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Comparative Transcriptomic Analysis Reveals Candidate Genes and Pathways Involved in Larval Settlement of the Barnacle Megabalanus Volcano

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Comparative Transcriptomic Analysis Reveals Candidate Genes and Pathways Involved in Larval Settlement of the Barnacle Megabalanus Volcano International Journal of Molecular Sciences Article Comparative Transcriptomic Analysis Reveals Candidate Genes and Pathways Involved in Larval Settlement of the Barnacle Megabalanus volcano Guoyong Yan 1,2, Gen Zhang 3 ID , Jiaomei Huang 1, Yi Lan 4, Jin Sun 4 ID , Cong Zeng 1, Yong Wang 1, Pei-Yuan Qian 4 and Lisheng He 1,* 1 Department of Life Sciences, Institute of Deep-sea Science and Engineering, Chinese Academy of Sciences, Sanya 572000, China; [email protected] (G.Y.); [email protected] (J.H.); [email protected] (C.Z.); [email protected] (Y.W.) 2 College of Earth Sciences, University of Chinese Academy of Sciences, Beijing 100864, China 3 The Shenzhen Nobel Science and Technology Service Co., Ltd., Nanshan District, Shenzhen 440305, China; [email protected] 4 Division of Life Sciences, The Hong Kong University of Science and Technology, Clear Water Bay, Kowloon, Hong Kong, China; [email protected] (Y.L.); [email protected] (J.S.); [email protected] (P-Y.Q.) * Correspondence: [email protected]; Tel.: +86-898-8838-0060 Received: 25 September 2017; Accepted: 23 October 2017; Published: 27 October 2017 Abstract: Megabalanus barnacle is one of the model organisms for marine biofouling research. However, further elucidation of molecular mechanisms underlying larval settlement has been hindered due to the lack of genomic information thus far. In the present study, cDNA libraries were constructed for cyprids, the key stage for larval settlement, and adults of Megabalanus volcano. After high-throughput sequencing and de novo assembly, 42,620 unigenes were obtained with a N50 value of 1532 bp. These unigenes were annotated by blasting against the NCBI non-redundant (nr), Swiss-Prot, Cluster of Orthologous Groups (COG), and Kyoto Encyclopedia of Genes and Genomes (KEGG) databases. Finally, 19,522, 15,691, 14,459, and 10,914 unigenes were identified correspondingly. There were 22,158 differentially expressed genes (DEGs) identified between two stages. Compared with the cyprid stage, 8241 unigenes were down-regulated and 13,917 unigenes were up-regulated at the adult stage. The neuroactive ligand-receptor interaction pathway (ko04080) was significantly enriched by KEGG enrichment analysis of the DEGs, suggesting that it possibly involved in larval settlement. Potential functions of three conserved allatostatin neuropeptide-receptor pairs and two light-sensitive opsin proteins were further characterized, indicating that they might regulate attachment and metamorphosis at cyprid stage. These results provided a deeper insight into the molecular mechanisms underlying larval settlement of barnacles. Keywords: Megabalanus volcano; transcriptome; larval settlement; neuropeptide; opsin; GPCRs 1. Introduction Barnacles are the only sessile marine crustacean playing important roles in costal ecosystems which mainly inhabit in intertidal to subtidal zones and are distributed all over the world [1]. As one of the major marine fouling organisms, the existence of barnacles leads to great economic losses for removing them in marine industries and navigation [2,3]. Therefore, there is significantly increasing interest in finding an efficient way to deal with biofouling by marine biologists as well as chemists. The life cycle of the barnacle consists of two phases, free swimming planktonic phase and permanent sessile phase. Newly hatched larvae (Nauplius I) molt six times to reach a non-feeding cyprid stage, which is the last stage of planktonic phase and the most important stage for larval settlement as well. Int. J. Mol. Sci. 2017, 18, 2253; doi:10.3390/ijms18112253 www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2017, 18, 2253 2 of 15 Larval settlement of the barnacle is a complicated process regulated by both external environmental factors and internal biological factors. Due to the lack of genome information, the progress of understanding the Int. J. Mol. Sci. 2017, 18, 2253 2 of 15 molecular mechanisms underlying barnacle larval settlement is relatively limited. For example, Clare et al., 1995,external found that environmental elevated level factors of theand intracellular internal biological cyclic factors. adenosine Due monophosphateto the lack of genome (cAMP) information, significantly increasedthe progress the settlement of understanding rate of cyprids the molecular [4]. Settlement-inducing mechanisms underlying protein barnacle complex larval (SIPC), settlement a glycoprotein is foundrelatively from the limited. adult extracts,For example, was Clar demonstratede et al., 1995, to found induce that the elevated conspecific level larvalof the