A versatile palindromic amphipathic repeat coding sequence horizontally distributed among diverse bacterial and eucaryotic microbes

Abstract

BackgroundIntragenic tandem repeats occur throughout all domains of life and impart functional and structural variability to diverse translation products. Repeat proteins confer distinctive surface phenotypes to many unicellular organisms, including those with minimal genomes such as the wall-less bacterial monoderms, Mollicutes. One such repeat pattern in this clade is distributed in a manner suggesting its exchange by horizontal gene transfer (HGT). Expanding genome sequence databases reveal the pattern in a widening range of bacteria, and recently among eucaryotic microbes. We examined the genomic flux and consequences of the motif by determining its distribution, predicted structural features and association with membrane-targeted proteins.ResultsUsing a refined hidden Markov model, we document a 25-residue protein sequence motif tandemly arrayed in variable-number repeats in ORFs lacking assigned functions. It appears sporadically in unicellular microbes from disparate bacterial and eucaryotic clades, representing diverse lifestyles and ecological niches that include host parasitic, marine and extreme environments. Tracts of the repeats predict a malleable configuration of recurring domains, with conserved hydrophobic residues forming an amphipathic secondary structure in which hydrophilic residues endow extensive sequence variation. Many ORFs with these domains also have membrane-targeting sequences that predict assorted topologies; others may comprise reservoirs of sequence variants. We demonstrate expressed variants among surface lipoproteins that distinguish closely related animal pathogens belonging to a subgroup of the Mollicutes. DNA sequences encoding the tandem domains display dyad symmetry. Moreover, in some taxa the domains occur in ORFs selectively associated with mobile elements. These features, a punctate phylogenetic distribution, and different patterns of dispersal in genomes of related taxa, suggest that the repeat may be disseminated by HGT and intra-genomic shuffling.ConclusionsWe describe novel features of PARCELs (Palindromic Amphipathic Repeat Coding ELements), a set of widely distributed repeat protein domains and coding sequences that were likely acquired through HGT by diverse unicellular microbes, further mobilized and diversified within genomes, and co-opted for expression in the membrane proteome of some taxa. Disseminated by multiple gene-centric vehicles, ORFs harboring these elements enhance accessory gene pools as part of the "mobilome" connecting genomes of various clades, in taxa sharing common niches.

Development of a novel plasmid as a shuttle vector for heterologous gene expression in Mycoplasma yeatsii

“…Interestingly, each of these matches is encoded on genomic islands found in M. mycoides cluster members that exhibit hallmarks of being integrated mobile elements based on strain-variable site of chromosomal integration, presence of genes involved in DNA mobility and detection of extrachromosomal forms for some units. The term Tra Island has been coined for these elements (Röske et al, 2010). All matches were to an ORF of unknown function that is encoded close to one terminus of each island, with greatest similarity to MCAP_0274 (ABC01763), the first ORF of the 43-kb Tra Island I in M. capricolum subsp.…”

Genome of brown tide virus (AaV), the little giant of the Megaviridae, elucidates NCLDV genome expansion and host–virus coevolution

“…S3l). Repeats characterized by DUF285 domains occur sporadically in unicellular microbes, especially in the obligate endosymbiotic class Mollicutes, and also in unicellular photosynthetic eukaryotes (Roske et al, 2010). ORFs containing these domains were termed Palindromic Amphipathic Repeat Coding Elements (PARCELs), characterized by repeating elements displaying dyad symmetry and variable hydrophilic and conserved hydrophobic regions (Roske et al, 2010).…”

“…These ORFs are also found as part of some bacterial mobile elements and plasmids. It has been suggested that PARCELs have spread in diverse bacterial and eukaryotic lineages through HGT and intragenomic shuffling (Roske et al, 2010). The sequence characteristics of PARCELs endow them with potential roles in gene expansion and recombination (Roske et al, 2010).…”

Complete Genome Sequence of Mycoplasma bovis Type Strain PG45 (ATCC 25523)

“…Fifteen of these LP genes (annotated as authentic frameshifts) are in the OFF configuration. Finally, nine LP genes, some having these poly-G or -C tracts, encode DUF285 motifs denoting recently described palindromic amphipathic repeat coding elements (PARCELs) distributed by HGT among diverse bacteria (12), including some Mollicutes (12,13). Analogous systems of variation and chromosomal plasticity occur in M. bovis and M. agalactiae, predicting phenotypic and genotypic instability in populations.…”