The transferome of metabolic genes explored: analysis of the horizontal transfer of enzyme encoding genes in unicellular eukaryotes

Background  

Metabolic networks are responsible for many essential cellular processes, and exhibit a high level of evolutionary conservation from bacteria to eukaryotes. If genes encoding metabolic enzymes are horizontally transferred and are advantageous, they are likely to become fixed. Horizontal gene transfer (HGT) has played a key role in prokaryotic evolution and its importance in eukaryotes is increasingly evident. High levels of endosymbiotic gene transfer (EGT) accompanied the establishment of plastids and mitochondria, and more recent events have allowed further acquisition of bacterial genes. Here, we present the first comprehensive multi-species analysis of E/HGT of genes encoding metabolic enzymes from bacteria to unicellular eukaryotes.     

The origins and early evolution of DNA mismatch repair genes--multiple horizontal gene transfers and co-evolution

To understand the evolutionary process of the DNA mismatch repair system, we conducted systematic phylogenetic analysis of its key components, the bacterial MutS and MutL genes and their eukaryotic homologs. Based on genome-wide homolog searches, we identified three new MutS subfamilies (MutS3-5) in addition to the previously studied MutS1 and MutS2 subfamilies. Detailed evolutionary analysis strongly suggests that frequent ancient horizontal gene transfer (HGT) occurred with both MutS and MutL genes from bacteria to eukaryotes and/or archaea. Our results further imply that the origins of mismatch repair system in eukaryotes and archaea are largely attributed to ancient HGT from bacteria instead of vertical evolution. Specifically, the eukaryotic MutS and MutL homologs likely originated from endosymbiotic ancestors of mitochondria or chloroplasts, indicating that not only archaea, but also bacteria are important sources of eukaryotic DNA metabolic genes. The archaeal MutS1 and MutL homologs were also acquired from bacteria simultaneously through HGT. Moreover, the distribution and evolution profiles of the MutS1 and MutL genes suggest that they have undergone long-term coevolution. Our work presents an overall portrait of the evolution of these important genes in DNA metabolism and also provides further understanding about the early evolution of cellular organisms.     

Ancient gene transfer from algae to animals: Mechanisms and evolutionary significance

ABSTRACT: BACKGROUND: Horizontal gene transfer (HGT) is traditionally considered to be rare in multicellular eukaryotes such as animals. Recently, many genes of miscellaneous algal origins were discovered in choanoflagellates. Considering that choanoflagellates are the existing closest relatives of animals, we speculated that ancient HGT might have occurred in the unicellular ancestor of animals and affected the long-term evolution of animals. RESULTS: Through genome screening, phylogenetic and domain analyses, we identified 14 gene families, including 92 genes, in the tunicate Ciona intestinalis that are likely derived from miscellaneous photosynthetic eukaryotes. Almost all of these gene families are distributed in diverse animals, suggesting that they were mostly acquired by the common ancestor of animals. Their miscellaneous origins also suggest that these genes are not derived from a particular algal endosymbiont. In addition, most genes identified in our analyses are functionally related to molecule transport, cellular regulation and methylation signaling, suggesting that the acquisition of these genes might have facilitated the intercellular communication in the ancestral animal. CONCLUSIONS: Our findings provide additional evidence that algal genes in aplastidic eukaryotes are not exclusively derived from historical plastids and thus important for interpreting the evolution of eukaryotic photosynthesis. Most importantly, our data represent the first evidence that more anciently acquired genes might exist in animals and that ancient HGT events have played an important role in animal evolution.     

Horizontal gene transfer in plants

Horizontal gene transfer (HGT) has played a major role in bacterial evolution and is fairly common in certain unicellular eukaryotes. However, the prevalence and importance of HGT in the evolution of multicellular eukaryotes remain unclear. Recent studies indicate that plant mitochondrial genomes are unusually active in HGT relative to all other organellar and nuclear genomes of multicellular eukaryotes. Although little about the mechanisms of plant HGT is known, several studies have implicated parasitic plants as both donors and recipients of mitochondrial genes. Most cases uncovered thus far have involved a single transferred gene per species; however, recent work has uncovered a case of massive HGT in Amborella trichopoda involving acquisition of at least a few dozen and probably hundreds of foreign mitochondrial genes. These foreign genes came from multiple donors, primarily eudicots and mosses. This review will examine the implications of such massive transfer, the potential mechanisms and consequences of plant-to-plant mitochondrial HGT in general, as well as the limited evidence for HGT in plant chloroplast and nuclear genomes.     

