Molecular characterization of the lipophorin receptor in the crustacean ectoparasite Lepeophtheirus salmonis

Khan, Muhammad Tanveer; Dalvin, Sussie; Waheed, Qaiser; Nilsen, Frank; Male, Rune

doi:10.1371/journal.pone.0195783

Cited by 6 publications

(5 citation statements)

References 66 publications

(81 reference statements)

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“…4). Lipid metabolism is also down regulated after attachment presumably due to the change of nutrition from stored lipids [127] to ingested host tissues. Furthermore, several copies of a gene with Blast hit to the protein Timeless [128], known for regulating circadian rhythm in Drosophila , are among the down regulated transcripts.…”

Section: Resultsmentioning

confidence: 99%

The salmon louse genome: copepod features and parasitic adaptations

Skern‐Mauritzen

Malde

Eichner

et al. 2021

Preprint

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Arthropods comprise the most populous groups of animals and show an astonishing diversity. Aquatic arthropods belonging to the sub-class Copepoda encompass a range of ecological roles from endo- and ectoparasites to grazers of phytoplankton that link primary producers to higher trophic levels. Despite the important role of copepods in central ecosystem services and their impact as parasites, representative genomic data and genome assemblies are scarce. This limits our opportunities to understand both the specific biology of individual species and unifying copepod genomic features that may govern their capacities to, for example, adapt to a changing environment. Among the copepod parasites we find Lepeophtheirus salmonis, an important ectoparasite that represents a threat to wild salmonid stocks and causes large annual losses to the salmon farming industry. Here we present the salmon louse genome - the first genome of a parasitic copepod that is fully sequenced and annotated. The 695.4 Mbp assembly was validated by a genetic linkage map and comprises 13 autosomes that recombine almost exclusively in males, one autosome that is shielded from recombination in both sexes and a ZZ-ZW style sex chromosome system. The genome assembly contains approximate 60% repetitive regions and comprise 13081 annotated predicted protein-coding genes. The predicted gene set appears to be quite complete as 92.4% of the expected Arthropod genes were found by a BUSCO. The gene annotations were validated by transcriptome sequencing that corresponds to the expected function of selected tissues. Transcriptome sequencing further revealed a marked shift in the gene expression pattern at the transition from the planktonic dispersal phase to the parasitic lifestyle after host attachment. Among other features, genes related to circadian rhythm are downregulated upon attaching to a host - probably reflecting abandoning a planktonic life with diurnal migration. The genome shows several evolutionary signatures including a large expansion of FNII domains, commonly considered vertebrate specific, and an incomplete heme homeostasis pathway suggesting that heme proteins are obtained from the host. The salmon louse has repeatedly demonstrated a large capacity to develop resistance against chemical treatments. Nonetheless, it exhibits low reduced numbers of several genes commonly involved in detoxification; cytochrome P450, ATP-Binding Cassette type transporters and Glutathione S-transferases. Interestingly, only one gene family with a putative detoxification role was expanded: the major vault proteins. Finally, the salmon louse has lost the ability to sustain peroxisomes, a loss apparently shared in the Caligid family but not among copepods in general.

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Section: Resultsmentioning

confidence: 99%

The salmon louse genome: copepod features and parasitic adaptations

Skern‐Mauritzen

Malde

Eichner

et al. 2021

Preprint

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“…The expression analysis of different tissues of female louse suggests that LsLp1 and LsLp2 are synthesized by the sub-epidermal tissue and the intestine and involved in the recruitment of lipids to different lice tissues. Lipid staining results suggest a major transport of lipids in adult female lice to the ovaries and developing oocytes in the genital segment [ 53 , 54 ]. Therefore, it is speculated that lipids from intestine are taken up by apolipoproteins produced in intestine or sub-cuticular tissues, and transported to the ovaries and oocytes via the hemolymph.…”

Section: Discussionmentioning

confidence: 99%

“…Recent studies in L. salmonis have shown that maternal lipids supplied to the maturing eggs during vitellogenesis are essential for growth and development of larvae [ 53 ]. Presence of lipophorin receptor [ 54 ] in ovaries and eggs suggest internalization of lipoproteins mediated through endocytosis, but the transport of lipids to the growing oocytes is undescribed.…”

Section: Introductionmentioning

confidence: 99%

Two apolipoproteins in salmon louse (Lepeophtheirus salmonis), apolipoprotein 1 knock down reduces reproductive capacity

