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Diatom Flagellar Genes and Their Expression During Sexual Reproduction in Leptocylindrus Danicus

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Diatom Flagellar Genes and Their Expression During Sexual Reproduction in Leptocylindrus Danicus Nanjappa et al. BMC Genomics (2017) 18:813 DOI 10.1186/s12864-017-4210-8 RESEARCH ARTICLE Open Access Diatom flagellar genes and their expression during sexual reproduction in Leptocylindrus danicus Deepak Nanjappa1,2* , Remo Sanges1, Maria I. Ferrante1 and Adriana Zingone1 Abstract Background: Flagella have been lost in the vegetative phase of the diatom life cycle, but they are still present in male gametes of centric species, thereby representing a hallmark of sexual reproduction. This process, besides maintaining and creating new genetic diversity, in diatoms is also fundamental to restore the maximum cell size following its reduction during vegetative division. Nevertheless, sexual reproduction has been demonstrated in a limited number of diatom species, while our understanding of its different phases and of their genetic control is scarce. Results: In the transcriptome of Leptocylindrus danicus, a centric diatom widespread in the world’s seas, we identified 22 transcripts related to the flagella development and confirmed synchronous overexpression of 6 flagellum-related genes during the male gamete formation process. These transcripts were mostly absent in the closely related species L. aporus, which does not have sexual reproduction. Among the 22 transcripts, L. danicus showed proteins that belong to the Intra Flagellar Transport (IFT) subcomplex B as well as IFT-A proteins, the latter previously thought to be absent in diatoms. The presence of flagellum-related proteins was also traced in the transcriptomes of several other centric species. Finally, phylogenetic reconstruction of the IFT172 and IFT88 proteins showed that their sequences are conserved across protist species and have evolved similarly to other phylogenetic marker genes. Conclusion: Our analysis describes for the first time the diatom flagellar gene set, which appears to be more complete and functional than previously reported based on the genome sequence of the model centric diatom, Thalassiosira pseudonana. This first recognition of the whole set of diatom flagellar genes and of their activation pattern paves the way to a wider recognition of the relevance of sexual reproduction in individual species and in the natural environment. Keywords: Leptocylindrus, Next generation sequencing, Transcriptome, Diatom, Sexual reproduction, Flagellar genes Background reproduction rates during population outburst must Diatoms are among the most important components of have profound consequences for the genetic variability the marine pelagial, where they contribute ca 40% of the and fitness of the individual species, thus influencing total production [1]. Diatom blooms fuel the whole evolutionary processes that are at the basis of the trophic web and are responsible for a considerable part formidable success of diatoms [2, 3]. Sexual processes in of the CO2 drawdown in the world’s oceans. In addition diatoms are also crucial to the restoration of the cell to the ecological role of diatom blooms in the oceanic size. Considerable miniaturization occurs during asexual biomass build-up, the enhanced asexual and sexual division due to the peculiar structure of the rigid silica shell, composed of two unequal parts each inherited by * Correspondence: [email protected] daughter cells, which reconstruct new, smaller silica 1Stazione Zoologica Anton Dohrn, Villa Comunale, 80121 Naples, Italy 2College of Earth, Ocean and Environment, University of Delaware, 700 halves within the maternal ones. Therefore, following the Pilottown Road, Lewes 19958, Delaware, USA high number of mitotic divisions during a bloom (1–2per © 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. Nanjappa et al. BMC Genomics (2017) 18:813 Page 2 of 11 day or more), the average cell size considerably decreases, flagellum or cilium structure complexes, while the cen- until gametes are formed and conjugation occurs. The soft trics have lost the IFT-A and BBSome subcomplexes, cell wall of the zygote allows cell enlargement, and a new retaining only the IFT-B subcomplex [16]. silica shell is formed only when the maximum size is The worldwide distributed marine centric diatom Lep- reached again. tocylindrus danicus [17–19] presents a peculiar sexual The occurrence of sexual reproduction in diatoms is reproduction modality, whereby the zygote formed by presumably widespread, and blooms are likely to