Patterns of prokaryotic lateral gene transfers affecting parasitic microbial eukaryotes

Abstract

BackgroundThe influence of lateral gene transfer on gene origins and biology in eukaryotes is poorly understood compared with those of prokaryotes. A number of independent investigations focusing on specific genes, individual genomes, or specific functional categories from various eukaryotes have indicated that lateral gene transfer does indeed affect eukaryotic genomes. However, the lack of common methodology and criteria in these studies makes it difficult to assess the general importance and influence of lateral gene transfer on eukaryotic genome evolution.ResultsWe used a phylogenomic approach to systematically investigate lateral gene transfer affecting the proteomes of thirteen, mainly parasitic, microbial eukaryotes, representing four of the six eukaryotic super-groups. All of the genomes investigated have been significantly affected by prokaryote-to-eukaryote lateral gene transfers, dramatically affecting the enzymes of core pathways, particularly amino acid and sugar metabolism, but also providing new genes of potential adaptive significance in the life of parasites. A broad range of prokaryotic donors is involved in such transfers, but there is clear and significant enrichment for bacterial groups that share the same habitats, including the human microbiota, as the parasites investigated.ConclusionsOur data show that ecology and lifestyle strongly influence gene origins and opportunities for gene transfer and reveal that, although the outlines of the core eukaryotic metabolism are conserved among lineages, the genes making up those pathways can have very different origins in different eukaryotes. Thus, from the perspective of the effects of lateral gene transfer on individual gene ancestries in different lineages, eukaryotic metabolism appears to be chimeric.

An archaeal origin of eukaryotes supports only two primary domains of life

“…That composite nature has been confirmed by comparative genomics, which has demonstrated that eukaryotic genomes contain a mixture of genes with different origins 13,[62][63][64][65][66] . Some genes are ancestrally present in all three groups or unique to eukaryotes, but many others appear to have origins through gene transfers from different Bacteria, including the endosymbiotic progenitors of mitochondria and plastids, and relatively few-including the core set of conserved proteins we have been discussing-have affinities with the Archaea.…”

“…The sequencing of genomes from across the tree of eukaryotes is beginning to provide a clearer picture of the impact on eukaryotic genomes of HGT from prokaryotes 65 . These data suggest that the acquisition of bacterial genes, at least by microbial eukaryotes, has been an ongoing RESEARCH REVIEW process that extends beyond the initial injection of genes provided by the mitochondrial and plastid endosymbionts.…”

“…Moreover, recent experiments have indicated that artificial membranes containing mixtures of bacterial and archaeal lipids are stable 99 , demonstrating the potential for natural mixed-membrane intermediate stages. Given these considerations, the reversion to bacterialtype membranes in eukaryotes might be explained as part of the same process whereby ancestral archaeal pathways were replaced by bacterial equivalents to yield the metabolic similarities observed between Bacteria and contemporary eukaryotes [62][63][64][65]95,96,100 . This transition need not have greatly affected membrane function: in the Haloarchaea, which have obtained a large number of bacterial genes by HGT, transporters derived from Bacteria appear to function normally in the archaeal plasma membrane 101 .…”

The biology of Trichomonas vaginalis in the light of urogenital tract infection

“…The Trichomonas BspA family is otherwise quite diverse and includes members with and without transmembrane domains (193 and 718, respectively), and whose length varies from about only 150 to more than 800 amino acids. The BspA protein family appears of bacterial origin and represents a rare example of a massive lateral gene transfer (LGT) event from prokaryote to eukaryote and it might be a consequence of the parasite actively feeding on host microbiota [49,60]. Other enzymes that also potentially trace back to LGT events include many glycantargeting enzymes such as ␤-galactosidase, ␣-and ␤-mannosidase or glucosylceramidase and are thought to be involved in mucin and other human glycan degradation [35].…”

Horizontally acquired genes in early-diverging pathogenic fungi enable the use of host nucleosides and nucleotides

“…Prior analysis of microsporidian genomes demonstrated that, like other microbial eukaryotes, this phylum of fungi has obtained multiple genes through HGT (20), which may have provided a portion of the raw material required for adaptation, as seen in other organisms (21). Known HGT events into Microsporidia include the following: (i) the ADP/ATP translocase gene family, originating from an HGT event that transferred the founding gene from a member of the bacterial phylum Chlamydia (10), which are known to steal energy-bearing molecules from their host; (ii) a sixgene folate synthesis pathway transferred into Encephalitozoon hellem from multiple donors, a transfer hypothesized to reduce host metabolic stress (11); and (iii) the acquisition of a glutamateammonia ligase from an unknown prokaryotic source by Spraguea lophii, which is thought to provide spores a mechanism for defense against the ammonia generated by the decomposing flesh in which they are embedded (12).…”