Horizontal gene transfer in the innovation and adaptation of land plants

Horizontal gene transfer (HGT) has been well documented in prokaryotes and unicellular eukaryotes, but its role in plants and animals remains elusive. In a recent study, we showed that at least 57 families of nuclear genes in the moss Physcomitrella patens were acquired from prokaryotes, fungi or viruses and that HGT played a critical role in plant colonization of land. In this paper, we categorize all acquired genes based on their putative functions and biological processes, and further address the importance of HGT in plant innovation and evolution.     

Does complexity constrain organelle evolution?

The evolution of eukaryotes was punctuated by invasions of the bacteria that have evolved to mitochondria and plastids. These bacterial endosymbionts founded major eukaryotic lineages by enabling them to carry out aerobic respiration and oxygenic photosynthesis. Yet, having evolved as free-living organisms, they were at first poorly adapted organelles. Although mitochondria and plastids have integrated within the physiology of eukaryotic cells, this integration has probably been constrained by the high level of complexity of their bacterial ancestors and the inability of gradual evolutionary processes to drastically alter complex systems. Here, I review complex processes that directly involve translation of plastid mRNAs and how they could constrain transfer to the nucleus of the genes encoding them.     

The scale and evolutionary significance of horizontal gene transfer in the choanoflagellate Monosiga brevicollis

Background

It is generally agreed that horizontal gene transfer (HGT) is common in phagotrophic protists. However, the overall scale of HGT and the cumulative impact of acquired genes on the evolution of these organisms remain largely unknown.

Results

Choanoflagellates are phagotrophs and the closest living relatives of animals. In this study, we performed phylogenomic analyses to investigate the scale of HGT and the evolutionary importance of horizontally acquired genes in the choanoflagellate Monosiga brevicollis. Our analyses identified 405 genes that are likely derived from algae and prokaryotes, accounting for approximately 4.4% of the Monosiga nuclear genome. Many of the horizontally acquired genes identified in Monosiga were probably acquired from food sources, rather than by endosymbiotic gene transfer (EGT) from obsolete endosymbionts or plastids. Of 193 genes identified in our analyses with functional information, 84 (43.5%) are involved in carbohydrate or amino acid metabolism, and 45 (23.3%) are transporters and/or involved in response to oxidative, osmotic, antibiotic, or heavy metal stresses. Some identified genes may also participate in biosynthesis of important metabolites such as vitamins C and K12, porphyrins and phospholipids.

Conclusions

Our results suggest that HGT is frequent in Monosiga brevicollis and might have contributed substantially to its adaptation and evolution. This finding also highlights the importance of HGT in the genome and organismal evolution of phagotrophic eukaryotes.

Electronic supplementary material

The online version of this article (doi:10.1186/1471-2164-14-729) contains supplementary material, which is available to authorized users.     

植物中的水平基因转移

水平基因转移是不通过生殖而进行的遗传物质交流, 在原核生物和单细胞真核生物的进化中起着重要作用。然而, 水平基因转移在多细胞真核生物之间的发生频率以及对多细胞真核生物进化的影响尚不明确。近期的一些研究显示, 水平基因转移在高等植物之间以及高等植物和其它生物之间普遍存在。该文将对高等植物中已发现的一些水平基因转移现象进行综述, 并尝试解析植物之间水平基因转移可能的机制及其重要意义。     

Horizontally Acquired Cellulases Assist the Expansion of Dietary Range in Pristionchus Nematodes

