Loss of Genetic Redundancy in Reductive Genome Evolution

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.

A Tribute to Disorder in the Genome of the Bloom-Forming Freshwater Cyanobacterium Microcystis aeruginosa

“…[35]). A contrario , a loss of genetic redundancy in bacteria displaying a reductive genome evolution, as observed in numerous pathogens [36] and in oceanic picocyanobacteria of the genus Prochlorococcus [15], would result in weak selection for robustness, reflecting the fact that these microorganisms live in stable environments. Thus, the unusually high genetic redundancy in the M. aeruginosa genomes might be regarded as an evolutionary strategy that allows this cyanobacterial species to occupy changing environments, such as freshwater ecosystems.…”

Genome Reduction Promotes Increase in Protein Functional Complexity in Bacteria

“…Moreover, the need for moonlighting activities may be exacerbated in pathogens and symbionts, which are predominantly asexual and unable to acquire genetic material horizontally. Although the question of how genome reductions lead to the changes in protein interactions has been explored previously (Ochman et al 2007;Tamames et al 2007;Lercher and Pal 2008;Mendonca et al 2011), this study addresses whether the proteins remaining in reduced genomes are functionally altered or diversifying to compensate for the gene loss. Although the new selective pressures instigated by gene loss can promote the functional diversification of proteins in reduced genomes, the genetic drift experienced by these genomes will also influence the evolution of these proteins, as suggested by a recent hypothesis put forward for evolution of complexity in eukaryotes (Fernandez and Lynch 2011).…”

Bacterial Genome Instability

“…Conversely, genes that are often lost encode proteins involved in cell envelope biogenesis, regulatory systems, metabolism (except for proteins needed for survival), and DNA repair and recombination. Repeated DNA, mobile elements, redundant pathways, and duplicated genes are almost always lost (545). Interestingly, the fact that comparable genome characteristics were visible in the majority of obligate intracellular symbionts and pathogens indicates that similar evolutionary forces led these bacterial genomes in this direction.…”