Are Fungi Plants And Animals Prokaryotes Or Eukaryotes

• Periodical Listing
• mBio
• 5.7(4); Jul-Aug 2016
• PMC4958254

mBio. 2016 Jul-Aug; seven(iv): e00863-16.

Transfer of DNA from Bacteria to Eukaryotes

ABSTRACT

Historically, the members of the Agrobacterium genus take been considered the only bacterial species naturally able to transfer and integrate Deoxyribonucleic acid into the genomes of their eukaryotic hosts. Yet, increasing evidence suggests that this ability to genetically transform eukaryotic host cells might exist more widespread in the bacterial world. Indeed, analyses of accumulating genomic data reveal cases of horizontal cistron transfer from bacteria to eukaryotes and suggest that it represents a significant force in adaptive evolution of eukaryotic species. Specifically, contempo reports indicate that bacteria other than Agrobacterium, such as Bartonella henselae (a zoonotic pathogen), Rhizobium etli (a plant-symbiotic bacterium related to Agrobacterium), or fifty-fifty Escherichia coli, have the ability to genetically transform their host cells nether laboratory weather condition. This DNA transfer relies on blazon IV secretion systems (T4SSs), the molecular machines that send macromolecules during conjugative plasmid transfer and too during ship of proteins and/or DNA to the eukaryotic recipient cells. In this review article, we explore the extent of possible transfer of genetic data from bacteria to eukaryotic cells too as the evolutionary implications and potential applications of this transfer.

INTRODUCTION

Vertical gene inheritance is the main pathway of transmission of genomic data from the parents to their offspring via germline or cell division. Nonetheless, genetic information can be transmitted also between organisms that are non direct related; these exchanges are termed horizontal cistron transfer (HGT; also known equally lateral factor transfer) (i). Amid prokaryotes, HGT—beginning observed as the spreading of drug resistance within a bacterial population (2)—is at present recognized as a major evolutionary forcefulness (3,–5). Indeed, several genome-broad studies have shown that HGT occurs at a loftier frequency between prokaryotic species, especially if they are closely related or if they coexist in the same habitat or community, which provides many opportunities for Deoxyribonucleic acid transfer (iv, v). Unlike evolution via gene duplications and mutations, a irksome and incremental process, HGT permits fast acquisition of a new function of import for species adaptation and survival.

Numerous cases of HGT from bacteria to eukaryotes accept been demonstrated, although this process is causeless to be much less frequent than HGT betwixt bacteria. The early on evolution of eukaryotes was marked by endosymbiotic events leading to permanent acquisition of major organelles, east.g., mitochondria that originated from proteobacteria and plastids that originated from cyanobacteria, followed past organelle-to-nucleus gene transfer, ordinarily referred to as endosymbiotic gene transfer (EGT) (6). Whereas the episodic gene transfer via EGT has a demonstrated evolutionary significance, the importance of HGT in the evolution of eukaryotes is all the same debated (7). A contempo study analyzing a large number of protein sequences from bacterial and eukaryotic organisms indicates that gene inheritance in eukaryotes is predominantly vertical and suggests that HGT occurs but occasionally and that sequences acquired by HGT practise not accrue in eukaryotic genomes and do not contribute to long-term development of factor content (8). Nonetheless, it is generally agreed that HGT from prokaryotes to eukaryotes does occur to a certain extent and, in some cases, plays a office in adaptive evolution (9). Whereas the identification of HGT genomic signatures indicates the existence of such events in the course of evolution, it does non inform near the pathway(south) and mechanisms(s) by which these sequences accept been transferred. Instead, this information derives from numerous studies of known systems of natural and experimental factor transfer from leaner to eukaryotic cells—such every bit the Agrobacterium-host plant interaction, the best-studied and best-understood system of transkingdom Dna transfer. Here, we review the major known cases of HGT from bacteria to eukaryotes that do not originate from prokaryote-derived permanent organelles, with a focus on natural and bogus prokaryote-to-eukaryote gene transfer systems that may assist us empathize the potential mechanisms involved in these transkingdom exchanges of genetic data.