maxi- conjugation turns into a thick walled spore that can re- mise encounter probability which is necessary to gamete sist in a dormancy phase for long time in the sediments. fusion and zygote formation. However, gametes or zy- In almost all diatoms the zygote gives rise to vegetative gotes or other signals of sexual reproduction have rarely cells instead, while resting stages are formed during been observed in the natural environment [4, 5], while asexual reproduction [20, 21]. By contrast, sexual information on the sexual cycle of diatoms is available reproduction has not been found in the congeneric L. for a limited number of species (200 over more than aporus, which despite a high morphological similarity, 10,000 known species) mostly through laboratory experi- differs from L. danicus in several physiological and eco- ments (see [6] for a review). Even less known are the logical characteristics [17, 18, 22–24]. To address func- molecular processes occurring during sexual tional differences between the two species, we cultivated reproduction. The scarce information available concerns them and sequenced their transcriptomes taking advan- early reports of SIG (sex induced gene) in the centric tage of the Marine Microbial Eukaryotic Transcriptome species Thalassiosira weissflogii [7], followed by more re- Sequencing Project (MMETSP, [25]). The comparison fined analyses in the pennate diatoms Pseudostaurosira led to the discovery of several genes linked to flagellar trainorii [8], Seminavis robusta [9, 10] and Pseudo- development in L. danicus. The aim of this study was to nitzschia multistriata [11]. Nowadays the use of gen- test their actual function through qPCR conducted along omic tools, boosted by the development of Next Gener- a sexual event induced in a laboratory experiment. In ation Sequencing techniques, offers the possibility to addition, we exploited the whole transcriptomic dataset search for genes activated during sexual reproduction produced within the MMETSP [25], where 305 species and start reconstructing the series of events accompany- from 210 genera were sequenced, to search for genes as- ing the different phases of this crucial process in diatom sociated to flagellar development in the available diatom life cycles. transcriptomes and trace phylogenetic relationships Interestingly, while in the prevalently benthic pennate across the protist tree based on two flagellar genes. diatoms the reproduction is heterothallic and isogamous, in the prevalently planktonic centric diatoms the Results reproduction is homothallic and large eggs and flagel- Identification of differentially represented GO terms lated male gametes are produced. This is the only case The transcriptomes of L. danicus (strain SZN-B650) and where flagellated stages are observed in diatoms, provid- L. aporus (strain SZN-B651) were obtained by sequencing ing a clear signal of sexual reproduction at least in cen- samples collected at the exponential phase, under identical tric species [6]. By contrast, flagella and cilia are growth conditions for the two species. The transcriptomes widespread in the vegetative phase of several groups of of the two species were assembled, annotated and mapped protists, where they confer motility to the cells and to as described in the supplementary material (Additional file some extent allow for movements across the water col- 1: Sequence assembly and annotation, and Table S1–Table umn. Among genes that have been associated to cell S4; Additional file 2: Figure S1; Additional file 3: Figure motility, those of the intraflagellar transport (IFT) parti- S2; Additional file 4: Figure S3; Additional file 5: Figure cles are specifically related to the flagellum/cilium devel- S4; Additional file 6: Figure S5). Comparative analysis, fol- opment and, along with kinesin and dynein motors, help lowing Fisher’s exact test (FDR <0.05), led the identifica- transport flagellum components from the cell body into tion of 10 GO terms that were identified as differentially the cilium [12]. The IFT particles consist of three represented between the two species (Additional file 7: subcomplexes called IFT-A, IFT-B and BBSome Table S5A). These classes contained 3917 and 2142 tran- (Bardet–Biedl syndrome). These subcomplexes are made scripts from L. danicus and L. aporus, respectively. Nine of many unique proteins and together they are involved of the ten GO terms were over represented in L. danicus, in the flagellar assembly, maintenance, and signalling while in L aporus only ‘protein tyrosine kinase activity’ [13–15]. IFT and BBSome genes are either retained or was over represented.
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