"Structure, Function and Evolution of the Nematode Genome"
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Structure, Function and Advanced article Evolution of The Article Contents . Introduction Nematode Genome . Main Text Online posting date: 15th February 2013 Christian Ro¨delsperger, Max Planck Institute for Developmental Biology, Tuebingen, Germany Adrian Streit, Max Planck Institute for Developmental Biology, Tuebingen, Germany Ralf J Sommer, Max Planck Institute for Developmental Biology, Tuebingen, Germany In the past few years, an increasing number of draft gen- numerous variations. In some instances, multiple alter- ome sequences of multiple free-living and parasitic native forms for particular developmental stages exist, nematodes have been published. Although nematode most notably dauer juveniles, an alternative third juvenile genomes vary in size within an order of magnitude, com- stage capable of surviving long periods of starvation and other adverse conditions. Some or all stages can be para- pared with mammalian genomes, they are all very small. sitic (Anderson, 2000; Community; Eckert et al., 2005; Nevertheless, nematodes possess only marginally fewer Riddle et al., 1997). The minimal generation times and the genes than mammals do. Nematode genomes are very life expectancies vary greatly among nematodes and range compact and therefore form a highly attractive system for from a few days to several years. comparative studies of genome structure and evolution. Among the nematodes, numerous parasites of plants and Strikingly, approximately one-third of the genes in every animals, including man are of great medical and economic sequenced nematode genome has no recognisable importance (Lee, 2002). From phylogenetic analyses, it can homologues outside their genus. One observes high rates be concluded that parasitic life styles evolved at least seven of gene losses and gains, among them numerous examples times independently within the nematodes (four times with of gene acquisition by horizontal gene transfer. Not only animals and three times with plants as hosts) (Blaxter et al., does the ‘gene for parasitism’ not exist, but also there 1998). This raises the question whether the different tran- sitions to a parasitic life style were paralleled by similar appear to be no common genomic characteristics of changes in the genomes. Should this be the case, it would be parasitic nematode genomes which would distinguish indicative for strong genomic constraints for the switch of them from genomes of free-living nematodes. life styles. Alternatively, if there are many ways to para- sitism, one would expect that there are no unifying genomic features among independent cases of parasitism. A switch Introduction from a fully free-living to a parasitic life style in one step appears highly unlikely. It is, therefore, generally accepted Nematodes are the largest animal phylum. But, out of the that prior to the transition to parasitism, so-called ‘pre- estimated number of 1–10 million species, only approxi- adaptations’ must have existed. These features evolved for mately 25 000 are formally described (Lambshead, 1993). entirely different reasons but later on facilitated the step to Next to their species richness, their ecological omni- parasitism (Dieterich and Sommer, 2009; Osche, 1962; presence in virtually all terrestrial and aquatic habitats and Poulin, 2007). Indeed, many nematodes spend at least a also their high number of individuals contribute to the part of their lives in association with other organisms importance of nematodes (Floyd et al., 2002; Lambshead, without being parasitic (Lee, 2002). These associations 1993). See also: Nematoda (Roundworms) range from short-term, rather unspecific, so-called phoretic Generally, nematodes develop through an embryonic interactions to highly species-specific long-term associ- stage followed by four developmental stages interchange- ations (Dieterich and Sommer, 2009; Poulin, 2007). Fre- ably called larval (L1–L4) or juvenile (J1–J4), which are quently, the dauer juveniles are the developmental stage, separated by molts (Lee, 2002). This life cycle exists in which engages in the interaction. In the example of the genus Pristionchus, they associate in a species-specific eLS subject area: Evolution & Diversity of Life manner with scarab beetles and only resume development after the death of the beetle (necromenic association) How to cite: (Sommer and Ogawa, 2011). The hypothesis that at least Ro¨delsperger, Christian; Streit, Adrian; and Sommer, Ralf J (February for some parasitic nematodes the infective stages are 2013) Structure, Function and Evolution of The Nematode Genome. homologous to the dauer juveniles in free-living nematodes In: eLS. John Wiley & Sons, Ltd: Chichester. is supported by empirical evidence (Ogawa et