Oxytricha as a modern analog of ancient genome evolution

Abstract

Several independent lines of evidence suggest that the modern genetic system was preceded by the ‘RNA world’ in which RNA genes encoded RNA catalysts. Current gaps in our conceptual framework of early genetic systems make it difficult to imagine how a stable RNA genome may have functioned and how the transition to a DNA genome could have taken place. Here we use the single-celled ciliate, Oxytricha, as an analog to some of the genetic and genomic traits that may have been present in organisms before and during the establishment of a DNA genome. Oxytricha and its close relatives have a unique genome architecture involving two differentiated nuclei, one of which encodes the genome on small, linear nanochromosomes. While its unique genomic characteristics are relatively modern, some physiological processes related to the genomes and nuclei of Oxytricha may exemplify primitive states of the developing genetic system.

GENOME STRUCTURE DRIVES PATTERNS OF GENE FAMILY EVOLUTION IN CILIATES, A CASE STUDY USINGCHILODONELLA UNCINATA(PROTISTA, CILIOPHORA, PHYLLOPHARYNGEA)

“…The new zygotic nucleus divides by mitosis and then develops into either a micronucleus or a somatic macronucleus. The macronucleus is transformed through a series of chromosomal rearrangements, including fragmentation, elimination of internal excised sequences, and amplification (Prescott 1994;Katz 2001;Riley and Katz 2001;Katz et al 2003;Chalker 2008;Heyse et al 2010;Chalker and Yao 2011;Nowacki et al 2011;Goldman and Landweber 2012). Gene scrambling, the presence of fragmented coding domains (termed macronuclear destined sequences) in noncanonical order in the micronucleus, has been described in ciliates from two classes, Spirotrichea (Prescott and Greslin 1992;Curtis and Landweber 1999;Nowacki and Landweber 2009) and Phyllopharyngea (represented by Chilodonella uncinata, Katz and Kovner 2010).…”

Emerging Frontiers in the Study of Molecular Evolution

“…Though the results of these studies sometimes disagree in their particulars (Becerra et al 2007;Goldman et al 2013), they portray a LUCA that had a complete translation system similar to those we see in extant organisms (Harris et al 2003;Goldman et al 2010;Fournier et al 2011) and a complex metabolic networks composed of protein enzymes (Braakman and Smith, 2012;Goldman et al , 2016Weiss et al 2016). LUCA also likely had a DNA genome (Forterre 2002;Goldman and Landweber 2012;Poole et al 2014) and cell membrane (Martin and Russell 2003;Peretó et al 2004), although these features are less certain since many proteins that support the DNA genome are not homologous between Bacteria and Archaea. Further, archaeal phospholipids have a different structure than bacterial and eukaryotic phospholipids.…”

Genomes on the Edge: Programmed Genome Instability in Ciliates

“…Such an interaction would also prevent transposons from integrating into the somatic genome, thereby keeping the MAC transposon free. Transmission of heritable information via RNA, rather than directly through DNA, may more generally help exclude DNA transposons from the new somatic genome (Goldman and Landweber, 2012). …”

“…A recurring theme of ciliate biology is the role of RNA as the driver in nucleic acid metabolism (Goldman and Landweber, 2012). Examples include myriad roles of long, noncoding RNAs (Chalker et al, 2005; Chalker and Yao, 2001; Heyse et al, 2010; Lepère et al, 2008; Nowacki et al, 2008, 2010) and small RNAs in the form of scanRNAs (Kataoka and Mochizuki, 2011; Lepère et al, 2009; Schoeberl et al, 2012) and piRNAs (Fang et al, 2012; Zahler et al, 2012) and their interaction.…”