Widespread of horizontal gene transfer in the human genome
© The Author(s). 2017
Received: 9 August 2016
Accepted: 21 March 2017
Published: 4 April 2017
A fundamental concept in biology is that heritable material is passed from parents to offspring, a process called vertical gene transfer. An alternative mechanism of gene acquisition is through horizontal gene transfer (HGT), which involves movement of genetic materials between different species. Horizontal gene transfer has been found prevalent in prokaryotes but very rare in eukaryote. In this paper, we investigate horizontal gene transfer in the human genome.
From the pair-wise alignments between human genome and 53 vertebrate genomes, 1,467 human genome regions (2.6 M bases) from all chromosomes were found to be more conserved with non-mammals than with most mammals. These human genome regions involve 642 known genes, which are enriched with ion binding. Compared to known horizontal gene transfer regions in the human genome, there were few overlapping regions, which indicated horizontal gene transfer is more common than we expected in the human genome.
Horizontal gene transfer impacts hundreds of human genes and this study provided insight into potential mechanisms of HGT in the human genome.
The acquisition of genes from an organism other than a direct ancestor, which is called horizontal gene transfer (HGT), is well known in bacteria and unicellular eukaryotes [1–6]. Although the transfer of genes is thought to be crucial in prokaryotic evolution, its existence in higher organisms, including animals, is less well established [7–9]. However, in recent years, more and more instances of horizontal gene transfer have been reported in multicellular eukaryotes, even in humans [7–12]. This phenomenon has been previously reported in bovine genome, which has a high abundance of the BovB sequence of the python and copperhead reptiles. However, the BovB sequence was more similar between cows and reptiles than cows and horses. A proposed mechanism for this phenomenon was horizontal gene transfer between organisms with ticks as the media . Another project discovered the “Space Invaders,” or SPIN elements, that were highly conserved between seven distantly related species from diverse lineages. A proposed mechanism to explain the similarity of sequences between two species with a very distant common ancestor was horizontal gene transfer .
A recent study investigated the possibility of HGT in 26 animal species (10 primates, 12 flies and four nematodes) and a simplified analysis in a further 14 vertebrates. Genome-wide comparative and phylogenetic analyses show that HGT in animals typically gives rise to tens or hundreds of active ‘foreign’ genes, largely concerned with metabolism. This analyses suggest that while fruit flies and nematodes have continued to acquire foreign genes throughout their evolution, humans and other primates have gained relatively few since their common ancestor .
In this study, we analyzed the pair-wise alignment data between the human reference genome hg19  and 53 other vertebrates (41 mammalian vertebrates and 12 non-mammalian vertebrates). We identified potential HGT regions in the human genome (see Methods). Genome annotations and genome-wide signals from recent genomics or epigenetics studies [15, 16] of these sequences have been gathered to infer the functions of these predicted HGT regions, and evolutionary trends of these sequences have been analyzed. This study thus sheds light upon the prevalence of HGT and provide an insight of its underlining mechanisms.
Pair-wise alignments between the human genome and 53 vertebrate genomes
We started with the pair-wise blastz alignments between the human reference genome hg19  and 53 other vertebrates (41 mammalian vertebrates and 12 non-mammalian vertebrates). The alignment data were then linked into chains and formed into an alignment net . More details about the pair-wise alignment data can be found in the UCSC Genome Browser website .
HGT identification pipeline
It’s notable that this set of predicted HGT regions are not comprehensive since some regions may be separated by small gaps between alignment sequences that cause two short, yet close, conserved sequences to be filtered out. In order to check the reliability of HGT predictions, we explored various identity thresholds in the pipeline (40%, 50 and 60%) between vertebrates and the human genome and the length coverage (40%, 20% and 0) between mammals and the human genome to calculate the number of predicted or candidate HGT regions.
Conservation analysis of predicted HGT regions
To verify the conservation levels of the sequences we extracted, we randomly sampled 50 sequences from our results and verified the sequences based on the existence of homologous sequence in several groups of vertebrates using the University of California Santa Cruz (UCSC) Comparative Genomics track (Primate Chain/Net, Placental Chain/Net, Vertebrate Chain/Net) [17, 19, 20]. We grouped the 53 vertebrates into two bins: the first bin includes all non-human mammals; the second bin includes all non-mammal vertebrates. For each of our samples, we determined if less than eight mammals have homology sequences with ≥40% identity with hg19 and ≥ 40% of the human genome region length covered.
