Abstract
The cockroach, Periplaneta americana, is an obnoxious and notorious pest of the world, with a strong ability to adapt to a variety of complex environments. However, the molecular mechanism of this adaptability is mostly unknown. In this study, the genes and microbiota composition associated with the adaptation mechanism were studied by analyzing the transcriptome and 16S rDNA pyrosequencing of the P. americana midgut, respectively. Midgut transcriptome analysis identified 82,905 unigenes, among which 64 genes putatively involved in digestion (11 genes), detoxification (37 genes) and oxidative stress response (16 genes) were found. Evaluation of gene expression following treatment with cycloxaprid further revealed that the selected genes (CYP6J1, CYP4C1, CYP6K1, Delta GST, alpha-amylase, beta-glucosidase and aminopeptidase) were upregulated at least 2.0-fold at the transcriptional level, and four genes were upregulated more than 10.0-fold. An interesting finding was that three digestive enzymes positively responded to cycloxaprid application. Tissue expression profiles further showed that most of the selected genes were midgut-biased, with the exception of CYP6K1. The midgut microbiota composition was obtained via 16S rDNA pyrosequencing and was found to be mainly dominated by organisms from the Firmicutes phylum, among which Clostridiales, Lactobacillales and Burkholderiales were the main orders which might assist the host in the food digestion or detoxification of noxious compounds. The preponderant species, Clostridium cellulovorans, was previously reported to degrade lignocellulose efficiently in insects. The abundance of genes involved in digestion, detoxification and response to oxidative stress, and the diversity of microbiota in the midgut might provide P. americana high capacity to adapt to complex environments.
Highlights
The insect midgut plays critical roles in digestion and nutrient uptake as well as detoxification and oxidative stress responses
88,619,510 raw reads were generated from Illumina sequencing of a cDNA library from P. americana midguts
Three genes were more abundant than other digestive enzyme genes (Fig 2B). These results indicated that active digestive processes were underway in the P. americana midgut
Summary
The insect midgut plays critical roles in digestion and nutrient uptake as well as detoxification and oxidative stress responses. These roles are essential for environmental adaptation. The insect midgut is considered to be the centre of detoxification metabolism and stress response, which include three major interrelated pathways: oxidation-reduction, conjugation and hydrolysis [4, 5]. Glutathione Stransferases (GSTs) are important conjugation enzymes, participating in the detoxification of oxidized lipids and exogenous toxins as well as participating in intracellular transport and hormone synthesis [14, 15]. Detoxification is carried out via hydrolysis and plays an important role in the degradation of insecticides, such as carboxylesterases (CarEs) catalyzing the hydrolysis of pyrethroids and organophosphates [16]. Other proteins, including cadherins, heat shock proteins (Hsps) and ATP-binding cassette transporters (ABC transporters), are involved in detoxification metabolism or stress response [17, 18]
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