Biodiversity and Activity of the Gut Microbiota across the Life History of the Insect Herbivore Spodoptera littoralis

Abstract

Microbes that live inside insects play critical roles in host nutrition, physiology, and behavior. Although Lepidoptera (butterflies and moths) are one of the most diverse insect taxa, their microbial symbionts are little-studied, particularly during metamorphosis. Here, using ribosomal tag pyrosequencing of DNA and RNA, we investigated biodiversity and activity of gut microbiotas across the holometabolous life cycle of Spodoptera littoralis, a notorious agricultural pest worldwide. Proteobacteria and Firmicutes dominate but undergo a structural “metamorphosis” in tandem with its host. Enterococcus, Pantoea and Citrobacter were abundant and active in early-instar, while Clostridia increased in late-instar. Interestingly, only enterococci persisted through metamorphosis. Female adults harbored high proportions of Enterococcus, Klebsiella and Pantoea, whereas males largely shifted to Klebsiella. Comparative functional analysis with PICRUSt indicated that early-instar larval microbiome was more enriched for genes involved in cell motility and carbohydrate metabolism, whereas in late-instar amino acid, cofactor and vitamin metabolism increased. Genes involved in energy and nucleotide metabolism were abundant in pupae. Female adult microbiome was enriched for genes relevant to energy metabolism, while an increase in the replication and repair pathway was observed in male. Understanding the metabolic activity of these herbivore-associated microbial symbionts may assist the development of novel pest-management strategies.

The microbiome of theMelitaea cinxiabutterfly shows marked variation but is only little explained by the traits of the butterfly or its host plant

“…In adult H . erato , males and females share similar microbial communities (Hammer et al ., ), whereas in Spodoptera littoralis the sexes harbour divergent bacterial communities, with higher Enterobacteriaceae proportion found in females (Chen et al ., ). It is noteworthy that even when found, the consequences of sex‐dimorphic microbiota in Lepidoptera are not well understood.…”

Ambient temperature‐mediated enzymic activities and intestinal microflora in Lymantria dispar larvae

“…Traditional cultivation‐dependent technique for microorganism research was limited by numerous microorganisms that cannot be cultured now, and cannot reflect the alteration of microbiota community. However, the advent of amplicon sequencing offered us an insight of the entire community structure and those uncultured microorganisms (B. Chen et al, ; Cheung et al, ; Shao et al, ). More and more nonegligible roles of intestinal microflora were revealed by sequencing technology.…”

“…The previous study suggested that intestinal microflora was involved in human's physical and mental health (Petersen, Skov, Thyssen, & Jensen, ; Stricoff & Robinson, ). Similarly, intestinal microflora plays diverse functions in invertebrate, such as olfactory behavior regulation (Qiao, Keesey, Hansson, & Knaden, ), metabolism (Ayayee, Muñoz‐Garcia, & Keeney, ; B. Chen et al, ), and immune (Lee, Lee, & Lee, ; Martemyanov et al, ; Xia et al, ). In addition, consistent changes of gut microbial community and host development indicated that the gut microbiota might be involved in the entomic development (B. Chen et al, ).…”

The Hologenome Across Environments and the Implications of a Host-Associated Microbial Repertoire

“…Furthermore, exposure to an environmental stress during an early life stage may later shape the initial colonizers at a later life stages and corresponding repertoire of microbial associates (e.g., amphibians: Kohl et al, 2013; insects: Hroncova et al, 2015; Chen et al, 2016; cnidarians: Fraune et al, 2016). These stage-specific influences on the physiology and survival of subsequent stages are referred to as carryover or latent effects (Pechenik et al, 1998; Pechenik, 2006).…”