The dynamic nature of eukaryotic genomes

Abstract

Analyses of diverse eukaryotes reveal that genomes are dynamic, sometimes dramatically so. In numerous lineages across the eukaryotic tree of life, DNA content varies within individuals throughout life cycles and among individuals within species. Discovery of examples of genome dynamism is accelerating as genome sequences are completed from diverse eukaryotes. Though much is known about genomes in animals, fungi, and plants, these lineages represent only 3 of the 60-200 lineages of eukaryotes. Here, we discuss diverse genomic strategies in exemplar eukaryotic lineages, including numerous microbial eukaryotes, to reveal dramatic variation that challenges established views of genome evolution. For example, in the life cycle of some members of the "radiolaria," ploidy increases from haploid (N) to approximately 1,000N, whereas intrapopulation variability of the enteric parasite Entamoeba ranges from 4N to 40N. Variation has also been found within our own species, with substantial differences in both gene content and chromosome lengths between individuals. Data on the dynamic nature of genomes shift the perception of the genome from being fixed and characteristic of a species (typological) to plastic due to variation within and between species.

Figure 1. Distribution of genomic features

Dynamic genomes are widespread across the eukaryotic tree of life. Occurrence of three metrics of genome dynamism are plotted onto our cartoon of the eukaryotic tree of life, the topology of which is derived from our interpretation of multigene genealogies (Parfrey et al. 2006; Rodriguez-Ezpeleta et al. 2007; Yoon et al. Submitted). (p) indicates paraphyly in radiolaria and green algae. Symbols indicate that the feature is reported in at least one taxon within the lineage. ⇑: Somatic polyploidy, ↑↓: Cyclic polyploidy, ◆: Intraspecific genome variation.

Figure 2. Exemplar microbial eukaryotes

Images of microbial organisms discussed reveal morphological diversity in addition to genomic diversity described in the text. Approximate size is give for reference. (a) Uronychia (ciliate) – 150μm, (b) Ammonia (Foraminifera) – 300 μm, (c) Amoeba proteus – 300 μm, (d) Aulacantha (Phaeodarea) – 200 μm, (e) Entamoeba – 25 μm, (f) Giardia – 12 μm. All except d are images of live organisms, d is a drawing from Haeckel (1862) from the library of Kurt Stueber (http://caliban.mpiz-koeln.mpg.de/~stueber/haeckel/radiolarien). All images used with permission from micro*scope (http://starcentral.mbl.edu/microscope/portal.php).

Figure 3. Diversity of nuclear cycles

Depiction of changes in DNA content through the nuclear cycles of nine lineages of eukaryotes. Horizontal axis and colors corresponds to the nuclear cycle stage as shown in the inset diagram, while the vertical axis measure approximate DNA content within the nucleus. Gray shading represents periods of multicellularity or multinuclearity. Inset diagram in panel a is the generalized nuclear cycle as exemplified by plants. Arrows represent progression of genome through karyogamy (red), mitosis as a diploid (blue), meiosis (yellow), and mitosis as a haploid (green). Amitosis in ciliates is black. The nuclear cycle of organisms may include some or all components of the generalized nuclear cycle. A dashed arrow indicates the absence of intervening steps. Panels d and e depict the fate of the somatic genomes, therefore they are dead ends.

Figure 4. Range of intraspecific variation

Individuals within a species (and population) do not have identical genomes. Intraspecific genomes can be different from the level of a few nucleotides, to chromosomes, to ploidy of the whole genome. We plot examples of this variation discussed in the text along a gradient of variation. The number of nucleotides involved increases from left to right.