Article,
Loss of Genetic Redundancy in Reductive Genome Evolution
PLOS Computational Biology, 7 (2): e1001082+ (Feb 17, 2011)
DOI: 10.1371/journal.pcbi.1001082
Abstract
Biological systems evolved to be functionally robust in uncertain environments, but also highly adaptable. Such robustness is partly achieved by genetic redundancy, where the failure of a specific component through mutation or environmental challenge can be compensated by duplicate components capable of performing, to a limited extent, the same function. Highly variable environments require very robust systems. Conversely, predictable environments should not place a high selective value on robustness. Here we test this hypothesis by investigating the evolutionary dynamics of genetic redundancy in extremely reduced genomes, found mostly in intracellular parasites and endosymbionts. By combining data analysis with simulations of genome evolution we show that in the extensive gene loss suffered by reduced genomes there is a selective drive to keep the diversity of protein families while sacrificing paralogy. We show that this is not a by-product of the known drivers of genome reduction and that there is very limited convergence to a common core of families, indicating that the repertoire of protein families in reduced genomes is the result of historical contingency and niche-specific adaptations. We propose that our observations reflect a loss of genetic redundancy due to a decreased selection for robustness in a predictable environment. Bacteria have found many niches in which to live, and one of them is inside eukaryotic cells. These intracellular bacteria include endosymbionts like Buchnera aphidicola, which provides its host, an aphid, with essential amino acids, as well as many pathogenic bacteria such as Mycobacterium leprae and Rickettsia prowazekii, the causative agents of leprosy and typhus, respectively. Even though they all evolved their intracellular lifestyle independently, all these bacteria lost a large number of genes as they adapted to their hosts, presumably because the rich environment where they found themselves no longer required such functions. For example, biosynthetic genes are frequently lost. It has been a matter of debate what decides whether a gene can be lost in evolution, and intracellular bacteria have been used as model systems to study these processes. In our study, we propose that when adopting an intracellular lifestyle, these bacteria extensively lost duplicated genes. We propose that this represents loss of copy redundancy that is possible because the host cell represents a predictable environment in which there is little pressure for the bacteria to retain these backups. In simplistic terms, if the road is always smooth, you are probably OK without a spare tire.