Genes Overlapping predicted HGT regions
We checked whether our sets of predicted HGT sequences overlapped with known coding genes in ENSEMBL database . We downloaded the Homo sapiens gene data from ENSEMBL database and converted them into bed format file. For each sequences dataset, we intersected the Ensembl Genes with these sequences to discover genes that had any overlap with the predicted HGT regions.
Coding status analysis
We extracted the transcript IDs from the overlapped Ensembl genes and searched these IDs through the Ensembl Human Gene sets table, in which these genes were classified as protein coding, pseudogenes, etc. .
Gene enrichment analysis
All involved genes were generated from Ensemble Genes  and enrichment of these genes was calculated using the Database for Annotation, Visualization and Integrated Discovery (DAVID [22, 23], version 6.7) with all human genes as the background level. All items were adjusted with the modified Fisher Exact p-value (EASE score) < 0.05. The gene enrichment results were shown in three aspects: 1) molecular functions, 2) biological processes, and 3) cellular components.
Chromatin state analysis
Using the Broad chromHMM  Chromatin State track in nine cell lines (Gm12878, H1hesc, Hepg2, Hmec, Hsmm, Huvec, K562, Nhek, Nhlf), we checked the chromatin states of HGT regions. We then compared the percentages of different chromatin states in these regions against the corresponding values in the whole human genome as the background.
We used the RepeatMasker track from the UCSC Genome Browser to generate distributions of the different types of repeats, including SINEs, LINEs, LTRs, DNA repeats and simple repeats . We divided the HGT regions and flanking regions into five regions: w1 (300 bps upstream regions of the HGT regions), w2 (the beginning 300 bps of the HGT regions), w3 (the middle regions of the HGT regions), w4 (the ending 300 bps of the HGT regions), and w5 (300 bps downstream of the HGT regions). We calculated the average proportions of different types of repeats in the five regions of our sequences and drew the average proportions curve of different types of repeats within the HGT regions and 300 bps upstream and downstream of the HGT regions.
GC content analysis
We calculated the GC content and drew GC content curve for the HGT regions with a similar approach as the above section we did for repeats.
Histone modification analysis
In order to predict regulatory functions of our sequence, regulatory related histone modification and histone variants on the sequences in H1-hESC cell lines was investigated. One transcription related histone marks: H3K4Me1; and four regulation-related histone marks and variations: H2A.Z, H3K4Me3, H3K9Ac, and H3K27Ac  were applied. In addition, one histone methylation related to polycomb-repression: H3K27Me3 [16, 24] was also included. All these datasets were downloaded from the corresponding tracks in the UCSC genome browser.
Highlighting conservation in phylogenetic tree
We took the phylogenetic tree directly from the Comparative Genomics track “Vertebrate Multiz Alignment & Conservation (100 Species)” [25, 26]. For each HGT region, we extracted the homologous sequences from related vertebrate genomes. Then we aligned these homology sequences by ClustalW and constructed the phylogenetic tree by Maximum Likelihood Method using MEGA6 . We compared this HGT homologous sequence based phylogenetic tree with the species phylogenetic tree and analyzed the differences between two phylogenetic trees. In order to show the predicted HGT events between these species, we used Sprit  to calculate the minimum subtree prune and regraft (SPR) distance between the species phylogenetic tree and the HGT homology sequence based phylogenetic tree.
Searching the homologous sequences in media species
In order to check the confidence levels of the HGT regions found in the human genome, we checked the possible transfer paths from other species to human. 22 HGT fragments (similarity between vertebrates and hg19 was larger than 60% with lengths at least 1000 bps and no alignment between mammalian genomes and hg19 was allowed) were aligned with blastn to the Nucleotide collection database of National Center for Biotechnology Information (NCBI), which consists of all nucleotide sequences available. We searched the Nucleotide collection database to find the homologous sequences of our HGT fragments in some species, which might be the media species for the HGT progress, such as parasites, bacteria or fungi.
