Comparative profiling of hepatopancreas transcriptomes in satiated and starving Pomacea canaliculata

Abstract

BackgroundAlthough Pomacea canaliculata is native to South and Central America, it has become one of the most abundant invasive species worldwide and causes extensive damage to agriculture and horticulture. Conventional physical and chemical techniques have been used to eliminate P. canaliculata, but the effects are not ideal. Therefore, it is important to devise a new method based on a greater understanding of the biology of P. canaliculata. However, the molecular mechanisms underlying digestion and absorption in P. canaliculata are not well understood due to the lack of available genomic information for this species, particularly for digestive enzyme genes.ResultsIn the present study, hepatopancreas transcriptome sequencing produced over 223 million high-quality reads, and a global de novo assembly generated a total of 87,766 unique transcripts (unigenes), of which 19,942 (22.7%) had significant similarities to proteins in the UniProt database. In addition, 296,675 annotated sequences were associated with Gene Ontology (GO) terms. A Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway enrichment was performed for the unique unigenes, and 262 pathways (p-value < 10−5) in P. canaliculata were found to be predominantly related to plant consumption and coarse fiber digestion and absorption. These transcripts were classified into four large categories: hydrolase, transferase, isomerase and cytochrome P450. The Reads Per Kilobase of transcript per Million mapped reads (RPKM) analysis showed that there were 523 down-regulated unigenes and 406 up-regulated unigenes in the starving apple snails compared with the satiated apple snails. Several important genes are associated with digestion and absorption in plants: endo-beta-1, 4-glucanase, xylanase, cellulase, cellulase EGX1, cellulase EGX3 and G-type lysozyme genes were identified. The qRT-PCR results confirmed that the expression patterns of these genes (except for the longipain gene) were consistent with the RNA-Seq results.ConclusionsOur results provide a more comprehensive understanding of the molecular genes associated with hepatopancreas functioning. Differentially expressed genes corresponding to critical metabolic pathways were detected in the transcriptome of starving apple snails compared with satiated apple snails. In addition to the cellulase gene, other genes were identified that may be important factors in plant matter metabolism in P. canaliculata, and this information has the potential to expedite the study of digestive physiology in apple snails.Electronic supplementary materialThe online version of this article (doi:10.1186/s12863-017-0485-7) contains supplementary material, which is available to authorized users.

Integrative Proteomic Analysis of Digestive Tract Glycosidases from the Invasive Golden Apple Snail, Pomacea canaliculata

“…canaliculata has revealed expanded cellulase gene families, which may give rise to increased gut enzyme versatility found in this study. It has also been shown that cellulose expression is influenced by the feeding state (i.e., satiated or starved) of apple snails . In addition, cellulases A0A2T7PPN6 (GHF9), A0A2T7NYY1 (GHF10), A0A2T7NZR0 (GHF10), and Pc89752 (GHF10) were uniquely found in the digestive contents indicating a possible origin in unicellular glands of the gut or in commensal symbiotic organisms .…”

“…Two different quantitative profiles were found in digestive gland: representatives from GHF2 (glucuronidases and mannosidases) and GHF3 (xylosidases) showed higher tissue values than contents while representatives from GHF5 (mannosidases), 10 (xylanases), and 16 (β-1,3-glucanases) families showed lower tissues values than contents. It is possible that the digestive gland expressed different hemicellulase isoforms which are associated with the ingested food types or the feeding state of the snails; however, future research will have to clarify this point. Mannosidases from GHF38 were detected in the salivary glands, but these peptides might be overestimated since this tissue showed about 7× less soluble proteins compared to other tissues and the samples were normalized by protein load prior to digestion and analysis.…”

Learning to starve: impacts of food limitation beyond the stress period

“…digestive and reproductive tissues). Few studies outside of Drosophila have utilized nextgeneration methods to measure gene expression throughout starvation (but see Khudyakov et al, 2015a,b;Yang et al, 2017). In whole-body studies on Drosophila, ∼25% of the genome had coding sequences with differential transcription during starvation (Harbison et al, 2005), underscoring the significant biological shifts necessary under food limitation.…”

Proteomic analysis of digestive tract peptidases and lipases from the invasive gastropod Pomacea canaliculata

“…It is possible that the higher structural and functional diversity of serine peptidases is influenced by the feeding state (satiated or starved) of apple snails and their ability to select among different macrophytes 24,69 . The feeding rate of macrophytes with higher nitrogen and phosphorus content positively influences eggs production and growth in P. canaliculata ; however, these parameters may decrease when snails consume plants with high phenolic content and/or physical and chemical defences 69 .…”

“…The diversity, origin, and characterization of digestive enzymes have been highlighted recently in invasive ampullariids because they are essential for the digestion of different food sources of macronutrients 7,16–22 . These enzymes include a set of genetically codified enzymes, as well as enzymes plausibly secreted by symbiotic bacteria 16,23,24 . Salivary and digestive glands of P. canaliculata are involved in the synthesis and secretion of glycosidases (i.e.…”