equivalents (μg/ml). (B) Phenoloxidase activity (slope at Vmax) measured from hemolymph samples. Results represent mean values ± SE.
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Figure 1: Enzyme activities in the hemolymph of last instar T. ni larva, fed on bacteria-free (-BAC) and bacteria-supplemented diet (+BAC). (A) General antibacterial activity measured as the diameter of the lytic zone on agar plates and transformed into lysozyme equivalents (μg/ml). (B) Phenoloxidase activity (slope at Vmax) measured from hemolymph samples. Results represent mean values ± SE.

Mentions: Adding bacteria to the artificial diet lead to higher lysozyme activity in comparison to larvae grown on the diet without bacteria (Kruskall-Wallis ANOVA; H1,58 = 7.77; p = 0.003) (Figure 1A). Immune induction can generally lead to an increase of the titer of antibacterial proteins and peptides in the hemolymph. These are usually lytic enzymes (e.g. lysozyme) causing bacterial cell wall degradation, and small pore forming peptides leading to the lysis and leakage of the bacterial membranes. The antibacterial 'cocktail' measured by lytic zone assays may consist not only of different lysozymes but also of unknown lytic and antibacterial proteins.


Immune system responses and fitness costs associated with consumption of bacteria in larvae of Trichoplusia ni.

Freitak D, Wheat CW, Heckel DG, Vogel H - BMC Biol. (2007)

Enzyme activities in the hemolymph of last instar T. ni larva, fed on bacteria-free (-BAC) and bacteria-supplemented diet (+BAC). (A) General antibacterial activity measured as the diameter of the lytic zone on agar plates and transformed into lysozyme equivalents (μg/ml). (B) Phenoloxidase activity (slope at Vmax) measured from hemolymph samples. Results represent mean values ± SE.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2235825&req=5

Figure 1: Enzyme activities in the hemolymph of last instar T. ni larva, fed on bacteria-free (-BAC) and bacteria-supplemented diet (+BAC). (A) General antibacterial activity measured as the diameter of the lytic zone on agar plates and transformed into lysozyme equivalents (μg/ml). (B) Phenoloxidase activity (slope at Vmax) measured from hemolymph samples. Results represent mean values ± SE.
Mentions: Adding bacteria to the artificial diet lead to higher lysozyme activity in comparison to larvae grown on the diet without bacteria (Kruskall-Wallis ANOVA; H1,58 = 7.77; p = 0.003) (Figure 1A). Immune induction can generally lead to an increase of the titer of antibacterial proteins and peptides in the hemolymph. These are usually lytic enzymes (e.g. lysozyme) causing bacterial cell wall degradation, and small pore forming peptides leading to the lysis and leakage of the bacterial membranes. The antibacterial 'cocktail' measured by lytic zone assays may consist not only of different lysozymes but also of unknown lytic and antibacterial proteins.

Bottom Line: Trichoplusia ni larvae are able to detect and respond to environmental microbes encountered in the diet, possibly even using midgut epithelial tissue as a sensing organ.Potential benefits of this immune system priming may outweigh the observed tradeoffs, as priming based on environmentally sensed bacterial may decrease risk of serious infection.These results show that food plant microbial communities represent a dynamic and unstudied part of the coevolutionary interactions between plants and their insect herbivores.

View Article: PubMed Central - HTML - PubMed

Affiliation: Max Planck Institute for Chemical Ecology, Department of Entomology, Hans-Knoell - Strasse 8, 07745 Jena, Germany. dfreitak@ice.mpg.de

ABSTRACT

Background: Insects helped pioneer, and persist as model organisms for, the study of specific aspects of immunity. Although they lack an adaptive immune system, insects possess an innate immune system that recognizes and destroys intruding microorganisms. Its operation under natural conditions has not been well studied, as most studies have introduced microbes to laboratory-reared insects via artificial mechanical wounding. One of the most common routes of natural exposure and infection, however, is via food; thus, the role of dietary microbial communities in herbivorous insect immune system evolution invites study. Here, we examine the immune system response and consequences of exposing a lepidopteran agricultural pest to non-infectious microorganisms via simple oral consumption.

Results: Immune system response was compared between Trichoplusia ni larvae reared on diets with or without non-pathogenic bacteria (Escherichia coli and Micrococcus luteus). Two major immune response-related enzymatic activities responded to diets differently - phenoloxidase activity was inhibited in the bacteria-fed larvae, whereas general antibacterial activity was enhanced. Eight proteins were highly expressed in the hemolymph of the bacteria fed larvae, among them immune response related proteins arylphorin, apolipophorin III and gloverin. Expression response among 25 putative immune response-related genes were assayed via RT-qPCR. Seven showed more than fivefold up regulation in the presence of bacterial diet, with 22 in total being differentially expressed, among them apolipophorin III, cecropin, gallerimycin, gloverin, lysozyme, and phenoloxidase inhibiting enzyme. Finally, potential life-history trade-offs were studied, with pupation time and pupal mass being negatively affected in bacteria fed larvae.

Conclusion: The presence of bacteria in food, even if non-pathogenic, can trigger an immune response cascade with life history tradeoffs. Trichoplusia ni larvae are able to detect and respond to environmental microbes encountered in the diet, possibly even using midgut epithelial tissue as a sensing organ. Potential benefits of this immune system priming may outweigh the observed tradeoffs, as priming based on environmentally sensed bacterial may decrease risk of serious infection. These results show that food plant microbial communities represent a dynamic and unstudied part of the coevolutionary interactions between plants and their insect herbivores.

Show MeSH
Related in: MedlinePlus