Genta FA, Dillon RJ, Terra WR, Ferreira C.. Potential role for gut microbiota in cell wall digestion and glucoside detoxification in Tenebrio molitor larvae. J Insect Physiol 52: 593-601

Departamento de Bioquímica, Instituto de Química, Universidade de São Paulo, C.P. 26077, São Paulo, SP 05513-970, Brazil.
Journal of Insect Physiology (Impact Factor: 2.47). 07/2006; 52(6):593-601. DOI: 10.1016/j.jinsphys.2006.02.007
Source: PubMed


Tenebrio molitor larvae were successfully reared free of cultivatable gut lumen bacteria, yeasts and fungi using two approaches; aseptic rearing from surface sterilized eggs and by feeding larvae with antibiotic-containing food. Insects were reared on a rich-nutrient complete diet or a nutrient-poor refractory diet. A comparison of digestive enzyme activities in germ free and conventional insects containing a gut microbiota did not reveal gross differences in enzymes that degrade cell walls from bacteria (lysozyme), fungi (chitinase and laminarinase) and plants (cellulase and licheninase). This suggested that microbial-derived enzymes are not an essential component of the digestive process in this insect. However, more detailed analysis of T. molitor midgut proteins using an electrophoretic separation approach showed that some digestive enzymes were absent and others were newly expressed in microbiota-free larvae. Larvae reared in antibiotic-containing refractory wheat bran diet performed poorly in comparison with controls. The addition of saligenin, the aglycone of the plant glucoside salicin, has more deleterious effects on microbiota-free larvae than on the conventionally reared larvae, suggesting a detoxifying role of midgut microbiota. Analysis of the volatile organic compounds released from the faecal pellets of the larvae shows key differences in the profiles from conventionally reared and aseptically reared larvae. Pentadecene is a semiochemical commonly found in other beetle species. Here we demonstrate the absence of pentadecene from aseptically reared larvae in contrast to its presence in conventionally reared larvae. The results are discussed in the light of the hypothesis that microbial products play subtle roles in the life of the insect, they are involved in the digestion of refractory food, detoxification of secondary plant compounds and modify the volatile profiles of the insect host.

