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The Purplish Bifurcate Mussel Mytilisepta Virgata Gene Expression Atlas Reveals a Remarkable Tissue Functional Specialization

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The Purplish Bifurcate Mussel Mytilisepta Virgata Gene Expression Atlas Reveals a Remarkable Tissue Functional Specialization Gerdol et al. BMC Genomics (2017) 18:590 DOI 10.1186/s12864-017-4012-z RESEARCH ARTICLE Open Access The purplish bifurcate mussel Mytilisepta virgata gene expression atlas reveals a remarkable tissue functional specialization Marco Gerdol1* , Yuki Fujii2, Imtiaj Hasan3,4, Toru Koike2, Shunsuke Shimojo2, Francesca Spazzali1, Kaname Yamamoto2, Yasuhiro Ozeki3, Alberto Pallavicini1† and Hideaki Fujita2† Abstract Background: Mytilisepta virgata is a marine mussel commonly found along the coasts of Japan. Although this species has been the subject of occasional studies concerning its ecological role, growth and reproduction, it has been so far almost completely neglected from a genetic and molecular point of view. In the present study we present a high quality de novo assembled transcriptome of the Japanese purplish mussel, which represents the first publicly available collection of expressed sequences for this species. Results: The assembled transcriptome comprises almost 50,000 contigs, with a N50 statistics of ~1 kilobase and a high estimated completeness based on the rate of BUSCOs identified, standing as one of the most exhaustive sequence resources available for mytiloid bivalves to date. Overall this data, accompanied by gene expression profiles from gills, digestive gland, mantle rim, foot and posterior adductor muscle, presents an accurate snapshot of the great functional specialization of these five tissues in adult mussels. Conclusions: We highlight that one of the most striking features of the M. virgata transcriptome is the high abundance and diversification of lectin-like transcripts, which pertain to different gene families and appear to be expressed in particular in the digestive gland and in the gills. Therefore, these two tissues might be selected as preferential targets for the isolation of molecules with interesting carbohydrate-binding properties. In addition, by molecular phylogenomics, we provide solid evidence in support of the classification of M. virgata within the Brachidontinae subfamily. This result is in agreement with the previously proposed hypothesis that the morphological features traditionally used to group Mytilisepta spp. and Septifer spp.withinthesamecladeareinappropriatedueto homoplasy. Keywords: Mussel, Transcriptome, RNA-seq, Lectins, Phylogenomics, Bivalve, Mollusk Background vertical distribution is often determined by the association The purplish bifurcate mussel Mytilisepta virgata with the lower-intertidal mussel Hormomya mutabilis [3]. (Wiegmann, 1837), also known as Septifer virgatus,is This mussel species developed remarkable morphological a small bivalve mollusk species commonly found in adaptations to cope with a wave-exposed environment, in- the middle/upper intertidal zone of moderately wave- cluding a ventrally flattened, particularly resistant shell exposed shores along the coasts of Japan, Taiwan, and and stronger byssal attachment to the substrate compared South Eastern China [1], between −10 and +70 cm to other subtidal and lower-intertidal sympatric mussel above the mean tide level [2]. M. virgata is usually species [3–5]. Furthermore, M. virgata appears to be found in dense mussel beds, whose lower limit of much more resistant to high temperature stress and air exposure than M. edulis, another invasive mussel species * Correspondence: [email protected] † which preferentially occupies the lower part of the intertidal Equal contributors zone in the same geographical region [2]. Mature individuals 1Department of Life Sciences, University of Trieste, Via Giorgieri 5, 34126 Trieste, Italy are usually 45 mm long and live for approximately 4–5years, Full list of author information is available at the end of the article © The Author(s). 