Horizontal gene transfer (HGT) enables the acquisition of novel traits via non-Mendelian inheritance of genetic material. HGT plays a prominent role in the evolution of prokaryotes, whereas in animals, HGT is rare and its functional significance is often uncertain. Here, we investigate horizontally acquired cellulase genes in the free-living nematode model organism Pristionchus pacificus. We show that these cellulase genes 1) are likely of eukaryotic origin, 2) are expressed, 3) have protein products that are secreted and functional, and 4) result in endo-cellulase activity. Using CRISPR/Cas9, we generated an octuple cellulase mutant, which lacks all eight cellulase genes and cellulase activity altogether. Nonetheless, this cellulase-null mutant is viable and therefore allows a detailed analysis of a gene family that was horizontally acquired. We show that the octuple cellulase mutant has associated fitness costs with reduced fecundity and slower developmental speed. Furthermore, by using various Escherichia coli K-12 strains as a model for cellulosic biofilms, we demonstrate that cellulases facilitate the procurement of nutrients from bacterial biofilms. Together, our analysis of cellulases in Pristionchus provides comprehensive evidence from biochemistry, genetics, and phylogeny, which supports the integration of horizontally acquired genes into the complex life history strategy of this soil nematode.     

Patterns of prokaryotic lateral gene transfers affecting parasitic microbial eukaryotes

Background

The 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.

Results

We 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.

Conclusions

Our 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.     

Speciation in <Emphasis Type="Italic">Chlamydia</Emphasis>: Genomewide Phylogenetic Analyses Identified a Reliable Set of Acquired Genes

Horizontal gene transfer (HGT), a process through which genomes acquire sequences from distantly related organisms, is believed to be a major source of genetic diversity in bacteria. A central question concerning the impact of HGT on bacterial genome evolution is the proportion of horizontally transferred sequences within genomes. This issue, however, remains unresolved because the various methods developed to detect potential HGT events identify different sets of genes. The present-day consensus is that phylogenetic analysis of individual genes is still the most objective and accurate approach for determining the occurrence and directionality of HGT. Here we present a genome-scale phylogenetic analysis of protein-encoding genes from five closely related Chlamydia, identifying a reliable set of sequences that have arisen via HGT since the divergence of the Chlamydia lineage. According to our knowledge, this is the first systematic phylogenetic inference-based attempt to establish a reliable set of acquired genes in a bacterial genome. Although Chlamydia are obligate intracellular parasites of higher eukaryotes, and thus suspected to be isolated from HGT more than the free-living species, our results show that their diversification has involved the introduction of foreign sequences into their genome. Furthermore, we also identified a complete set of genes that have undergone deletion, duplication, or rearrangement during this evolutionary period leading to the radiation of Chlamydia species. Our analysis may provide a deeper insight into how these medically important pathogens emerged and evolved from a common ancestor.     

A cryptic algal group unveiled: a plastid biosynthesis pathway in the oyster parasite Perkinsus marinus

Plastids are widespread in plant and algal lineages. They are also exploited by some nonphotosynthetic protists, including malarial parasites, to support their diverse modes of life. However, cryptic plastids may exist in other nonphotosynthetic protists, which could be important in studies on the diversity and evolution of plastids. The parasite Perkinsus marinus, which causes mass mortality in oyster farms, is a nonphotosynthetic protist that is phylogenetically related to plastid-bearing dinoflagellates and apicomplexans. In this study, we searched for P. marinus methylerythritol phosphate (MEP) pathway genes, responsible for de novo isoprenoid synthesis in plastids, and determined the full-length gene sequences for 6 of 7 of these genes. Phylogenetic analyses revealed that each P. marinus gene clusters with orthologs from plastid-bearing eukaryotes, which have MEP pathway genes with essentially the same mosaic pattern of evolutionary origin. A new analytical method called sliding-window iteration of TargetP was developed to examine the distribution of targeting preferences. This analysis revealed that the sequenced genes encode bipartite targeting peptides that are characteristic of proteins targeted to secondary plastids originating from endosymbiosis of eukaryotic algae. These results support our idea that Perkinsus is a cryptic algal group containing nonphotosynthetic secondary plastids. In fact, immunofluorescent microscopy indicated that 1 of the MEP pathway enzymes, 1-deoxy-D-xylulose 5-phosphate reductoisomerase, was localized to small compartments near mitochondrion, which are possibly plastids. This tiny organelle seems to contain very low quantities of DNA or may even lack DNA entirely. The MEP pathway genes are a useful tool for investigating plastid evolution in both of the photosynthetic and nonphotosynthetic eukaryotes and led us to propose the hypothesis that ancestral "chromalveolates" harbored plastids before a secondary endosymbiotic event.     

