Transcriptomic and Proteomic Analysis of Arion vulgaris—Proteins for Probably Successful Survival Strategies?

Bulat, Tanja; Šmidák, Roman; Sialana, Fernando J.; Jung, Gangsoo; Rattei, Thomas; Bilban, Martin; Sattmann, Helmut; Lübec, Gert; Aradská, Jana

doi:10.1371/journal.pone.0150614

Cited by 13 publications

(12 citation statements)

References 44 publications

(42 reference statements)

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“…These were the minor proteins Tri_111928/K1QJ54_CRAGI and Comp52297_c0_seq1_2/K1R3V2 (Additional file 4 : Table S2). Another 43 identified proteins were most similar in FASTA searches to various molluscs, the largest single fraction (22 minor proteins) originating from a combined transcriptomic and proteomic study of the shell-less terrestrial gastropod Arion vulgaris [ 136 ].…”

Section: Resultsmentioning

confidence: 99%

In-depth proteomic analyses of Haliotis laevigata (greenlip abalone) nacre and prismatic organic shell matrix

et al. 2018

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BackgroundThe shells of various Haliotis species have served as models of invertebrate biomineralization and physical shell properties for more than 20 years. A focus of this research has been the nacreous inner layer of the shell with its conspicuous arrangement of aragonite platelets, resembling in cross-section a brick-and-mortar wall. In comparison, the outer, less stable, calcitic prismatic layer has received much less attention. One of the first molluscan shell proteins to be characterized at the molecular level was Lustrin A, a component of the nacreous organic matrix of Haliotis rufescens. This was soon followed by the C-type lectin perlucin and the growth factor-binding perlustrin, both isolated from H. laevigata nacre, and the crystal growth-modulating AP7 and AP24, isolated from H. rufescens nacre. Mass spectrometry-based proteomics was subsequently applied to to Haliotis biomineralization research with the analysis of the H. asinina shell matrix and yielded 14 different shell-associated proteins. That study was the most comprehensive for a Haliotis species to date.MethodsThe shell proteomes of nacre and prismatic layer of the marine gastropod Haliotis laevigata were analyzed combining mass spectrometry-based proteomics and next generation sequencing.ResultsWe identified 297 proteins from the nacreous shell layer and 350 proteins from the prismatic shell layer from the green lip abalone H. laevigata. Considering the overlap between the two sets we identified a total of 448 proteins. Fifty-one nacre proteins and 43 prismatic layer proteins were defined as major proteins based on their abundance at more than 0.2% of the total. The remaining proteins occurred at low abundance and may not play any significant role in shell fabrication. The overlap of major proteins between the two shell layers was 17, amounting to a total of 77 major proteins.ConclusionsThe H. laevigata shell proteome shares moderate sequence similarity at the protein level with other gastropod, bivalve and more distantly related invertebrate biomineralising proteomes. Features conserved in H. laevigata and other molluscan shell proteomes include short repetitive sequences of low complexity predicted to lack intrinsic three-dimensional structure, and domains such as tyrosinase, chitin-binding, and carbonic anhydrase. This catalogue of H. laevigata shell proteins represents the most comprehensive for a haliotid and should support future efforts to elucidate the molecular mechanisms of shell assembly.Electronic supplementary materialThe online version of this article (10.1186/s12953-018-0139-3) contains supplementary material, which is available to authorized users.

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Section: Resultsmentioning

confidence: 99%

In-depth proteomic analyses of Haliotis laevigata (greenlip abalone) nacre and prismatic organic shell matrix

et al. 2018

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“…The results partially confirmed the findings of a tandem-repeat galectin from the freshwater snail, Biomphalaria glabrata, wherein 6 aa within each CRD was responsible for galactosyl-binding activity (Yoshino et al, 2008). Generally, tandem-repeat galectins of invertebrates contain 6-8 conserved aa that confers sugar-binding activity (Huang et al, 2007).The transcriptome of Spanish slug, Arion vulgaris identified unigenes with coding sequences for tandemrepeat galectins (Bulat et al, 2016). The I. fruhstorferi unigene sequence showing matches to galectin-6 (If_Gal6) was predicted to contain a coding sequence of 435 nucleotides encoding 144 aa.…”

Section: Resultsmentioning

confidence: 99%

“…Towards exploring the gene structure dynamics of lectin families and their related function as PRRs in innate immunity, we screened unigene sequences homologous to galectin-4 and galectin-6 in I. fruhstorferi. Earlier, transcriptome characterization of Spanish slug, Arion vulgaris identified ten unigenes coding in silico for tandem-repeat galectins (Bulat et al, 2016).To our knowledge, this study represents only the second investigation of galectins at the structural level in the slug species.…”

Section: Introductionmentioning

confidence: 86%

In silico characterization of single and tandem-repeat galectin from terrestrial slug, Incilaria fruhstorferi