2017 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Gerdol et al. BMC Genomics (2017) 18:590 Page 2 of 24 although exceptional cases of 65 mm long specimen surviv- assessment of its size made by flow cytometry. The ing up to 12 years have been recorded. Sexual maturity is calculated genome c-value, 1.08, further confirmed by a reached after 12 months and, although fertility is maintained very similar estimate for the closely related Mytilisepta throughout the entire year, spawning events follow a bi- keenae (1.06) [19], reveals that the purplish Japanese modal pattern (the first one occurring in February–March, mussel genome is about 2/3 the size of those of Mytilus the second one in September–December) [6]. spp. and among the smallest known mytiloid genomes, From a taxonomical point of view, M. virgata has long but quite in line with the average genome size for all been considered as a member of the Septifer genus (and bivalves (Animal Genome Size Database, http://www.ge- therefore named S. virgatus) and placed within the nomesize.com/). subfamily Septiferinae [7]. However, this clade was later Due the narrow scientific interest posed so far on found to be polyphyletic and, based on the revised hier- mussel species other than Mytilus spp., deep sea vent archical classification of NCBI Taxonomy, M. virgata, mussels (Bathymodiolus spp.) and Perna viridis, M. along with and most of the other species previously virgata represents an interesting alternative subject for paced within this subfamily, has been moved to Mytili- the study of the evolution of Mytiloida and for the inves- nae (Rafinesque, 1815). However, the current taxonom- tigation of some peculiar gene family expansion events ical classification still does not appear to accurately which specifically occurred in this lineage [20]. reflect the evolutionary history of these mussels. Indeed, The main aim of the present work was to provide the more than a decade ago, molecular studies based on first curated and publicly accessible genomic resource Cytochrome c oxidase subunit I (COI) first pointed out for this species. The de novo assembled and functionally that M. virgata and the morphologically similar Septifer annotated transcriptome, together with gene expression excisus (Wiegmann, 1837) pertained to two different data from five different adult tissues, will serve as a clades within the order Mytiloida [8]. This observation is sequence and gene expression database for future gen- strongly supported by a recent study by Trovant and etic and molecular studies. The data we present will pro- colleagues, which reported that COI and 18S/28S– vide a substantial contribution in the improvement of based phylogeny identified both M. virgata and Myti- scientific studies in this marine mussel. While discussing lisepta bifurcata (Conrad, 1837) as members of the the potential function of tissue-specific genes, we put a same clade, together with Perumytilus purpuratus particular emphasis on expanded families encoding (Lamarck, 1819) and Brachidontes rostratus (Dunker, lectin-like proteins involved in carbohydrate recognition, 1857) (both pertaining to the Brachidontinae family), a class of molecules with a great biotechnological poten- but distantly related to Septifer bilocularis [9]. Based tial which could find a practical application in many on these results, the authors further suggested that areas of biomedical and biological research [21, 22]. Mytilisepta should be retained as a separate genus within Brachidontinae and that the septum structure Methods involved in the insertion of the adductor muscle and Collection of samples used for the current morphological classification of The selected sampling site was a natural mussel bed different species within the Septifer genusisthe found in a tide pool in Oshima, Saikai city (Nagasaki product of homoplasy. prefecture, Japan). Based on national and local fishing Apart from its disputed taxonomical placement, very regulations, no permits were required for the collection limited scientific attention has been so far focused on M. of shellfish. Five adult mussels, whose shell size approxi- virgata, with only a handful of studies dealing with its mately ranged between 4 and 5 cm, were collected, morphological adaptations [5], embryonic development dissected using razor blades and scissors, and tissues [10], reproductive cycle [6] and population dynamics [2]. were immediately placed in RNAlater (Thermo Fisher To date, only 31 nucleotide and 11 amino acid se- Scientific, Waltham, USA). Namely, the following tissues quences have been deposited in public repositories for were dissected and stored for subsequent RNA extrac- this species (data retrieved from NCBI, June 2017). tion: hemocytes (collected with a syringe), posterior ad- These include several partial sequences used for ductor muscle, inner mantle, mantle rim, digestive phylogenetic analyses [9, 11, 12], microsatellites [13], a gland, gills and foot (Fig. 1). The collected tissues were complete mitochondrial sequence (KX094521.1) and a subsequently chopped into smaller parts weighting ap- few unrelated sequences referring to still unpublished proximately 20 mg; for each of the sampled tissues, one manuscripts, highlighting the still nearly non-existing of these slices
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