In our pipeline (see Methods), we compared pair-wise alignment block regions between 53 vertebrates and the human genome and extracted those human genome sequences that show greater conservation with non-mammalian vertebrates than with most mammals. With the similarity threshold (40%) and the length coverage (40%) between mammalian genomes and hg19, our pipeline has found 1,467 HGT regions longer than 1,000 bps.
The location bias of predicted HGT regions in chromosomes
Distribution of predicted HGT regions in chromosomes of the human genome
Since the HGT regions we predicted here happened after the split of primates from mammals, this discovery leads us to conjecture that the HGT fragments might be more likely to insert on both ends of the chromosomes.
Analysis of overlapped genes
The types of genes overlapping HGT regions
Non gene region
Gene enrichment analysis of genes overlapping HGT regions by DAVID
GO:0043167 ~ ion binding
GO:0043169 ~ cation binding
GO:0046872 ~ metal ion binding
Chromatin states of predicted HGT regions
Chromatin states of predicted HGT regions
Repetitive elements in predicted HGT regions
Compared to the flanking regions, the predicted HGT regions contains higher percentages of “simple repeat” and “Low complexity repeat”. But for the other types of repeats, such as “LTR”, “SINE” and “LINE” repeats, the percentage in HGT regions is lower than the upstream and downstream regions (Fig. 5b).
GC contents of predicted HGT regions
We calculated the average percentage of CG content of predicted HGT regions and their 300 bps upstream and downstream regions. The average GC percentage of HGT regions is higher than the upstream and downstream regions (Fig. 5c).
Histone modification analysis of predicted HGT regions
We calculated the average percentage of regulatory related histone modification signals in predicted HGT regions and their 300 bp upstream and downstream regions. Results showed no significant feature of histone modification in HGT regions (Fig. 5d).
Phylogenetic tree analysis
Our pipeline can find the HGT regions which have greater conservation with non-mammalian vertebrates than with most mammals. It is also important to note that we allow less than eight mammals containing homologous sequences with the human genome. Indeed, for most HGT regions we have found, some mammals do have homologous sequences with hg19 and most of them are the primates. This phenomenon indicated horizontal gene transfer happened between the ancestor of primates and the non-mammalian vertebrates.
In order to further understand the HGT mechanism, we extracted homologous sequence of the predicted horizontal gene transfer sequences in mammals and non-mammalian species, constructed sequence phylogenetic tree and compared it with species phylogenetic tree. Comparison of two phylogenetic trees showed that, in most cases, two phylogenetic trees were not consistent. Then we compared the tree constructed from predicted HGT regions to the tree constructed from species genomes using the program SPRIT that estimated the number of required subtree prune and regrafts (SPR) to transform one tree into another. It was apparent from the SPRIT output that for most HGT regions, at least three or four SPRs are required to explain the homologous sequences' phylogenetic tree topology. Each SPR may correspond to at least one HGT event, therefore we conclude that at least three or four interspecies HT events have occurred during the evolutionary history of vertebrates. Besides, when we verify the possibility of these HGT events, we found that there were at least one HGT event between the ancestor of all or most primates and the non-mammalian.
The homologous sequences in media species
The homologous sequences of predicted HGT regions in parasites of human
Horizontal transfer sequences
Echinostoma caproni, Trichomonas vaginalis, Brugia malayi, Nippostrongylus brasiliensis
Lottia gigantea, Plasmodium yoelii
Toxocara canis genome, Eimeria maxima
Leishmania infantum, Neospora caninum, Protopolystoma xenopodis, Leishmania mexicana, Echinostoma caproni, Neospora caninum, Toxocara canis, Ascaris lumbricoides
Protopolystoma xenopodis, Enterobius vermicularis, Nippostrongylus brasiliensis, Echinostoma caproni, Helicobacter pylori, Leishmania infantum, Trichobilharzia regenti, Taenia asiatica
The reliability of predicted HGT regions predicted in the human genome
In our pipeline, we can also change the similarity threshold (40%, 50, 60%) between vertebrates and hg19 and the length coverage (40%, 20%, 0) between mammalian vertebrates and hg19 to calculate the number of sequences and the total bases we extracted for HGT regions. With different threshold values, we have discovered different number of sequences. We have discovered 22 HGT regions when we set the similarity threshold to 60% and length coverage to 0. These 22 sequences are more likely to be the result of HGT events. We verified the sequences based on the existence of homologous sequence in several groups of vertebrates using the University of California Santa Cruz (UCSC) Comparative Genomics (Primate Chain/Net, Placental Chain/Net, Vertebrate Chain/Net), finding 19 sequences have an abnormal conservation. When we lowered the similarity threshold to 40% and raised the length coverage to 40%, we have discovered 1,467 predicted HGT regions. In order to verify the result of 1,467 sequences, we sampled 50 of them to check their conservation levels manually in mammals and non-mammalian species using the (UCSC) Comparative Genomics track (Primate Chain/Net, Placental Chain/Net, Vertebrate Chain/Net). We found 44 of the 50 regions (88%) have an abnormal conservation. Therefore, there might be hundreds or even more than a thousand predicted HGT regions in the human genome.
