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A Novel Flatworm-Specific Gene Implicated in Reproduction In www.nature.com/scientificreports OPEN A novel fatworm-specifc gene implicated in reproduction in Macrostomum lignano Received: 30 August 2017 Magda Grudniewska 1, Stijn Mouton1, Margriet Grelling1, Anouk H. G. Wolters2, Jeroen Kuipers2, Accepted: 30 January 2018 Ben N. G. Giepmans2 & Eugene Berezikov 1 Published: xx xx xxxx Free-living fatworms, such as the planarian Schmidtea mediterranea, are extensively used as model organisms to study stem cells and regeneration. The majority of fatworm studies so far focused on broadly conserved genes. However, investigating what makes these animals diferent is equally informative for understanding its biology and might have biomedical value. We re-analyzed the neoblast and germline transcriptional signatures of the fatworm M. lignano using an improved transcriptome assembly and show that germline-enriched genes have a high fraction of fatworm- specifc genes. We further identifed the Mlig-sperm1 gene as a member of a novel gene family conserved only in free-living fatworms and essential for producing healthy spermatozoa. In addition, we established a whole-animal electron microscopy atlas (nanotomy) to visualize the ultrastructure of the testes in wild type worms, but also as a reference platform for diferent ultrastructural studies in M. lignano. This work demonstrates that investigation of fatworm-specifc genes is crucial for understanding fatworm biology and establishes a basis for such future research in M. lignano. Animal models inspired researchers for hundreds of years. In biomedicine, a variety of organisms is employed to study e.g. development, ageing, and mechanistic underpinnings of diseases, with the aim of translating these fndings to humans. While most research focusses on the use of established models, such as yeast, nematodes, fruit fies, and mice, it is sometimes the unique feature of a non-standard experimental model that brings the breakthrough. For example, squalamine, a compound isolated from dogfsh sharks, exhibits strong anti-fungal and anti-bacterial activity. It was shown to be very efcient in fghting a broad spectrum of human pathogens, strengthening its therapeutic potential1. Another example is a recent study deciphering the remarkable resistance of tardigrades to X-ray radiation, which led to the discovery of a novel DNA protector, the Dsup protein. When expressed in human cells, this protein shows the ability to protect human DNA as well2. Tese examples indicate the power of exploring nature’s biodiversity, with a focus on organisms demonstrating extreme characteristics, such as a remarkable resistance to environmental factors, astonishing regeneration abilities, or an extremely long lifespan3–6. One of such organisms is the free-living, hermaphrodite fatworm Macrostomum lignano (Fig. 1a), which has a number of interesting features such as the ability of whole-body regeneration7, a high resistance to ionizing irradiation up to 210 Gray8, and the presence of a population of actively proliferating neoblasts, which represent the stem cells and progenitors of fatworms9–11. Recently, we established the transcriptional signatures of the proliferating somatic neoblasts and germline cells, and demonstrated the role of several genes conserved between M. lignano and human in stem cell and germline biology12. To understand the biology of this model organism, it will, however, be crucial to also perform functional studies of non-conserved genes. Tis is illustrated for example by the recent identifcation of three novel Mlig-stylet genes, which are required for the diferentiation of the male copulatory apparatus during tail-regeneration13. Importantly, investigating non-conserved genes may also lead to discoveries translatable to human health, such as improved wound healing or novel anthelminthic drugs. Te present study demonstrates the groundwork we laid for this novel research direction. As a frst step, we reanal- yzed the published dataset using an improved transcriptome assembly, and reassessed the conservation level of 1European Research Institute for the Biology of Ageing, University of Groningen, University Medical Center Groningen, Antonius Deusinglaan 1, 9713AV, Groningen, The Netherlands. 2Department of Cell Biology, University of Groningen, University Medical Center Groningen, Antonius Deusinglaan 1, 9713AV, Groningen, The Netherlands. Magda Grudniewska and Stijn Mouton contributed equally to this work. Correspondence and requests for materials should be addressed to E.B. (email: [email protected]) SCIENTIFIC REPORTS | (2018) 8:3192 | DOI:10.1038/s41598-018-21107-4 1 www.nature.com/scientificreports/ a b c d e eye Dp gut H Nh testes Br ovaries f Nu S Bs Figure 1. Te structure of testes and sperm cells in healthy control and Mlig-sperm1 knockdown M. lignano animals. (a) Illustration of the simplifed morphology of M. lignano, indicating the location of the eyes, gut, testes, and ovaries. (b,c) Comparison of the overall morphology between control (b) and Mlig-sperm1(RNAi) (c) individuals. (d) Schematic