al., 2009; DOI: 10.1002/9780470015902.a0024603 Wang et al., 2009). Therefore, the ability to form dauer eLS & 2013, John Wiley & Sons, Ltd. www.els.net 1 Structure, Function and Evolution of The Nematode Genome juveniles and phoretic and necromenic interactions might Below are briefly introduced those nematode species for have served as preadaptations for the evolution of para- which whole genome draft sequences were published at the sitism because they allowed a stepwise formation of tight time when this article was written (August, 2012). For this and specific interactions (Dieterich and Sommer, 2009) review the authors limit themselves to the discussion of prior to the transition to a truly parasitic life style. these published genome sequences. Additionally, almost One of the best studied model organisms, the free-living complete genomes are in the process of being analysed and worm Caenorhabditis elegans belongs to the nematodes annotated and are available from various institutions (Community). With the extensive knowledge about C. (see http://www.nematodes.org/nematodegenomes/index. elegans as an excellent base line, nematodes are becoming php/959_Nematode_Genomes). The life cycles and the increasingly popular for evolutionary studies (Sommer, basic biology of the different nematodes are described in 2009). C. elegans was the first multicellular organism that numerous textbooks. (For space restriction, the infor- had its genome sequenced in 1998 (C. elegans Sequencing mation presented below is without references; the reader is Consortium, 1998). It is important to note that until today, advised to refer the literature used to compile it (Anderson, C. elegans is the only metazoan with a fully sequenced 2000; Castagnone-Sereno, 2006; Community; Eckert et al., genome in the sense that there are no sequence gaps left. 2005; Lee, 2002; Riddle et al., 1997; Wenk and Renz, 2003; Recently, draft genome sequences of multiple other free- Zhao et al., 2008 and the respective genome publications, living and parasitic nematodes were published and their Table 1).) To illustrate the differences between nematodes, number is increasing rapidly (http://www.nematodes.org/ for each species numbers for the size of the adult, minimal nematodegenomes/index.php/959_Nematode_Genomes). generation time and adult reproductive life span are pro- See also: Caenorhabditis elegans as an Experimental vided. These numbers are to be taken as ballpark figures Organism; Caenorhabditis elegans Genome Project only because the published numbers often vary consider- In combination with the excellent understanding of ably between different sources. The phylogenetic clade the phylogenetic relationship of the species in question listed is according to Blaxter et al. (1998). (Blaxter et al., 1998; Holterman et al., 2006; Figure 1), these genome sequences are a yielding source for the investi- Free-living nematodes gation of the structure and evolution of genomes. Among nematodes, examples of phylogenetically very closely C. elegans, Caenorhabditis briggsae, Caenorhabditis related species that have completely different ecologies and angaria and Pristionchus pacificus (all clade V) species with very similar ecologies that are, however, only very distantly related are found. This makes nematodes an Adult length: 1 mm long (hermaphrodite/female, males attractive system to study how genomes are shaped by the slightly smaller) environment and evolutionary descent. Minimal generation time: 3–4 days Taxonomic groups Species with sequenced genome Rhabditida Caenorhabditis elegans, C. briggsae, C. angaria Rhabditina V Diplogasterida Pristionchus pacificus Tylenchida Meloidogyne incognita, M. hapla Tylenchina IV Apchelenchida Bursaphelenchus xylophilus Ascardiomorpha Ascaris suum Spiruina III Spiruromorpha Brugia malayi Other chromatodera EnopliaII DorylaimaI Trichocephalida Trichinella spiralis Figure 1 Phylogenetic relationship of the nematodes with published genome sequences. The phylogeny follows Blaxter et al. (1998). Roman numerals denote the clade. 2 eLS & 2013, John Wiley & Sons, Ltd. www.els.net Table 1 Summary statistics of nematode genomes. Overview of genomic features for 10 nematode genome assemblies. Numbers differ from the original publications as they were recomputed from genome assemblies and gene annotations from wormbase (www.wormbase.org) release WS230. The program mreps 2.5 was used for repeat annotation Species C. elegans C. briggsae C. angaria P. pacificus B. malayi M. hapla M. incognita B. xylophilus A. suum T. spiralis eLS Assembly size (Mb) 100.3 105.4 79.7 153.2 89.3 53.0 82.1 73.1 265.3 58.5 & 2013, John Wiley & Sons, Ltd. www.els.net Number of scaffolds 7 12 33 559 18 083 27 210 3452 9538 5527 29 831 6863 N50 scaffold size (Mb) 17.5 17.5 0.01 1.2 0.04 0.3 0.1 1.0 0.4 6.4 GC content (%) 35.4 37.3