SIGNATURES OF BACTERIUM-TO-EUKARYOTE HGT IN GENOME SEQUENCES

In most cases, the first step in identifying an HGT event is the detection of a sequence that does non follow the expected phyletic distribution. However, the presence of such a sequence may also issue from differential cistron loss in virtually species of a unmarried clade, leading to the impression that this gene is present only in one remaining species. The classical method to validate a suspected HGT consequence is phylogenetic inference: the finding of a topological disagreement betwixt a strongly supported gene tree and the known species tree is a good indicator of an HGT event (4, vii, 10). Other accompaniment methods may assist to confirm the occurrence of HGT, such equally base limerick, the presence or absence of introns, codon usage, synteny assay, and such ecological features as a shared niche or location for the species involved. Still, the exact identity of the prokaryotic species from which the sequence caused by HGT originates is sometimes difficult to determine because of subsequent evolution of the transferred sequence or because the "donor" species is extinct.

The complete sequencing of Dictyostelium discoideum (11) revealed xviii genes resulting from potential HGT from bacteria, which sometimes conferred new functions, such as a dipeptidase enzymatic activity potentially able to degrade the bacterial cell wall. Similarly, Galdieria sulphuraria, a ruddy alga that lives in extreme, i.e., hot, acidic, and heavy-metal-rich, environments harbors genes obtained through HGT from bacteria and archaea and that may correspond, later duplication and diversification, as much equally 5% of its protein-encoding genes. Most of these proteins of suspected bacterial origin, such as an arsenic membrane protein pump like to those found in thermoacidophilic leaner, are expressed and are believed to have facilitated ecological adaptation of Thou. sulphuraria to extreme environments in the course of the evolution of this species (12).

Several cases of potential HGT from bacterial sources likewise take been identified in Saccharomyces cerevisiae and other yeast species (13, 14). For example, the URA1 gene, which encodes the enzyme dihydroorotate dehydrogenase required for anaerobic synthesis of uracil, appears to originate from the lactic acid leaner Lactobacillales. In establish-associated fungi, the acquisition of bacterial genes by HGT is considered widespread and likely represents a significant forcefulness in their adaptive evolution (15). These genes oftentimes encode factors involved in niche specification, pathogenicity, and adaptation to different metabolic requirements (x). Often, HGT occurs into found-pathogenic fungi living in the community with many other establish-associated prokaryotic and eukaryotic microorganisms (16). In particular, within the genomes of three species of Colletotrichum, a genus of found-pathogenic fungi that cause the crop-destructive disease anthracnose, at least 11 contained HGT events from bacterial genomes were identified (17). These transferred genes encode factors involved either in interaction with host constitute and fungal virulence or in various metabolic processes, and they likely play a function for niche adaptation. Similarly, two species of the vascular wilt fungus Verticillium acquired by HGT from proteobacteria a gene that encodes a glucan glycosyltransferase involved in synthesis of extracellular glucans important for virulence (18).

Microbial eukaryotes, such equally D. discoideum or Grand. sulphuraria, and most fungi either are unicellular or brandish a predominant unicellular phase in their life cycle; thus, in these species, genes can be vertically transmitted during cell partitioning. Nonetheless, for more circuitous, multicellular organisms, HGT tin can be transmitted vertically only by two general mechanisms: when the recipient cells are germline cells or when they are able to dedifferentiate and/or regenerate to a functional organism past asexual reproduction.

In multicellular organisms, bacterium-to-animal jail cell HGT appears to be express to invertebrates, and it has originated either from gene transfer from endosymbiotic bacteria to their hosts or from transfer from bacteria to asexual animals (19). 1 of the nigh striking examples of HGT from bacterial endosymbionts to animate being hosts is the gene transfer from Wolbachia to different arthropods and nematodes (twenty). Wolbachia species are proficient candidates for heritable HGT: they are intracellular symbionts, maternally inherited, and transmitted through egg cytoplasm. Among xi sequenced arthropod genomes, eight contain Wolbachia sequences acquired via HGT; interestingly, the transferred sequences sometimes represented a significant portion (up to xxx%) of the genome. HGT also had occurred from nonendosymbiont bacteria to freshwater asexual animals, such as Hydra magnipapillata (21) and bdelloid rotifers (22). On a few occasions, however, initial indications that creature genomes contain numerous genes originating from HGT were refuted by subsequent more than-detailed analyses. For example, a big number of potential HGT events were first reported for the human genome (23), merely this claim was disproved afterward closer test of the information based on phylogenetic analysis that included a larger number of eukaryotic species (24).