Patnaik¹,

Hwang²,

Baliarsingh³

et al. 2019

JEB

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Galectins are β-galactoside binding proteins currently represented by 15 members (Galectin-1 through Galectin-15). The members are differentiated on the basis of the number of carbohydrate recognition domains (CRDs), the linker region connecting dual CRDs, and the conserved amino acid (aa) residues within CRDs. In this study, galactosyl-binding lectin family proteins were screened and characterized from transcriptome of terrestrial slug Incilaria fruhstorferi using bioinformatics analysis. I. fruhstorferi unigene sequences showing identity to galectins in the orthologous species were used for prediction of ORFs using FGENESH software. Subsequently, the ORFs were validated for conserved domain analysis using BLASTp and SMART programs. The multiple sequence alignments and percent identity/distance was elucidated using Clustal X2 and represented in GeneDoc sequence visualization program. The phylogenetic tree was inferred using MEGA7. A single-repeat and a tandem-repeat galectin (If_Gal6 and If_Gal4, respectively) were retrieved from the transcriptome profile of terrestrial slug, I. fruhstorferi. The predicted If_Gal4 and If_Gal6 comprised of 693 nucleotides translated to 230 aa residues and 435 nucleotides translated to 144 aa residues, respectively. If_Gal4 possessed two CRDs, each showing the highly conserved aa responsible for galactosyl-binding activity. Surprisingly, If_Gal6 is a single-CRD protein in contrast to the common tandemrepeat galectins illustrated for Gal6 in most other invertebrate and vertebrate species. At the level of aa sequence, If_Gal4 showed maximum of 54% identity and minimum distance of 0.459 with the sea snail, Haliotis discus Galectin-4 (Hd_Gal4). Cluster analysis showed higher similarities of If_Gal4 with selected molluscan Galectin-4 aa sequences. If_Gal6 showed 41% identity with the air-breathing freshwater snail, Biomphalaria glabrata Galectin-6 (Bg_Gal6) supposed to exist as dual-CRD molluscan galectin. Discovery and structural characterization of a single-CRD galectin from I. fruhstorferi is second in molluscs after the sequence was reported from the Pacific oyster, Crassostrea gigas. Carbohydrate-recognition domains, Galectin, Incilaria fruhstorferi, Phytogenetic analysis In silico characterization of single and tandemrepeat galectin from terrestrial slug, Incilaria fruhstorferi

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“…The C1q domain‐containing proteins are a family of proteins characterized by a globular C1q (gC1q) domain in their C‐terminus (Carland & Gerwick, ). They are involved with several processes in vertebrates and are associated with the innate immune system response in molluscs (Bulat et al, ; Castillo, Salazar, & Joffe, ; Gestal, Pallavicini, Venier, Novoa, & Figueras, ; Zhang et al, ). While their differential expression here could indicate stress‐induced immunosuppression due to lowered allocation of resources to immune function in response to predators, we observed no significant effects of predator kairomones in other genes associated with innate immunity.…”

Section: Discussionmentioning

confidence: 99%

Transcriptomic responses to predator kairomones in embryos of the aquatic snail Radix balthica

Tills

Truebano

Feldmeyer

et al. 2018

Ecology and Evolution

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The ability of organisms to respond to predation threat by exhibiting induced defenses is well documented, but studies on the potential mechanistic basis for such responses are scarce. Here, we examine the transcriptomic response to predator kairomones of two functionally distinct developmental stages in embryos of the aquatic snail Radix balthica: E8—the stage at which a range‐finding trial indicated that kairomone‐induced accelerated growth and development first occurred; and E9—the stage at which embryos switched from ciliary‐ to crawling‐driven locomotion. We tested whether expression profiles were influenced by kairomones and whether this influence varied between stages. We also identified potential candidate genes for investigating mechanisms underpinning induced responses. There were 6,741 differentially expressed transcripts between developmental stages, compared to just five in response to predator kairomones. However, on examination of functional enrichment in the transcripts responding to predator kairomones and adopting a less stringent significance threshold, 206 transcripts were identified relating to muscle function, growth, and development, with this response being greater at the later E9 stage. Furthermore, these transcripts included putative annotations for genes identified as responding to predator kairomones in other taxa, including C1q, lectin, and actin domains. Globally, transcript expression appeared reduced in response to predator kairomones and we hypothesize that this might be a result of metabolic suppression, as has been reported in other taxa in response to predation threat.

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Transcriptomic and Proteomic Analysis of Arion vulgaris—Proteins for Probably Successful Survival Strategies?

Cited by 13 publications

References 44 publications

In-depth proteomic analyses of Haliotis laevigata (greenlip abalone) nacre and prismatic organic shell matrix

In-depth proteomic analyses of Haliotis laevigata (greenlip abalone) nacre and prismatic organic shell matrix

In silico characterization of single and tandem-repeat galectin from terrestrial slug, Incilaria fruhstorferi

Transcriptomic responses to predator kairomones in embryos of the aquatic snail Radix balthica

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