Khan

Dalvin

Nilsen

et al. 2021

Biochemistry and Biophysics Reports

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The salmon louse, Lepeophtheirus salmonis is an ectoparasite of salmonid fish in the Northern Hemisphere, causing large economical losses in the aquaculture industry and represent a threat to wild populations of salmonids. Like other oviparous animals, it is likely that female lice use lipoproteins for lipid transport to maturing oocytes and other organs of the body. As an important component of lipoproteins, apolipoproteins play a vital role in the transport of lipids through biosynthesis of lipoproteins. Apolipoproteins have been studied in detail in different organisms, but no studies have been done in salmon lice. Two apolipoprotein encoding genes ( LsLp1 and LsLp2 ) were identified in the salmon lice genome. Transcriptional analysis revealed both genes to be expressed at all stages from larvae to adult with some variation, LsLp1 generally higher than LsLp2 and both at their highest levels in adult stages of the louse. In adult female louse, the LsLp1 and LsLp2 transcripts were found in the sub-epidermal tissue and the intestine. RNA interference-mediated knockdown of LsLp1 and LsLp2 in female lice resulted in reduced expression of both transcripts. LsLp1 knockdown female lice produced significantly less offspring than control lice, while knockdown of LsLp2 in female lice caused no reduction in the number of offspring. These results suggest that LsLp1 has an important role in reproduction in female salmon lice.

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“…Other sequences relevant for cell development and reproduction were up-regulated in T. stylifera collected on May 23rd, such as me31b (ATP-Dependent RNA Helicase), Vldlr (Very Low-Density Lipoprotein Receptor) and Vasa (ATP-Dependent RNA Helicase Vasa). These genes are known to play key roles in germ cell formation [100,101] as well as in oocyte development and differentiation [102][103][104].…”

Section: Discussionmentioning

confidence: 99%

RNA-Seq and differential gene expression analysis in Temora stylifera copepod females with contrasting non-feeding nauplii survival rates: an environmental transcriptomics study

et al. 2020

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Background Copepods are fundamental components of pelagic food webs, but reports on how molecular responses link to reproductive success in natural populations are still scarce. We present a de novo transcriptome assembly and differential expression (DE) analysis in Temora stylifera females collected in the Gulf of Naples, Mediterranean Sea, where this copepod dominates the zooplankton community. High-Throughput RNA-Sequencing and DE analysis were performed from adult females collected on consecutive weeks (May 23rd and 30th 2017), because opposite naupliar survival rates were observed. We aimed at detecting key genes that may have influenced copepod reproductive potential in natural populations and whose expression was potentially affected by phytoplankton-derived oxylipins, lipoxygenase-derived products strongly impacting copepod naupliar survival. Results On the two sampling dates, temperature, salinity, pH and oxygen remained stable, while variations in phytoplankton cell concentration, oxylipin concentration and oxylipin-per-diatom-cell production were observed. T. stylifera naupliar survival was 25% on May 23rd and 93% on May 30th. De novo assembly generated 268,665 transcripts (isoforms) and 120,749 unique ‘Trinity predicted genes’ (unigenes), of which 50% were functionally annotated. Out of the 331 transcript isoforms differentially expressed between the two sampling dates, 119 sequences were functionally annotated (58 up- and 61 down-regulated). Among predicted genes (unigenes), 144 sequences were differentially expressed and 31 (6 up-regulated and 25 down-regulated) were functionally annotated. Most of the significantly down-regulated unigenes and isoforms were A5 Putative Odorant Binding Protein (Obp). Other differentially expressed sequences (isoforms and unigenes) related to developmental metabolic processes, protein ubiquitination, response to stress, oxidation-reduction reactions and hydrolase activities. DE analysis was validated through Real Time-quantitative PCR of 9 unigenes and 3 isoforms. Conclusions Differential expression of sequences involved in signal detection and transduction, cell differentiation and development offered a functional interpretation to the maternally-mediated low naupliar survival rates observed in samples collected on May 23rd. Down-regulation of A5 Obp along with higher quantities of oxylipins-per-litre and oxylipins-per-diatom-cell observed on May 23rd could suggest oxylipin-mediated impairment of naupliar survival in natural populations of T. stylifera. Our results may help identify biomarker genes explaining variations in copepod reproductive responses at a molecular level.

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Molecular characterization of the lipophorin receptor in the crustacean ectoparasite Lepeophtheirus salmonis

Cited by 6 publications

References 66 publications

The salmon louse genome: copepod features and parasitic adaptations

The salmon louse genome: copepod features and parasitic adaptations

Two apolipoproteins in salmon louse (Lepeophtheirus salmonis), apolipoprotein 1 knock down reduces reproductive capacity

RNA-Seq and differential gene expression analysis in Temora stylifera copepod females with contrasting non-feeding nauplii survival rates: an environmental transcriptomics study

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