A comparative genomic study of the early land constitute Physcomitrella patens and of a angiosperm, Arabidopsis, uncovered 57 families of nuclear genes that potentially had been acquired past HGT, mainly from bacterial species (25). Several of these genes are involved in land-plant-specific activities, e.g., xylem formation, defense, and regulation of growth, suggesting that HGT played an of import role in the transition from the aquatic to the terrestrial environs. Furthermore, phylogenetic evidence supports the idea that the major biosynthetic pathway of auxin, the principal hormone of land plants, is derived from the bacterium-to-plant HGT (26). Another series of HGT events in plants resulted from the insertion of Agrobacterium transfer Deoxyribonucleic acid (T-Dna) into the plant genome and its vertical transfer via sexual reproduction (27). It was first reported in Nicotiana glauca (28, 29) then found in nearly species of Nicotiana tested to engagement (thirty, 31). In a screen of more than than 100 dicotyledonous found species, Agrobacterium T-Dna sequences were detected in two species of the genus Linaria (32). More recently, the presence of T-DNA sequences acquired past HGT was discovered in the genomes of several varieties of cultivated sweetness potato, Ipomoea batatas (33). The origin of the T-DNA-derived genes was identified every bit a mikimopine strain of Agrobacterium rhizogenes for both Nicotiana and Linaria and probable as an ancestral form of A. rhizogenes for I. batatas. Some of these T-Deoxyribonucleic acid genes are however expressed at a detectable level in modern plants, although whether they have a functional part in the plant biology remains unknown. These HGT events originating from Agrobacterium species represent a rare example for which the source of the transferred genes is clearly identified and the transfer pathway is well studied (see below).

NATURAL AND EXPERIMENTAL BACTERIUM-TO-EUKARYOTE DNA TRANSFER SYSTEMS

The major known natural and artificial systems for gene transfer from bacterial to eukaryotic cells include such leaner as Agrobacterium and Rhizobium species and Escherichia coli, and they are summarized in Fig. 1. The first system is the Agrobacterium-to-found jail cell DNA transfer, which represents the paradigm of eukaryotic genetic transformation by bacteria and has long been considered a unique example in living nature; thus, it is the most-studied example of transkingdom gene transfer (34, 35). Agrobacterium is a plant-pathogenic bacterium that causes neoplastic growths, i.e., uncontrolled cell divisions that form galls or root proliferations, in its host plants by transferring a segment of DNA into the host cell genome. Most of the bacterial genes essential for cistron transfer are located on a large tumor-inducing plasmid, termed the Ti plasmid, which also contains the transferred Deoxyribonucleic acid segment, termed the T-DNA, that is delimited and specified by two short straight repeat sequences, left and right borders. Establish-derived phenolic and sugar point molecules trigger the expression of the virulence (vir) genes in Agrobacterium cells, and the encoded Vir proteins mediate the transfer of the T-Dna to the plant cell. The T-DNA is transferred as a single-stranded molecule, produced by the VirD2 endonuclease, which, in association with the VirD1 Deoxyribonucleic acid topoisomerase (36), mediates the mobilization of the transferrable T-DNA from the Ti plasmid by a strand replacement mechanism; VirD2 so remains covalently bound to the 5′ terminus of the T-DNA molecule. Upon interaction with the coupling factor VirD4, the VirD2–T-Dna complex is directed to the blazon Four secretion system (T4SS) composed of 11 proteins encoded by the virB operon. The T4SS so mediates the translocation of the VirD2–T-DNA complex, as well equally several other Vir protein effectors, from the bacterium to the host jail cell cytoplasm. The fate of the T-DNA in the host cell relies on multiple interactions with Agrobacterium and host prison cell proteins, taking advantage of several host jail cell pathways to ensure the T-Dna nuclear import and integration into the host genome. Both VirD2 and the single-stranded DNA binding protein VirE2—which packages T-Deoxyribonucleic acid into a helical nucleoprotein complex, termed the transfer (T) complex—can interact, directly or indirectly, with host factors to allow nuclear import of the T complex. This procedure likely occurs in a polar manner such that VirD2 directs the T-Deoxyribonucleic acid to the nuclear pore while VirE2 facilitates the passage of the unabridged T complex through the pore via the importin-α-dependent nuclear import pathway. Inside the nucleus, the T circuitous is proteolytically uncoated from its associated bacterial and host proteins, presumably by interacting with the host ubiquitin/proteasome arrangement (UPS). Then, the single-stranded T-Dna virtually likely is converted to a double-stranded form and integrated into the establish genome by the host Dna repair machinery. Interestingly, under laboratory conditions, Agrobacterium is able to transfer Deoxyribonucleic acid to many nonplant cells, from fungi to human being cultured cells (37), suggesting that T-Deoxyribonucleic acid nuclear import and subsequent processing and integration are mediated by factors found in all various eukaryotic species, rather than by factors specific for host plants. Furthermore, Agrobacterium is as well able to transfer sequences from a mobilizable plasmid (RSF1010) to found cells via the activeness of Vir proteins and of the plasmid mobilization functions (38).

