Structural features and the persistence of acquired proteins

Abstract

ORFan genes can constitute a large fraction of a bacterial genome, but due to their lack of homologs, their functions have remained largely unexplored. To determine if particular features of ORFan-encoded proteins promote their presence in a genome, we analyzed properties of ORFans that originated over a broad evolutionary timescale. We also compared ORFan genes to another class of acquired genes (HOPs), which have homologs in other bacteria. A total of 54 ORFan and HOP genes selected from different phylogenetic depths in the Escherichia coli lineage were cloned, expressed, purified and subjected to CD spectroscopy. A majority of genes could be expressed, but only 18 yielded sufficient soluble protein for spectral analysis. Of these, half were significantly α-helical, three were predominantly β-sheet, and six were of intermediate or indeterminate structure. Although a higher proportion of HOPs yielded soluble proteins with resolvable secondary structures, ORFans resembled HOPs with regard to most of the other features tested. Overall, we found that those ORFan and HOP genes that have persisted in the E. coli lineage were more likely to encode soluble and folded proteins, more likely to display environmental modulation of their gene expression, and by extrapolation, are more likely to be functional.

Molecular signatures for the Crenarchaeota and the Thaumarchaeota

“…Unlike the ORFan proteins, which are unique to a given species or strains and are subject to rapid gene loss (Siew and Fischer 2003;Lerat et al 2005), these SPs proteins are distinctive characteristics of all or most species/strains from a given clade, indicating that they are important for these groups (Graham et al 2000;Fang et al 2005;Fang et al 2008;Narra et al 2008;Dutilh et al 2008b;Gao et al 2009). Although the mechanism responsible for the evolution of genes for these proteins is unclear (Dutilh et al 2008b;Kuo and Ochman 2009), their presence in specific clades indicates that their genes first evolved or were introduced in a common ancestor and were retained by its descendents.…”

Microbial systematics in the post-genomics era

“…A vast number of lineage-specific proteins unique to certain species, strain or even genome, which are also called ''ORFans'', are introduced recently during speciation or strain divergence (Daubin and Ochman 2004). Studies have shown that these proteins present at the tips of the phylogeny evolve fast and are subject to loss if not conferring advantages to the host (Narra et al 2008;Kuo and Ochman 2009). However, if the lineage-specific proteins originate deep within a clade and are retained by all the descendents from the progenitor, they are confined to the monophyletic group (Gao et al 2006;Dutilh et al 2008;Gupta and Gao 2010;Gupta and Mathews 2010).…”

“…The sum of both core and noncore genes from different strains of a given species is now referred to as the ''pan-genome'' (Tettelin et al 2008). The non-core genes are postulated to contribute to functions such as niche adaptation, antibiotic resistance and the ability to colonize new hosts (Kuo and Ochman 2009;Narra et al 2008;Coleman and Chisholm 2010;Tettelin et al 2008). Based upon their branching in phylogenetic trees, genomic arrangement and uniquely shared genes/proteins (Touchon et al 2009;Liu et al 1999;Gupta, unpublished results), different strains of some species can be divided into a number of distinct clades.…”

“…Gene transfer provides the bacterial genome with a new set of genes that helps it to explore and adapt to new ecological niches (Kuo and Ochman 2009;Stackebrandt et al 2002;Oren 2010). If the gene transfers occurred at a deeper clade level and the new genes are retained by all the descendants from the progenitor, then the gene transfer events have likely contributed to the divergence of the clade and the new genes are already incorporated into the cellular protein interaction network (Lerat et al 2005;Narra et al 2008;Ragan and Beiko 2009). Besides, the genes acquired via lateral gene transfer over time get ameliorated and many of them exhibit little or no similarity to the original genes and they come to resemble the native genes with regard to characteristics such as their GC content or codon usage (Lawrence and Ochman 1997;Marri and Golding 2008;Koski et al 2001).…”

Phylogenetic Framework and Molecular Signatures for the Main Clades of the Phylum Actinobacteria

“…In contrast to the orphan open reading frame (ORFan) proteins that are specific for particular species or strains and are subject to rapid loss (64,175,265), many proteins of unknown (or even known) functions are unique and distinctive, characteristic of various species from monophyletic clades of different phylogenetic depths (74,98,100,118,130,274). The presence of these proteins in a conserved state in all or most species and strains from these clades, but nowhere else, suggests that the genes for these proteins first evolved in a common ancestor of these clades, followed by their retention by various descendants (74,80,98,100,210). Thus, these proteins represent CSPs that are distinctive characteristics of particular lineages, and they provide useful molecular markers for defining or distinguishing those groups from other bacteria (118).…”