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Infective larvae of Anisakis simplex (Nematoda) accumulate trehalose and glycogen in response to starvation and temperature stress.

ABSTRACT: Anisakis simplex L3 larvae infect fish and other seafood species such as squid or octopi; therefore, humans consuming raw or undercooked fish may become accidental hosts for this parasite. These larvae are induced to enter hypometabolism by cold temperatures. It is assumed that sugars (in particular trehalose and glycogen) are instrumental for survival under environmental stress conditions. To elucidate the mechanisms of environmental stress response in A. simplex, we observed the effects of starvation and temperature on trehalose and glycogen content, the activity of enzymes metabolizing those sugars, and the relative expression of genes of trehalose and glycogen metabolic pathways. The L3 of A. simplex synthesize trehalose both in low (0°C) and high temperatures (45°C). The highest content of glycogen was observed at 45°C at 36?h of incubation. On the second day of incubation, tissue content of trehalose depended on the activity of the enzymes: TPS was more active at 45°C, and TPP was more active at 0°C. The changes in TPP activity were consistent with the transcript level changes of the TPP gene, and the trehalose level, while glycogen synthesis correlates with the expression of glycogen synthase gene at 45°C; this suggests that the synthesis of trehalose is more essential. These results show that trehalose plays a key role in providing energy during the thermotolerance and starvation processes through the molecular and biochemical regulation of trehalose and glycogen metabolism.

SUBMITTER: Lopienska-Biernat E

PROVIDER: S-EPMC6451339 | biostudies-literature | 2019 Mar

REPOSITORIES: biostudies-literature

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Infective larvae of Anisakis simplex (Nematoda) accumulate trehalose and glycogen in response to starvation and temperature stress.

Łopieńska-Biernat Elżbieta E Stryiński Robert R Dmitryjuk Małgorzata M Wasilewska Barbara B

Biology open 20190321 3

Anisakis simplex L3 larvae infect fish and other seafood species such as squid or octopi; therefore, humans consuming raw or undercooked fish may become accidental hosts for this parasite. These larvae are induced to enter hypometabolism by cold temperatures. It is assumed that sugars (in particular trehalose and glycogen) are instrumental for survival under environmental stress conditions. To elucidate the mechanisms of environmental stress response in A. simplex, we observed the ...[more]

PMID: 30824422

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Project description:BackgroundAnisakis simplex sensu stricto and Anisakis pegreffii are sibling species of nematodes parasitic on marine mammals. Zoonotic human infection with third stage infective larvae causes anisakiasis, a debilitating and potentially fatal disease. These 2 species show evidence of hybridisation in geographical areas where they are sympatric. How the species and their hybrids differ is still poorly understood.ResultsThird stage larvae of Anisakis simplex s.s., Anisakis pegreffii and hybrids were sampled from Merluccius merluccius (Teleosti) hosts captured in waters of the FAO 27 geographical area. Specimens of each species and hybrids were distinguished with a diagnostic genetic marker (ITS). RNA was extracted from pools of 10 individuals of each taxon. Transcriptomes were generated using Illumina RNA-Seq, and assembled de novo. A joint assembly (here called merged transcriptome) of all 3 samples was also generated. The inferred transcript sets were functionally annotated and compared globally and also on subsets of secreted proteins and putative allergen families. While intermediary metabolism appeared to be typical for nematodes in the 3 evaluated taxa, their transcriptomes present strong levels of differential expression and enrichment, mainly of transcripts related to metabolic pathways and gene ontologies associated to energy metabolism and other pathways, with significant presence of excreted/secreted proteins, most of them allergens. The allergome of the 2 species and their hybrids has also been thoroughly studied; at least 74 different allergen families were identified in the transcriptomes.ConclusionsA. simplex s.s., A. pegreffi and their hybrids differ in gene expression patterns in the L3 stage. Strong parent-of-origin effects were observed: A. pegreffi alleles dominate in the expression patterns of hybrids albeit the latter, and A. pegreffii also display significant differences indicating that hybrids are intermediate biological entities among their parental species, and thus of outstanding interest in the study of speciation in nematodes. Analyses of differential expression based on genes coding for secreted proteins suggests that co-infections presents different repertoires of released protein to the host environment. Both species and their hybrids, share more allergen genes than previously thought and are likely to induce overlapping disease responses.