Schematic summary of known natural and experimental pathways for DNA transfer from bacteria to eukaryotic cells. Agrobacterium and related bacteria, E. coli, and Bartonella henselae tin can transfer DNA to different types of eukaryotic cells via the activity of their type IV secretion systems equanimous of VirD4/VirB proteins. Inside the host eukaryotic prison cell, the bacterial transferred Deoxyribonucleic acid, usually a single-stranded molecule packaged into a nucleoprotein complex, is imported into the host nucleus. Nuclear import and further DNA processing, i.e., conversion to a double-stranded class, integration into the recipient cell genome, or formation of an episome, depend on interactions of the transferred DNA and its associated proteins with numerous host cell factors that represent unlike types of cellular machineries, such equally nuclear import machinery, the ubiquitin/proteasome organization, and Dna repair mechanism. For further details, see the text.

As early as 1977, information technology was reported that the Ti plasmid of Agrobacterium could be transferred by conjugation to cells of the related species Rhizobium trifolii, which conferred on those leaner the ability to trigger virulence, i.eastward., evolution of crown galls, on several plant species (39). Later, information technology was shown that the introduction of both a disarmed Ti plasmid, i.eastward., harboring the vir genes just no T-DNA, and a binary plasmid, i.e., containing T-Dna but no vir genes, into such Rhizobiaceae species equally Rhizobium leguminosarum, R. trifolii, and Phyllobacterium myrsinacearum, produced virulent bacteria able to transfer T-Dna to Arabidopsis, tobacco, and rice (xl), whereas potato plants were genetically transformed by Sinorhizobium meliloti, Rhizobium sp. strain NGR234, and Mesorhizobium loti supplied with a similar binary vector set (41). Another bacterial species of the Rhizobiaceae family unit, Ensifer adherens, when equipped with a cointegrated vector containing both the vir region and T-DNA from Agrobacterium, was used to transform tater and rice plants (42, 43). All these species are symbiotic bacteria that belong to the same Rhizobiales order as Agrobacterium and are able to mediate nitrogen assimilation for their host plants.

In all these studies, the vir region of a virulent strain of Agrobacterium had to be supplied along with the T-Dna in order to confer competence for plant transformation on the bacterial species, which naturally encoded no native plant transformation machinery. However, several species of rhizobia contain their own vir genes, with different levels of homology to the Agrobacterium vir genes. Specifically, Rhizobium etli strain CFN42 naturally contains, on its p42a plasmid, a functional T-DNA transfer machinery comprising all the necessary vir gene functions. Indeed, when a binary plasmid, containing a T-Deoxyribonucleic acid but not the vir region, was introduced into R. etli, the resulting strain was able to transfer and integrate T-DNA into establish cells, albeit with a lower frequency than that with Agrobacterium (44). This T-DNA transfer was not observed with mutants of R. etli that lack one of the essential vir genes (virG or virE2) or with R. leguminosarum, a species very close to R. etli overall but with merely very weak homology to the vir genes. Importantly, our assay of the known Deoxyribonucleic acid sequences of R. etli detected no homologies to known Agrobacterium T-Deoxyribonucleic acid sequences, i.e., T-Deoxyribonucleic acid borders or T-Deoxyribonucleic acid genes; even so, we cannot rule out the possibility that R. etli might contain its own, specific T-DNA sequences undetectable past in silico analyses.