settlementintracellular [ 5cyclic]. Inadenosine the last monophosphate few years, the (cAMP) rapid developmentsignificantly increased of next generationthe settlement sequence rate of (NGS), cyprids especially [4]. RNA-seq,Settlement-inducing made it possible protein to get complex the transcriptome (SIPC), a glycoprotein of a species found in afrom less the time- adult and extracts, cost-consuming was way.demonstrated For barnacles, to induce Chen etthe al., conspecific 2011, obtained larval settlement the transcriptome [5]. of Amphibalanus amphitrite by 454 In the last few years, the rapid development of next generation sequence (NGS), especially RNA- pyrosequencing, and 23,451 contiguous sequences were identified. Among them, 7954 unigenes were seq, made it possible to get the transcriptome of a species in a less time- and cost-consuming way. differentially expressed between larval and adult stage, 743 unigenes were uniquely expressed in the For barnacles, Chen et al., 2011, obtained the transcriptome of Amphibalanus amphitrite by 454 larvalpyrosequencing, stages, and 443 and unigenes 23,451 contiguous were at least sequences 10-fold were higher identified. in larvae Among than them, adults 7954 [6]. unigenes Those specifically were or highlydifferentially expressed expressed genes between in larvae larval provided and adult potential stage, 743 candidates unigenes were for uniquely the mechanism expressed studiesin the on larvallarval settlement. stages, and Based 443 unigenes on the were transcriptome at least 10-fold database, higher in the larvae neuropeptidome than adults [6]. Those of A. specifically amphitrite was characterized,or highly expressed revealing genes 14 neuropeptides in larvae provided and potential peptide candidates hormones for through the mechanism in silico studies transcriptome on mining.larval Further settlement. real-time Based PCR on andthe transcriptome bioassay results database, showed the that neuropeptidome these neuropeptides of A. amphitrite were involved was in larvalcharacterized, settlement [ 7revealing]. Moreover, 14 neuropeptides He et al., 2012 and and peptide Zhang hormones et al., 2013 through discovered in silico that transcriptome the activation of the MKK3-p38mining. Further MAPK real-time pathway PCR mightand bioassay involve results settlement showed [ 8that,9]. these These neuropeptides progresses demonstratedwere involved that in larval settlement [7]. Moreover, He et al., 2012 and Zhang et al., 2013 discovered that the activation transcriptome database could greatly facilitate the researches on the molecular mechanisms underlying of the MKK3-p38 MAPK pathway might involve settlement [8,9]. These progresses demonstrated barnacle larval settlement. that transcriptome database could greatly facilitate the researches on the molecular mechanisms Theunderlying cyprid barnacle of barnacle larval Megabalanussettlement. volcano (Pilsbry, 1916) is quite bigger in size than that of A. amphitriteThe, socyprid sometimes of barnacle it is Megabalanus a better model volcano organism, (Pilsbry, when1916) is researchers quite bigger need in size to observethan that theof A. cyprid behavioramphitrite or dissect., so sometimes Yet, the itgenetic is a better resources model organism, of Megabalanus when researchersbarnacle need are still to observe lacking, the which cyprid might hinderbehavior studies or ondissect. molecular Yet, the mechanism genetic resources underlying of MegabalanusMegabalanus barnaclebarnacle are still larvallacking, settlement. which might In the presenthinder study, studies both on cyprids molecular and mechanism adults of underlying the barnacle MegabalanusM. volcano barnacle(Figure larval1I,J) settlement. were sampled In the for RNA-seq.present The study, differentially both cyprids expressed and adults genesof the barnacle (DEGs) M. or volcano pathways (Figure between 1I,J) were cyprids sampled and for adults RNA- were identified.seq. The Neuropeptides differentially expressed and cognate genes G (DEGs) Protein-coupled or pathways receptors between (GPCRs),cyprids and and adults light-sensitive were identified. Neuropeptides and cognate G Protein-coupled receptors (GPCRs), and light-sensitive proteins were screened and characterized. These results provide good genomic resources of the proteins were screened and characterized. These results provide good genomic resources of the barnacle M. volcano for further investigations. barnacle M. volcano for further investigations. Figure 1. Embryos, larvae and adults of barnacle Megabalanus volcano. (A) Zygote; (B) 2-cells; (C) 4- Figurecells; 1. Embryos,(D) Multi-cells; larvae (E and) Later adults developed of barnacle embryo;Megabalanus (F) Fully developed volcano.( Aembryo;) Zygote; (G) ( BNauplius) 2-cells; II; (C ()H 4-cells;) (D) Multi-cells;Nauplius VII; (E )(I Later) Cyprid; developed and (J) Adult. embryo; (F) Fully developed embryo; (G) Nauplius II; (H) Nauplius VII; (I)
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