Project description:Anisakis pegreffii is known as one of the causes of a fish-borne zoonosis, anisakidosis. Despite its significant public health and food hygiene impacts, little is known of the pathogenesis, genetic background of this parasite, at least partly due to the lack of genome and transcriptome information. In this study, RNA-seq and de novo assembly were conducted to obtain transcriptome profiles of the A. pegreffii third and fourth larvae. The third stage larvae (APL3) were collected from chub mackerel and the fourth stage larvae (APL4) were obtained by in vitro culture. In total, 47,243 and 43,660 unigenes were expressed in APL3 and APL4 transcriptomes. Of them, 18,753 were known and 28,490 were novel for APL3, while 18,996 were known and 24,664 were novel for APL4. The most abundantly expressed genes in APL3 were mitochondrial enzymes (COI, COII, COIII) and polyubiquitins (UBB, UBIQP_XENLA). Collagen-related genes (col-145, col-34, col-138, Bm1_54705, col-40) were the most abundantly expressed in APL4. Mitochondrial enzyme genes (COIII, COI) were also highly expressed in APL4. Among the transcripts, 614 were up-regulated in APL3, while 1,309 were up-regulated in APL4. Several protease and protein biosynthesis-related genes were highly expressed in APL3, all of which are thought to be crucial for invading host tissues. Collagen synthesis-related genes were highly expressed in APL4, reflecting active biosynthesis of collagens occurs during moulting process of APL4. Of these differentially expressed genes, several genes (SI, nas-13, EF-TSMT, SFXN2, dhs-27) were validated to highly transcribed in APL3, while other genes (col-40, F09E10.7, pept-1, col-34, VIT) in APL4. The biological roles of these genes in vivo will be deciphered when the reference genome sequences are available, together with in vitro experiments.Anisakis pegreffii is known as one of the causes of a fish-borne zoonosis, anisakidosis. Despite its significant public health and food hygiene impacts, little is known of the pathogenesis, genetic background of this parasite, at least partly due to the lack of genome and transcriptome information. In this study, RNA-seq and de novo assembly were conducted to obtain transcriptome profiles of the A. pegreffii third and fourth larvae. The third stage larvae (APL3) were collected from chub mackerel and the fourth stage larvae (APL4) were obtained by in vitro culture. In total, 47,243 and 43,660 unigenes were expressed in APL3 and APL4 transcriptomes. Of them, 18,753 were known and 28,490 were novel for APL3, while 18,996 were known and 24,664 were novel for APL4. The most abundantly expressed genes in APL3 were mitochondrial enzymes (COI, COII, COIII) and polyubiquitins (UBB, UBIQP_XENLA). Collagen-related genes (col-145, col-34, col-138, Bm1_54705, col-40) were the most abundantly expressed in APL4. Mitochondrial enzyme genes (COIII, COI) were also highly expressed in APL4. Among the transcripts, 614 were up-regulated in APL3, while 1,309 were up-regulated in APL4. Several protease and protein biosynthesis-related genes were highly expressed in APL3, all of which are thought to be crucial for invading host tissues. Collagen synthesis-related genes were highly expressed in APL4, reflecting active biosynthesis of collagens occurs during moulting process of APL4. Of these differentially expressed genes, several genes (SI, nas-13, EF-TSMT, SFXN2, dhs-27) were validated to highly transcribed in APL3, while other genes (col-40, F09E10.7, pept-1, col-34, VIT) in APL4. The biological roles of these genes in vivo will be deciphered when the reference genome sequences are available, together with in vitro experiments.

Dataset Information

Infective larvae of Anisakis simplex (Nematoda) accumulate trehalose and glycogen in response to starvation and temperature stress.

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Infective larvae of <i>Anisakis simplex</i> (Nematoda) accumulate trehalose and glycogen in response to starvation and temperature stress.

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