Faster rates of evolution are linked to tiny genomes, study finds


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Inside every cell lies a genome – a full set of DNA that contains the instructions for building an organism. Across the biological world, genomes show a staggering diversity in size. For example, the genome of the Japanese white flower, Paris japonica, is over 150 billion base pairs, meaning that almost 100 meters of DNA is squeezed into each cell. In comparison, single-celled prokaryotes, like bacteria, have tiny genomes, averaging less than 5 million base pairs. Some prokaryotes have even smaller genomes that are fewer than 500,000 base pairs. But scientists still don’t fully understand the driving forces responsible for reducing the size of genomes.

Faster rates of evolution are linked to tiny genomes, study finds
A microscope image showing Blattabacterium, a species of bacteria that lives inside
the cells of cockroaches and termites [Credit: OIST]

Now, in an international collaboration, led by the Okinawa Institute of Science and Technology Graduate University (OIST) and the University of Sydney, and including researchers from the University of the Ryukyus, the Tokyo Institute of Technology, and RIKEN, scientists have found a link between mutation rate – how quickly the DNA sequence changes – and genome size. Writing in Current Biology, the researchers reported that prokaryotes with higher mutation rates lose genes at a faster pace, and therefore have smaller genomes.

“This was a really surprising result,” said Professor Tom Bourguignon, co-first author of the study and head of the Evolutionary Genomics Unit at OIST. “Currently, the most accepted idea is that population size is the main factor that determines genome size in prokaryotes, particularly in endosymbionts, but our research challenges this view.”

Endosymbionts are organisms that live inside the bodies or cells of other organisms, and typically have much smaller genomes than their free-living counterparts. The Evolutionary Genomics Unit researches an endosymbiont called Blattabacterium, a bacterial species that lives inside cockroaches and termites and provides their hosts with vital nitrogen-containing nutrients. But only a small number of these bacteria are passed on from a mother insect host to a daughter insect host, which keeps their effective population size very low.

“At small population sizes, natural selection is much less effective, and evolution is driven more strongly by chance,” said Dr. Yukihiro Kinjo, co-first author and a postdoctoral scholar from the Evolutionary Genomics Unit. “Without enough selection pressure to maintain specific genes, mutations can arise that inactive and erode these genes, eventually leading to their total loss from the genome.”

While population size as a driving force for genome reduction may be an attractive idea, many free-living prokaryotes that live in larger populations have also evolved smaller genomes, suggesting that it’s only part of the story. Additional explanations have also been proposed but, until now, the mutation rate – or the speed at which evolution occurs – has been overlooked.

In the study, the scientists collected genome data from a diverse range of prokaryotes, including strains from two endosymbiotic lineages and seven free-living lineages.

For each lineage, the team constructed an evolutionary tree that showed how the strains had diverged from each other. With the help of the OIST Biological Complexity Unit, led by Professor Simone Pigolotti, the scientists then created models that reconstructed how gene loss had occurred in each strain. They then estimated the mutation rate, population size and selection pressure for each strain and compared it to the amount of gene loss.

Surprisingly, the scientists did not find a clear link between estimated population size and rate of gene loss. Instead, they found a relationship between mutation rate and gene loss for seven out of the nine lineages studied, with higher mutation rates associated with faster rates of gene loss, resulting in smaller genomes.

“Although we haven’t established a cause, there is a theoretical prediction that explains this observation; if the rate of mutation outweighs a selection pressure to maintain a gene, the gene will be lost from the genome,” said Dr. Kinjo.

The scientists also found clues as to how the gene loss occurred, as strains with smaller genomes had lost genes involved in repairing DNA.

“DNA repair genes fix damaged DNA, so when they are lost the mutation rate of a strain can quickly increase. Most mutations are harmful, so this can quickly inactivate other genes and drive their loss from the genome. If some of these inactivated genes are also involved in DNA repair, this can further accelerate mutation rate and gene loss,” explained Professor Gaku Tokuda, from the University of the Ryukyus.

Although the answers to how gene loss occurs are becoming clearer, whether there are evolutionary reasons behind why prokaryotes increase their rate of mutation to shrink their genome, and if so, what these reasons are, remains an open question.

“Figuring out the evolutionary explanation for what we see is really complicated. It could be that an increased rate of mutation occurs to provide an adaptive advantage, such as the removal of unwanted or unnecessary genes. But we still can’t rule out the possibility that the increased rate of mutation is non-adaptive and due to chance,” said Dr. Kinjo.

Overall, their findings shed new light on the evolution of small genomes, prompting a re-think of the current dominant idea of genome reduction being driven by small population sizes.

“Unlike with population size, our results suggest that mutation rate could drive genome reduction in both free-living and endosymbiotic prokaryotes. This could be the first step in comprehensively understanding what drives changes in genome size across all prokaryotes,” said Prof. Bourguignon.

Source: Okinawa Institute of Science and Technology [August 06, 2020]



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