Comparison against invariant regions among many human genomes
The human invariant regions with probably HGT phenomenon
Comparison with other existing HGT regions
There were 145 horizontal transfer genes found in Primates in a previous study . We compared our result with these 145 genes and found that very few (5) genes were in both results. Comparing our pipeline with this previous study, we found that both pipelines extracted those human genome regions that show greater conservation with distant species than with the close species. However, in previous articles, the human genes having greater conservation with non-metazoan than metazoan were identified while our pipeline looked for human genome sequences having greater conservation with non-mammals than mammals. In another words, we looked for HGT events happened more recently than those found in the previous studies. Therefore, very few genes were found in both two results.
Horizontal gene transfer in Eukaryotes
According to our previous knowledge of biology, horizontal gene transfer in prokaryotes is a common phenomenon, and the underlying mechanism has been extensively studied. In recent years, the studies of horizontal gene transfer in Eukaryotes has gradually increased, though these findings still remain controversy. At present, these previous studies still have many shortcomings, such as lack of evidences to prove these sequences are indeed derived from the horizontal gene transfer, few studies of underlying mechanism, incapability of finding common features of these HGT regions, and so on.
In this study, we not only identified 1,467 HGT regions in the human genome, but also analyzed the phenomenon of horizontal gene transfer in Eukaryotes. We analyzed the conservation of HGT regions in different Eukaryotic genomes to determine whether these sequences are derived from the horizontal gene transfer or not. The analysis of chromosomal locations of these sequences and repeat contents lead us to find some possible features of these HGT regions. We discovered the genes that had any overlap with our extracted sequences and we found most significant gene functions impact by HGT, by using gene function enrichment analysis. Comparing the phylogenetic tree built by homologous sequences with the species phylogenetic tree, we can predict the process of horizontal gene transfer. Besides, we also discovered the homologous sequences in the common parasite of humans and other eukaryotes. It has been reported that horizontal gene transfer in Eukaryotes need some media species to spread the genomic fragments. And these media species might be intracellular parasitic bacterium (Wolbachia) or some endoparasites (schistosomiasis, Trypanosoma) . One study of Schistosoma genome found that Schistosomiasis share more orthologues with the vertebrates than they do with the ecdysozoans . So the interaction between the host genome and the parasite genome might be a possible step in HGT. We discovered the homologous sequences in the common parasites (Schistosomiasis) of humans and other Eukaryotes, which provided the evidence to prove horizontal gene transfer process we predicted is true.
In general, the majority of the HGT regions discovered by our pipeline is credible. The pipeline we built to analyze horizontal gene transfer in Eukaryotes is also reasonable. According to our previous discussion, we believe that horizontal gene transfer is more common than we expected in the human genome. This study will provide a reference for future study of the horizontal gene transfer in Eukaryotes.
Hundreds of human genes were found to be more conserved with non-mammals than with most mammals. Few of these genes overlapped with known horizontal transferred genes. This indicated that horizontal gene transfer is more common than we expected in the human genome. This study provided insight into potential mechanisms of HGT in the human genome.
