The Complex Intron Landscape and Massive Intron Invasion in a Picoeukaryote Provides Insights into Intron Evolution

Abstract

Genes in pieces and spliceosomal introns are a landmark of eukaryotes, with intron invasion usually assumed to have happened early on in evolution. Here, we analyze the intron landscape of Micromonas, a unicellular green alga in the Mamiellophyceae lineage, demonstrating the coexistence of several classes of introns and the occurrence of recent massive intron invasion. This study focuses on two strains, CCMP1545 and RCC299, and their related individuals from ocean samplings, showing that they not only harbor different classes of introns depending on their location in the genome, as for other Mamiellophyceae, but also uniquely carry several classes of repeat introns. These introns, dubbed introner elements (IEs), are found at novel positions in genes and have conserved sequences, contrary to canonical introns. This IE invasion has a huge impact on the genome, doubling the number of introns in the CCMP1545 strain. We hypothesize that each IE class originated from a single ancestral IE that has been colonizing the genome after strain divergence by inserting copies of itself into genes by intron transposition, likely involving reverse splicing. Along with similar cases recently observed in other organisms, our observations in Micromonas strains shed a new light on the evolution of introns, suggesting that intron gain is more widespread than previously thought.

A survey of transposable element classification systems – A call for a fundamental update to meet the challenge of their diversity and complexity

“…In order to allow splicing most of them have GT-AG donor and an acceptor site ends as well as a predicted branch point motif followed by a polypyrimidine tract (van der Burgt et al, 2012). Some display unusual GT-TG ends that have been reported in other species including human (Verhelst et al, 2013). These hallmark features support the conclusion that ILEs splice using a branched lariat RNA intermediate.…”

“…300 bps. A few bigger ILEs (>2000 bps) are also present (Verhelst et al, 2013). These sequences have no strict insertion target sequence.…”

“…However, even if these enzymes perform the reverse transcription into DNA of mRNA containing newly inserted ILE they cannot be considered as being SINEs. Indeed, their features (absence of similarity of their 3 0 end with that of a known LINE; absence of target site duplication at the insertion site; insertion in a single orientation only into transcribed gene regions) indicate a putative mechanism of integration into genes different from that of known SINEs that use LINE machinery to transpose into metazoan chromosomes (Vassetzky and Kramerov, 2013;Collemare et al, 2013;Verhelst et al, 2013).…”

“…It appears therefore that group II introns and ILEs are two types of TEs that might use similar integration pathways (Yenerall and Zhou, 2012;Collemare et al, 2013;Verhelst et al, 2013). This conclusion is supported even if: (1) the RT used for their mobility is unrelated, (2) there are no similarities between the intrastrand dyadic structures of their ends, and (3) their ability to splice from an mRNA via a branched lariat RNA intermediate raises questions about their evolutionary relationships.…”

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“…Comparative analyses of discordant intron positions among conserved homologous genes have been carried out in diverse eukaryotic lineages. Although intron gains are generally reported at a lower frequency than intron losses, the reported intron gains have been accumulated to a considerable number (Csuros et al 2011;Fablet et al 2009;Hooks et al 2014;Irimia & Roy 2014;Li et al 2014;Roy & Gilbert 2005;Roy & Penny 2006;Torriani et al 2011;van der Burgt et al 2012;Verhelst et al 2013;Yenerall et al 2011;Yenerall & Zhou 2012;Zhu & Niu 2013a). Unfortunately, the source sequences of most of these reported intron gains have not been identified.…”