Download full-text


Available from: Fernando Genta
  • Source
    • "Usually high activity of laminarinase in insects feeding on fungi is observed. Microorganisms which possess licheninase and laminarinase, occurring in the midgut, serve rather in the detoxification processes of plant toxic aglycones than in food digestion (Scrivener et al. 1997, Azevedo et al 2003, Terra and Ferreira 2005, Genta et al. 2006). The glycosidases in the midgut of D. virgifera imago hydrolyzing a-and b-glucosidic, a-and b-galactosidic bonds showed maximum activities in acidic pH. "
    [Show abstract] [Hide abstract]
    ABSTRACT: The western corn rootworm, Diabrotica virgifera virgifera LeConte (Coleoptera: Chrysomelidae) is an important pest of maize. The diet of the D. virgifera imago is rich in starch and other polysaccharides present in cereals such as maize. Therefore, knowledge about enzymes involved in digestion of such specific food of this pest seems to be important. The paper shows, for the first time, the activities of main glycolytic enzymes in the midgut of D. virgifera imago: endoglycosidases (a-amylase, cellulase, chitinase, licheninase, laminarinase); exoglycosidases (a- and b-glucosidases, a- and b-galactosidases) and disaccharidases (maltase, isomaltase, sucrase, trehalase, lactase, and cellobiase). Activities of a-amylase, a-glucosidase, and maltase were the highest among assayed endoglycosidases, exoglycosidases, and disaccharidases, respectively. This indicates that in the midgut of D. virgifera imago a-amylase, a-glucosidase and maltase are important enzymes in starch hydrolysis and products of its digestion. These results lead to conclusion that inhibition of most active glycolytic enzymes of D. virgifera imago may be another promising method for chemical control of this pest of maize.
    Full-text · Article · May 2015 · Journal of Insect Science
  • Source
    • "These compounds often accumulate in the heartwood of the plant [109]. While many insects endogenously produce impressive arrays of detoxification enzymes or have mechanisms to sequester plant toxins, many beetle species directly benefit from detoxification enzymes produced by microbes [110,111]. For example, microbial communities associated with bark beetles feeding in phloem tissue, which serves as a conduit for toxic defensive chemicals, are highly enriched for detoxification genes [112]. "
    [Show abstract] [Hide abstract]
    ABSTRACT: The Asian longhorned beetle (Anoplophoraglabripennis) is an invasive, wood-boring pest that thrives in the heartwood of deciduous tree species. A large impediment faced by A. glabripennis as it feeds on woody tissue is lignin, a highly recalcitrant biopolymer that reduces access to sugars and other nutrients locked in cellulose and hemicellulose. We previously demonstrated that lignin, cellulose, and hemicellulose are actively deconstructed in the beetle gut and that the gut harbors an assemblage of microbes hypothesized to make significant contributions to these processes. While lignin degrading mechanisms have been well characterized in pure cultures of white rot basidiomycetes, little is known about such processes in microbial communities associated with wood-feeding insects. The goals of this study were to develop a taxonomic and functional profile of a gut community derived from an invasive population of larval A. glabripennis collected from infested host trees and to identify genes that could be relevant for the digestion of woody tissue and nutrient acquisition. To accomplish this goal, we taxonomically and functionally characterized the A. glabripennis midgut microbiota through amplicon and shotgun metagenome sequencing and conducted a large-scale comparison with the metagenomes from a variety of other herbivore-associated communities. This analysis distinguished the A. glabripennis larval gut metagenome from the gut communities of other herbivores, including previously sequenced termite hindgut metagenomes. Genes encoding enzymes were identified in the A. glabripennis gut metagenome that could have key roles in woody tissue digestion including candidate lignin degrading genes (laccases, dye-decolorizing peroxidases, novel peroxidases and β-etherases), 36 families of glycoside hydrolases (such as cellulases and xylanases), and genes that could facilitate nutrient recovery, essential nutrient synthesis, and detoxification. This community could serve as a reservoir of novel enzymes to enhance industrial cellulosic biofuels production or targets for novel control methods for this invasive and highly destructive insect.
    Full-text · Article · Sep 2013 · PLoS ONE
  • Source
    • "In the current study, the role of bacterial symbionts in growth and development of E. integriceps was investigated. It has long been established that bacteria associated with insects can be involved in food digestion, providing nutrition, detoxification, pheromone production, regulation of pH, synthesis of vitaminsand sterols, temperature tolerance, resistance against pathogens and parasitoids, and even modifying the use of host plants by phytophagous insects (Dillon and Dillon 2004; Genta et al. 2006; Feldhaar 2011; Ferrari and Vavre 2011), thereby affecting insect development, defense against natural enemies, immunity, reproduction, and speciation (Hurst and Werren 2001; Braendle et al. 2003; Dillon and Dillon 2004; Koropatnick et al. 2004; Backhed et al. 2005; Baumann 2005; Macdonald and Monteleone 2005). "
    [Show abstract] [Hide abstract]
    ABSTRACT: Abstract The Sunn pest, Eurygaster integriceps Puton (Hemiptera: Scutelleridae), is the most important pest of wheat and barley in wide areas of the world. Different aspects of the insect's life history have been studied, but to date nothing is known about their microbial symbionts. Here, the contribution of symbiotic bacteria to the fitness of the bug was investigated by combining two different approaches to manipulate the host's microbial community: the supplementation of antibiotics into the insects' diet and egg surface sterilization. First, bacteria cultured from gut homogenates were subjected to antibiotic screening tests using 20 different antibiotics. Norfloxacin was the most effective antibiotic, with the greatest inhibition zone among all antibiotics tested. Feeding norfloxacin to adult E. integriceps individuals significantly impaired growth and development of the offspring in a dose-dependent manner, i.e., higher antibiotic doses increased the negative effects on nymphal growth and development. Total developmental time from first nymphal instars to adult emergence in control animals was 30.1 days, but when adults had been offered diets with 10, 20, and 30 µg antibiotic per mg diet, the offspring's developmental time was prolonged to 32.8, 34.0, and 34.8 days, respectively. In the highest two doses of norfloxacin, all of the nymphs died before reaching the fifth nymphal instar. Similar results as for the antibiotic treatment were obtained when egg surface sterilization was used to manipulate the microbial community of E. integriceps. These results indicate that bacterial symbionts play a crucial role in the successful development of the host.
    Full-text · Article · Sep 2013 · Journal of Insect Science
Show more