Horizontal gene transfer in eukaryotic evolution

Horizontal gene transfer (HGT; also known as lateral gene transfer) has had an important role in eukaryotic genome evolution, but its importance is often overshadowed by the greater prevalence and our more advanced understanding of gene transfer in prokaryotes. Recurrent endosymbioses and the generally poor sampling of most nuclear genes from diverse lineages have also complicated the search for transferred genes. Nevertheless, the number of well-supported cases of transfer from both prokaryotes and eukaryotes, many with significant functional implications, is now expanding rapidly. Major recent trends include the important role of HGT in adaptation to certain specialized niches and the highly variable impact of HGT in different lineages.     

ANALYSIS OF ALEXANDRIUM TAMARENSE (DINOPHYCEAE) GENES REVEALS THE COMPLEX EVOLUTIONARY HISTORY OF A MICROBIAL EUKARYOTE1

Microbial eukaryotes may extinguish much of their nuclear phylogenetic history due to endosymbiotic/horizontal gene transfer (E/HGT). We studied E/HGT in 32,110 contigs of expressed sequence tags (ESTs) from the dinoflagellate Alexandrium tamarense (Dinophyceae) using a conservative phylogenomic approach. The vast majority of predicted proteins (86.4%) in this alga are novel or dinoflagellate‐specific. We searched for putative homologs of these predicted proteins against a taxonomically broadly sampled protein database that includes all currently available data from algae and protists, and reconstructed a phylogeny from each of the putative homologous protein sets. Of the 2,523 resulting phylogenies, 14%–17% are potentially impacted by E/HGT involving both prokaryote and eukaryote lineages, with 2%–4% showing clear evidence of reticulate evolution. The complex evolutionary histories of the remaining proteins, many of which may also have been affected by E/HGT, cannot be interpreted using our approach with currently available gene data. We present empirical evidence of reticulate genome evolution that combined with inadequate or highly complex phylogenetic signal in many proteins may impede genome‐wide approaches to infer the tree of microbial eukaryotes.     

Ancestral paralogs and pseudoparalogs and their role in the emergence of the eukaryotic cell

Gene duplication is a crucial mechanism of evolutionary innovation. A substantial fraction of eukaryotic genomes consists of paralogous gene families. We assess the extent of ancestral paralogy, which dates back to the last common ancestor of all eukaryotes, and examine the origins of the ancestral paralogs and their potential roles in the emergence of the eukaryotic cell complexity. A parsimonious reconstruction of ancestral gene repertoires shows that 4137 orthologous gene sets in the last eukaryotic common ancestor (LECA) map back to 2150 orthologous sets in the hypothetical first eukaryotic common ancestor (FECA) [paralogy quotient (PQ) of 1.92]. Analogous reconstructions show significantly lower levels of paralogy in prokaryotes, 1.19 for archaea and 1.25 for bacteria. The only functional class of eukaryotic proteins with a significant excess of paralogous clusters over the mean includes molecular chaperones and proteins with related functions. Almost all genes in this category underwent multiple duplications during early eukaryotic evolution. In structural terms, the most prominent sets of paralogs are superstructure-forming proteins with repetitive domains, such as WD-40 and TPR. In addition to the true ancestral paralogs which evolved via duplication at the onset of eukaryotic evolution, numerous pseudoparalogs were detected, i.e. homologous genes that apparently were acquired by early eukaryotes via different routes, including horizontal gene transfer (HGT) from diverse bacteria. The results of this study demonstrate a major increase in the level of gene paralogy as a hallmark of the early evolution of eukaryotes.     

