Abstract

Cockroaches are insects that can accommodate diets of different composition, including lignocellulosic materials. Digestion of these compounds is achieved by the insect’s own enzymes and also by enzymes produced by gut symbionts. The presence of different and modular bacterial phyla on the cockroach gut tract suggests that this insect could be an interesting model to study the organization of gut bacterial communities associated with the digestion of different lignocellulosic diets. Thus, changes in the diversity of gut associated bacterial communities of insects exposed to such diets could give useful insights on how to improve hemicellulose and cellulose breakdown systems. In this work, through sequence analysis of 16S rRNA clone libraries, we compared the phylogenetic diversity and composition of gut associated bacteria in the cockroach Periplaneta americana collected in the wild-types or kept on two different diets: sugarcane bagasse and crystalline cellulose. These high fiber diets favor the predominance of some bacterial phyla, such as Firmicutes, when compared to wild-types cockroaches. Our data show a high bacterial diversity in P. americana gut, with communities composed mostly by the phyla Bacteroidetes, Firmicutes, Proteobacteria and Synergistetes. Our data show that the composition and diversity of gut bacterial communities could be modulated by diet composition. The increased presence of Firmicutes in sugarcane bagasse and crystalline cellulose-fed animals suggests that these bacteria are strongly involved in lignocellulose digestion in cockroach guts.BackgroundCockroaches are omnivorous animals that can incorporate in their diets food of different composition, including lignocellulosic materials. Digestion of these compounds is achieved by the insect’s own enzymes and also by enzymes produced by gut symbiont. However, the influence of diet with different fiber contents on gut bacterial communities and how this affects the digestion of cockroaches is still unclear. The presence of some bacterial phyla on gut tract suggests that cockroaches could be an interesting model to study the organization of gut bacterial communities during digestion of different lignocellulosic diets. Knowledge about the changes in diversity of gut associated bacterial communities of insects exposed to such diets could give interesting insights on how to improve hemicellulose and cellulose breakdown systems.Methodology/principal findingsWe compared the phylogenetic diversity and composition of gut associated bacteria in the cockroach P. americana caught on the wild or kept on two different diets: sugarcane bagasse and crystalline cellulose. For this purpose we constructed bacterial 16S rRNA gene libraries which showed that a diet rich in cellulose and sugarcane bagasse favors the predominance of some bacterial phyla, more remarkably Firmicutes, when compared to wild cockroaches. Rarefaction analysis, LIBSHUFF and UniFrac PCA comparisons showed that gene libraries of wild insects were the most diverse, followed by sugarcane bagasse fed and then cellulose fed animals. It is also noteworthy that cellulose and sugarcane bagasse gene libraries resemble each other.Conclusion/significanceOur data show a high bacterial diversity in P. americana gut, with communities composed mostly by the phyla Bacteroidetes, Firmicutes, Proteobacteria and Synergistetes. The composition and diversity of gut bacterial communities could be modulated by font of diet composition. The increased presence of Firmicutes in sugarcane bagasse and crystalline cellulose-fed animals suggests that these bacteria are strongly involved in lignocellulose digestion in cockroach guts.

Highlights

  • Lignocellulosic materials, such as sugarcane bagasse, have been considered promising materials in the biofuel industry for the synthesis of second generation ethanol

  • Most sequences from the sugarcane and cellulose fed libraries were represented by the Firmicutes and Bacteroidetes phyla, as observed in the microbiota of other animals submitted to high fiber content diets (Ley et al 2008)

  • In wild-types animals, BLAST searches performed with the bacterial sequences that could not be classified with the RDP tool retrieved only low similarity sequences suggesting that these microorganisms possibly represent new bacterial groups

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Summary

Introduction

Lignocellulosic materials, such as sugarcane bagasse, have been considered promising materials in the biofuel industry for the synthesis of second generation ethanol. The anatomical adaptations of the gut form specialized micro-environmental chambers with different pH levels and redox potential that promote an important increase in concentrations and functionality of the intestinal enzymes These chambers allow the effective breakdown of lignocellulosic biomass and a concomitant release of sugar monomers (Watanabe and Tokuda 2010). These microorganisms are absolutely essential to the digestion of many different animals, from insects to humans, and their diversity has been mainly studied by 16S rRNA sequence analysis. This approach has revealed the presence of several bacterial species that are mostly affiliated, but not restricted, to the phyla Firmicutes, Actinobacteria, Bacterioidetes, and Spirochetes (Hongo et al 2005; Gill et al 2006) that are strongly associated to the stage I of digestion

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