Top Ten Genomes – (ii) Dynamically Changing Genomes

This week we are talking about highly unusual genomes, and started the discussion with lamprey in the previous commentary. One interesting property of the lamprey genome, if you remember, is its ability to dynamically shrink during the phases of development. The genome programmatically chops off about 20% of it, when lamprey grows from germ line to more complex multi-cellular organism. This removal not only affects junk dna, but also deletes coding genes.

That raises the question - how did lamprey genome evolve to programmatically get rid of parts of its chromosomes? How many other genomes have the same ability? The answer to the first question is not known, but on the second one

• plenty of other eukaryotic genomes can dynamically change size. Professor Laura Katz and collaborators put together two wonderful papers compiling a large list of several dynamically changing genomes.

The Dynamic Nature of Eukaryotic Genomes

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 60200 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.

-————————————

The Dynamic Nature of Genomes across the Tree of Life

Genomes are dynamic in lineages across the tree of life. Among bacteria and archaea, for example, DNA content varies throughout life cycles, and nonbinary cell division in diverse lineages indicates the need for coordination of the inheritance of genomes. These observations contrast with the textbook view that bacterial and archaeal genomes are monoploid (i.e., single copied) and fixed both within species and throughout an individuals lifetime. Here, we synthesize information on three aspects of dynamic genomes from exemplars representing a diverse array of bacterial and archaeal lineages: 1) ploidy level variation, 2) epigenetic mechanisms, and 3) life cycle variation. For example, the Euryarchaeota analyzed to date are all polyploid, as is the bacterium Epulopiscium that contains up to tens of thousands of copies of its genome and reproduces by viviparity. The bacterium Deinococcus radiodurans and the archaeon Halobacterium sp. NRC-1 can repair a highly fragmented genome within a few hours. Moreover, bacterial genera such as Dermocarpella and Planctomyces reproduce by fission (i.e., generating many cells from one cell) and budding, highlighting the need for regulation of genome inheritance in these lineages. Combining these data with our previous work on widespread genome dynamics among eukaryotes, we hypothesize that dynamic genomes are a rule rather than the exception across the tree of life. Further, we speculate that all domains may have the ability to distinguish germline from somatic DNA and that this ability may have been present the last universal common ancestor.

Their widespread existence changes the current view of genomes being static entities. In fact, even those genomes known to be static may change size, as Eric Haag discovered in case of worm. We covered his work last year and here were a few comments he made on his observations.

1. Its important to understand that I discussed quite a number of different species in my talk, all of which are the genus Caenorhabditis, but only one of which was C. elegans.

2. The deletions I discussed happened in the recent evolutionary history of C. elegans, C. briggsae, and other less-studied species, all united (we think) only by having adopted a self-fertile hermaphrodite mode of sex. Philosophically Im not sure when to say the deletions occurred with respect to taxonomy (i.e. was the pre-hermaphroditic C. elegans ancestor already C. elegans or something else? But hopefully you get the point: C. elegans, as conventionally defined as an extant taxon, is already shrunken.

3. The deletions shouldnt be characterized as programmed, because that implies precisely regulated and highly predictable loss, and we dont have evidence for that. What we do have is evidence for loss that is predictable in quantity and to a lesser extent by broad chromosomal domain (i.e. more in the ends, less in the middle). These features are probably due to the interaction of stochastic mutational events (which may have certain biases) and the landscape of genetic redundancy at the time the lineage switches to self- fertility.

The genome shrinkage stuff was part of a set of vignettes related to the

consequences of becoming a self-fertile hermaphrodite. I mentioned genome shrinkage (the issue above), deregulation of sex-biased gene expression, and increased vulnerability to harm by mating with obligately outcrossing relatives. I summarized that half of the talk by suggesting that these consequences eventually slam the door on returning to an outcrossing mode of reproduction, and make selfing species more subject to extinction when the environment changes.

I can also summarize the first part of the talk as being about how independently evolved hermaphroditic species, C. elegans and C. briggsae, have both repeated and idiosyncratic aspects to the way they regulate the key trait that makes that possibleXX sperm production. That was based to a large extent on work from my lab, but also with major contributions from the groups of Judith Kimble, Tim Schedl, Ron Ellis, and David Pilgrim (who was also a meeting co-organizer).

The belief that the genomes are static is widespread. Eric Haag mentioned that the sequencing centers did not pay attention to him at first, when he pointed out the possibility of worm genomes dynamically changing size. Therefore, we pick the entire class of dynamically changing genomes as the second candidate in the top ten genome list.