Supertrees disentangle the chimerical origin of eukaryotic genomes

Eukaryotes are traditionally considered to be one of the three natural divisions of the tree of life and the sister group of the Archaebacteria. However, eukaryotic genomes are replete with genes of eubacterial ancestry, and more than 20 mutually incompatible hypotheses have been proposed to account for eukaryote origins. Here we test the predictions of these hypotheses using a novel supertree-based phylogenetic signal-stripping method, and recover supertrees of life based on phylogenies for up to 5,741 single gene families distributed across 185 genomes. Using our signal-stripping method, we show that there are three distinct phylogenetic signals in eukaryotic genomes. In order of strength, these link eukaryotes with the Cyanobacteria, the Proteobacteria, and the Thermoplasmatales, an archaebacterial (euryarchaeotes) group. These signals correspond to distinct symbiotic partners involved in eukaryote evolution: plastids, mitochondria, and the elusive host lineage. According to our whole-genome data, eukaryotes are hardly the sister group of the Archaebacteria, because up to 83% of eukaryotic genes with a prokaryotic homolog have eubacterial, not archaebacterial, origins. The results reject all but two of the current hypotheses for the origin of eukaryotes: those assuming a sulfur-dependent or hydrogen-dependent syntrophy for the origin of mitochondria.     

Identification of horizontally transferred genes in the genus Colletotrichum reveals a steady tempo of bacterial to fungal gene transfer

Background

Horizontal gene transfer (HGT) is the stable transmission of genetic material between organisms by means other than vertical inheritance. HGT has an important role in the evolution of prokaryotes but is relatively rare in eukaryotes. HGT has been shown to contribute to virulence in eukaryotic pathogens. We studied the importance of HGT in plant pathogenic fungi by identifying horizontally transferred genes in the genomes of three members of the genus Colletotrichum.

Results

We identified eleven HGT events from bacteria into members of the genus Colletotrichum or their ancestors. The HGT events include genes involved in amino acid, lipid and sugar metabolism as well as lytic enzymes. Additionally, the putative minimal dates of transference were calculated using a time calibrated phylogenetic tree. This analysis reveals a constant flux of genes from bacteria to fungi throughout the evolution of subphylum Pezizomycotina.

Conclusions

Genes that are typically transferred by HGT are those that are constantly subject to gene duplication and gene loss. The functions of some of these genes suggest roles in niche adaptation and virulence. We found no evidence of a burst of HGT events coinciding with major geological events. In contrast, HGT appears to be a constant, albeit rare phenomenon in the Pezizomycotina, occurring at a steady rate during their evolution.

Electronic supplementary material

The online version of this article (doi:10.1186/1471-2164-16-2) contains supplementary material, which is available to authorized users.     

Organelle origins and ribosomal RNA

As the detailed molecular biology of organelle genomes has unfolded, there has been a general acceptance of the view that plastids and mitochondria are of endosymbiotic, eubacterial origin. Plastid genes are strikingly similar to their eubacterial (particularly cyanobacterial) counterparts in sequence, organization, and mode of expression, and such features strongly support the hypothesis that the plastid and its genome were derived in evolution from a blue-green alga-like endosymbiont. Mitochondria, on the other hand, are problematic: mitochondrial genes are organized and expressed in remarkably diverse ways in the different major groups of eukaryotes, and in no case are these features particularly characteristic of either bacterial or nuclear genomes. There is, however, clear evidence derived from gene sequence supporting the eubacterial ancestry of mitochondria, and some of the most compelling data have come from analyses of mitochondrial ribosomal RNA (rRNA). Plant mitochondrial rRNA genes diverge in sequence at a particularly slow rate, and these genes have proven to be especially supportive of the endosymbiont hypothesis, pointing to an origin of mitochondria from within the alpha subdivision of the purple bacteria. Ribosomal RNA sequences provide a basis for the construction of global phylogenetic trees that probe the evolutionary history of organelles, and that address the question of whether mitochondria and plastids are monophyletic or polyphyletic in origin. Such studies raise the possibility that the rRNA genes of plant mitochondria originated separately from the mitochondrial rRNA genes of other eukaryotes.