structure of an adult sperm cell. Dp, distal process (feeler); H, head; Nh, notch; Br, bristle; Nu, nucleus; S, shaf; Bs, brush. For a detailed description of sperm cells in M. lignano see Ref.16. (e,f) Comparison of sperm morphology between control (e) and knockdown (f) worms using DIC microscopy. Scale bars are 100 µm (b,c) and 10 µm (e,f). genes enriched in the neoblasts and germline cells. In addition, we present the characterization of a previously uncharacterized gene which we named Mlig-sperm1. Knockdown of this gene results in aberrations in the gonads and sperm structure, and leads to a reduced fertility. Tis serves as a case study to illustrate the recently developed techniques and resources allowing in depth gene characterization of M. lignano. Results Extended M. lignano transcriptome assembly. As part of the M. lignano genome annotation we have recently published a genome-guided transcriptome assembly Mlig_RNA_3_7_DV1_v114. We noticed that some real but lowly expressed genes, such as TERT15, were not included in this transcriptome assembly because all predicted transcripts with low expression levels (RPKM < 0.5) were fltered out. To mitigate this problem, we extended the transcriptome assembly by keeping low expression transcripts if they contain a predicted open read- ing frame of at least 100 amino acids. Te new transcriptome assembly, Mlig_RNA_3_7_DV1_v3, has 143,648 transcriptional units, which are processed into 153,985 genes afer identifcation of trans-splicing events, and include duplicated gene copies and alternative transcript forms (Supplementary Table 1). Clustering of sequences by 95% global sequence identity results in 53,480 and 88,426 non-redundant transcriptional units and genes respectively (Supplementary Table 1). Characterization of conservation levels in diferent gene groups. To identify the conservation lev- els of genes enriched in proliferating cells, we frst re-analyzed the previously established proliferating neoblast and germline transcriptional signatures12 using the extended transcriptome assembly Mlig_RNA_3_7_DV1_v3 (Supplementary Table 2, Supplementary Fig. 1). While the conclusions of the previous work do not change with the new analysis, the number of transcript clusters classifed as ‘stringent neoblast’ increased from 357 to 489 (Supplementary Fig. 1k); in contrast, the number of ‘irradiation’ and ‘germline’ transcript clusters decreased from 7,277 to 5,901 and from 2,739 to 2,604 respectively (Supplementary Fig. 1c,g). We assigned the conservation level to each M. lignano gene as ‘conserved’ if there is a signifcant homology with human genes, as ‘fatworm-specifc’ if homologs are identifed only in the free-living Schmidtea mediterranea and/or the parasite Schistosoma man- soni, or as ‘M. lignano-specifc’ if no homologs are detected (Table 1). Te distribution analysis of the conserva- tion levels between diferent gene categories revealed striking diferences between neoblast and germline genes. While overall 47.3% of M. lignano genes are conserved in human, 8.2% are fatworm-specifc and 44.5% are Macrostomum-specifc (Table 1), for the neoblast genes the fraction of human-conserved genes is substantially higher at 85%, while fatworm-specifc and non-conserved gene fractions are only 2.8% and 12.2% respectively (Table 1). At the same time, the fraction of germline genes conserved in human is 37.6%, which is signifcantly less than overall, while the fraction of Macrostomum-specifc genes rises to 54.2% (Table 1). Since in this analysis we used all transcripts from the Mlig_RNA_3_7_DV1_v3 transcriptome assembly, including transcripts with- out predicted open reading frame (ORF), it is possible that the fraction of Macrostomum-specifc transcripts is infated. We repeated the conservation distribution analysis using only transcripts with ORFs and cluster- ing sequences at 95% amino-acid identity level to exclude biases due to possible expansions of gene families. However, the picture did not change signifcantly: overall 55.3% of genes are conserved in human, 9.7% are SCIENTIFIC REPORTS | (2018) 8:3192 | DOI:10.1038/s41598-018-21107-4 2 www.nature.com/scientificreports/ Total Homologs in Homologs in S. Homologs in S. Flatworm- number human mediterranea mansoni specifc* M. lignano- specifc Transcript clusters All 50,673 23,969 (47.30%) 25,716 (50.75%) 21,581 (42.59%) 4,159 (8.21%) 22,545 (44.49%) Neoblasts 1,062 902 (84.93%) 871 (82.02%) 838 (78.91%) 30 (2.82%) 130 (12.24%) Neoblasts, 489 406 (83.03%) 379 (77.51%) 370 (75.66%) 14 (2.86%) 69 (14.11%) stringent Germline 2,604 979 (37.60%) 1067 (40.98%) 840 (32.26%) 213 (8.18%) 1,412 (54.22%) Protein clusters All 30,017 16,605 (55.32%) 17,758 (59.16%) 14,819 (49.37%) 2,913 (9.70%) 10,499 (34.98%) Neoblasts 840 723 (86.07%) 693 (82.50%) 676 (80.48%) 25 (2.98%) 92 (10.95%) Neoblasts, 404 336 (83.17%) 310 (76.73%) 307 (75.99%) 10 (2.48%) 58 (14.36%) stringent Germline 1,917 815 (42.51%) 882 (46.01%) 707 (36.88%) 173 (9.02%) 929 (48.46%) Table 1. Conservation of diferent M. lignano gene groups in human and fatworms. *Present in S.
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