Horizontal Gene Transfer
Distance: subtree prune and regraft distance
This work was supported by grants from the National Natural Science Foundation of China [61272250, 61472246 and J1210047]; the National Basic Research Program of China [2013CB956103]; and the National High-Tech R&D Program (863) [2014AA02150 and 2012AA101601]. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Availability of data and materials
All datasets were taken from publicly available websites. All scripts for this paper have been deposited into Github at https://github.com/huangwenze/HGT-in-Human-Genome and are freely available to all users.
CW conceived and designed the project; WH, LT and YL implemented and tested the system; CW, WH, LT, YL, NH and CS analyzed the data; CW, WH, LT and YL wrote the manuscript. All authors read and approved the final manuscript.
The authors declare that they have no competing interests.
Consent for publication
Ethics approval and consent to participate
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Open AccessThis 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.
- Freeman VJ. Studies on the virulence of bacteriophage-infected strains of Corynebacterium diphtheriae. Journal of bacteriology. 1951;61(6):675–88.PubMedPubMed CentralGoogle Scholar
- Syvanen M. Cross-species gene transfer; implications for a new theory of evolution. Journal of theoretical biology. 1985;112(2):333–43.View ArticlePubMedGoogle Scholar
- Jain R, Rivera MC, Lake JA. Horizontal gene transfer among genomes: the complexity hypothesis. Proceedings of the National Academy of Sciences of the United States of America. 1999;96(7):3801–6.View ArticlePubMedPubMed CentralGoogle Scholar
- Barlow M. What antimicrobial resistance has taught us about horizontal gene transfer. Methods in molecular biology. 2009;532:397–411.View ArticlePubMedGoogle Scholar
- Gyles C, Boerlin P. Horizontally transferred genetic elements and their role in pathogenesis of bacterial disease. Veterinary pathology. 2014;51(2):328–40.View ArticlePubMedGoogle Scholar
- Rossi F, Rizzotti L, Felis GE, Torriani S. Horizontal gene transfer among microorganisms in food: current knowledge and future perspectives. Food microbiology. 2014;42:232–43.View ArticlePubMedGoogle Scholar
- Chan CX, Bhattacharya D, Reyes-Prieto A. Endosymbiotic and horizontal gene transfer in microbial eukaryotes: Impacts on cell evolution and the tree of life. Mobile genetic elements. 2012;2(2):101–5.View ArticlePubMedPubMed CentralGoogle Scholar
- Keeling PJ. Role of horizontal gene transfer in the evolution of photosynthetic eukaryotes and their plastids. Methods in molecular biology. 2009;532:501–15.View ArticlePubMedGoogle Scholar
- Pace 2nd JK, Gilbert C, Clark MS, Feschotte C. Repeated horizontal transfer of a DNA transposon in mammals and other tetrapods. Proceedings of the National Academy of Sciences of the United States of America. 2008;105(44):17023–8.View ArticlePubMedPubMed CentralGoogle Scholar
- Crisp A, Boschetti C, Perry M, Tunnacliffe A, Micklem G. Expression of multiple horizontally acquired genes is a hallmark of both vertebrate and invertebrate genomes. Genome biology. 2015;16:50.View ArticlePubMedPubMed CentralGoogle Scholar
- Gilbert C, Cordaux R. Horizontal transfer and evolution of prokaryote transposable elements in eukaryotes. Genome biology and evolution. 2013;5(5):822–32.View ArticlePubMedPubMed CentralGoogle Scholar
- El Baidouri M, Carpentier MC, Cooke R, Gao D, Lasserre E, Llauro C, Mirouze M, Picault N, Jackson SA, Panaud O. Widespread and frequent horizontal transfers of transposable elements in plants. Genome research. 2014;24(5):831–8.View ArticlePubMedPubMed CentralGoogle Scholar
- Walsh AM, Kortschak RD, Gardner MG, Bertozzi T, Adelson DL. Widespread horizontal transfer of retrotransposons. Proceedings of the National Academy of Sciences of the United States of America. 2013;110(3):1012–6.View ArticlePubMedGoogle Scholar
- Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, Baldwin J, Devon K, Dewar K, Doyle M, FitzHugh W, et al. Initial sequencing and analysis of the human genome. Nature. 2001;409(6822):860–921.View ArticlePubMedGoogle Scholar
- Ernst J, Kellis M. Discovery and characterization of chromatin states for systematic annotation of the human genome. Nature biotechnology. 2010;28(8):817–25.View ArticlePubMedPubMed CentralGoogle Scholar
- Ernst J, Kheradpour P, Mikkelsen TS, Shoresh N, Ward LD, Epstein CB, Zhang X, Wang L, Issner R, Coyne M, et al. Mapping and analysis of chromatin state dynamics in nine human cell types. Nature. 2011;473(7345):43–9.View ArticlePubMedPubMed CentralGoogle Scholar
- Kent WJ, Baertsch R, Hinrichs A, Miller W, Haussler D. Evolution’s cauldron: duplication, deletion, and rearrangement in the mouse and human genomes. Proceedings of the National Academy of Sciences of the United States of America. 2003;100(20):11484–9.View ArticlePubMedPubMed CentralGoogle Scholar
- Karolchik D, Barber GP, Casper J, Clawson H, Cline MS, Diekhans M, Dreszer TR, Fujita PA, Guruvadoo L, Haeussler M, et al. The UCSC Genome Browser database: 2014 update. Nucleic acids research. 2014;42(Database issue):D764–770.View ArticlePubMedGoogle Scholar
- Chiaromonte F, Yap VB, Miller W. Scoring pairwise genomic sequence alignments. Pacific Symposium on Biocomputing Pacific Symposium on Biocomputing. 2002;7:115–26.
- Schwartz S, Kent WJ, Smit A, Zhang Z, Baertsch R, Hardison RC, Haussler D, Miller W. Human-mouse alignments with BLASTZ. Genome research. 2003;13(1):103–7.View ArticlePubMedPubMed CentralGoogle Scholar
- Flicek P, Amode MR, Barrell D, Beal K, Billis K, Brent S, Carvalho-Silva D, Clapham P, Coates G, Fitzgerald S, et al. Ensembl 2014. Nucleic acids research. 2014;42(Database issue):D749–755.View ArticlePubMedGoogle Scholar
- da Huang W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nature protocols. 2009;4(1):44–57.View ArticleGoogle Scholar
- da Huang W, Sherman BT, Lempicki RA. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic acids research. 2009;37(1):1–13.View ArticleGoogle Scholar
- Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, Wang Z, Wei G, Chepelev I, Zhao K. High-resolution profiling of histone methylations in the human genome. Cell. 2007;129(4):823–37.View ArticlePubMedGoogle Scholar
- Blanchette M, Kent WJ, Riemer C, Elnitski L, Smit AF, Roskin KM, Baertsch R, Rosenbloom K, Clawson H, Green ED, et al. Aligning multiple genomic sequences with the threaded blockset aligner. Genome research. 2004;14(4):708–15.View ArticlePubMedPubMed CentralGoogle Scholar
- Murphy WJ, Eizirik E, O’Brien SJ, Madsen O, Scally M, Douady CJ, Teeling E, Ryder OA, Stanhope MJ, de Jong WW, et al. Resolution of the early placental mammal radiation using Bayesian phylogenetics. Science. 2001;294(5550):2348–51.View ArticlePubMedGoogle Scholar
- Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular biology and evolution. 2013;30(12):2725–9.View ArticlePubMedPubMed CentralGoogle Scholar
- Hill T, Nordstrom KJ, Thollesson M, Safstrom TM, Vernersson AK, Fredriksson R, Schioth HB. SPRIT: Identifying horizontal gene transfer in rooted phylogenetic trees. BMC evolutionary biology. 2010;10:42.View ArticlePubMedPubMed CentralGoogle Scholar
- Brant SV, Loker ES. Can specialized pathogens colonize distantly related hosts? Schistosome evolution as a case study. PLoS pathogens. 2005;1(3):167–9.View ArticlePubMedGoogle Scholar
- Schaack S, Gilbert C, Feschotte C. Promiscuous DNA: horizontal transfer of transposable elements and why it matters for eukaryotic evolution. Trends in ecology & evolution. 2010;25(9):537–46.View ArticleGoogle Scholar
- Schistosoma japonicum Genome S, Functional Analysis C: The Schistosoma japonicum genome reveals features of host-parasite interplay. Nature 2009, 460(7253):345–351.