Operon Conservation and the Evolution of trans-Splicing in the Phylum Nematoda

Abstract

The nematode Caenorhabditis elegans is unique among model animals in that many of its genes are cotranscribed as polycistronic pre-mRNAs from operons. The mechanism by which these operonic transcripts are resolved into mature mRNAs includes trans-splicing to a family of SL2-like spliced leader exons. SL2-like spliced leaders are distinct from SL1, the major spliced leader in C. elegans and other nematode species. We surveyed five additional nematode species, representing three of the five major clades of the phylum Nematoda, for the presence of operons and the use of trans-spliced leaders in resolution of polycistronic pre-mRNAs. Conserved operons were found in Pristionchus pacificus, Nippostrongylus brasiliensis, Strongyloides ratti, Brugia malayi, and Ascaris suum. In nematodes closely related to the rhabditine C. elegans, a related family of SL2-like spliced leaders is used for operonic transcript resolution. However, in the tylenchine S. ratti operonic transcripts are resolved using a family of spliced leaders related to SL1. Non-operonic genes in S. ratti may also receive these SL1 variants. In the spirurine nematodes B. malayi and A. suum operonic transcripts are resolved using SL1. Mapping these phenotypes onto the robust molecular phylogeny for the Nematoda suggests that operons evolved before SL2-like spliced leaders, which are an evolutionary invention of the rhabditine lineage. The genome of the nematode worm Caenorhabditis elegans was the first of any animal to be completely sequenced. One surprising finding in this worm's genome was that about one-fifth of its genes were organised as sets of from two to eight genes expressed from the same promoter, similar to bacterial “operons.” The pre-mRNAs made from these operons are processed by an intermolecular ligation process called SL trans-splicing. Other animal genomes, such as the human genome or that of the fruit fly contain neither operons nor SL trans-splicing. In this article, Guiliano and Blaxter have investigated whether this curious facet of genome organisation is peculiar to C. elegans and close relatives by examining the genomes of a wide range of parasitic and free-living nematodes. The authors find that both operons and trans-splicing are present across the nematodes, and that operons evolve as other genome features do. All of the species surveyed use trans-splicing to resolve their multigene pre-mRNAs into single-gene mRNAs, but the details differ significantly from the process in C. elegans. In particular, the short piece of RNA that is attached to the beginning of operon-derived mRNAs has changed independently in many nematode groups.