The transfer of plasmid DNA can likewise occur from bacteria (E. coli) to yeast (South. cerevisiae) (45). This transfer was effective with both broad-host-range and F-factor plasmids, which stand for the ii chief types of conjugative plasmids in Gram-negative bacteria. The transfer mechanism exhibited similarities with bacterial conjugation: for example, physical contact between the cells was required as well as genetic factors, i.east., mob and oriT, necessary for bacterial conjugation. Dna transfer was also observed from East. coli to other yeast species, such as Kluyveromyces lactis and Pichia angusta (46) or Saccharomyces kluyveri (47). The ability of Eastward. coli to deliver DNA molecules via conjugation-like pathways to other types of eukaryotic cells was likewise reported for factor transfer to cultured human cells (48) and, more recently, to the unicellular algae diatoms (49). Although there is no definitive proof that such bacterium-to-eukaryote conjugation occurs in nature, these examples advise that the ability to transfer genetic data to eukaryotic hosts is not restricted to Agrobacterium.

In another instance of potential ability to genetically transform the host cell, Bartonella henselae, a facultative intracellular human bacterial pathogen, was shown to transfer a modified ambiguous plasmid (50) or derivatives of the R388 plasmid (51) into homo cultured cells via a conjugation-like mechanism. Indeed, the bacterial strains used in these experiments harbored a T4SS, which was required for the transport of plasmids from the bacterium to the host cell, and this Dna transfer was disrupted in B. henselae strains with a mutated virB region. Interestingly, host cell partition was required for expression of the transgene, suggesting that the bacterium is unable to utilise the host nuclear import pathways and, instead, relies on breakdown of the host nuclear envelope. This B. henselae-human jail cell Dna transfer produced stable transgenic jail cell lines, indicating the integration of the transferred sequences in the host jail cell genome. Whereas the Bartonella T4SS is known to transport effector proteins essential for virulence into the host cells (52), its apparent ability to transfer plasmid Deoxyribonucleic acid has no demonstrated role in the infection process and may correspond the relic of an ancestral function.

POTENTIAL MECHANISMS OF BACTERIUM-TO-EUKARYOTE HGT

Dna transfer into bacterial cells is known to occur via three different mechanisms: transformation (uptake of free DNA in solution), bacteriophage-mediated transduction (i.e., both generalized and specialized transduction), and plasmid-mediated transfer (i.e., conjugation, which usually requires close contact betwixt donor and recipient cells). But are these mechanisms applicable to HGT? Potential HGT pathways may be inferred from studies of natural and experimental bacterium-to eukaryote factor transfer systems. Although yeast cells have been suggested to larn exogenous DNA under conditions close to their natural environment (53), in that location are no known naturally occurring mechanisms of DNA uptake in eukaryotic cells. In a study of HGT between Wolbachia and Aedes aegypti (54), bacteriophage sequences were found close to the transferred genes, suggesting the role of bacteriophages equally HGT vectors. It has also been suggested that some viruses, in particular giant viruses, may mediate transfer of Dna from bacteria to eukaryotes, but this pathway of HGT has not been confirmed experimentally (12).

Notably, near bacteria possessing the ability to transfer DNA to eukaryotic host cells belong to the Alphaproteobacteria class (55). Nigh of these bacterial species show a degree of interaction with eukaryotic hosts, from pathogenic or symbiotic lifestyles, e.m., Agrobacterium and Rhizobium, to optional or obligate parasitism of intracellular bacteria, e.thou., Bartonella and Wolbachia. In these species, the "mobilome," i.e., the pool of plasmids containing shared genetic information, plays a prominent role, which almost likely underlies high genome plasticity and gene mobility between leaner equally well equally the ability of these bacteria to transfer Dna to eukaryotic cells.

In known natural and experimental bacterium-to-eukaryote DNA transfer systems, i.e., bacterium-yeast conjugation, Bartonella-mediated transformation of animal cells, and Agrobacterium/Rhizobium-mediated genetic transformation of diverse eukaryotes, the ship of Dna from the bacterial jail cell to the recipient cell cytoplasm depends on conjugation-like mechanisms mediated by the bacterial T4SS. T4SSs are specialized molecular superstructures able to transport protein and DNA molecules between donor leaner and a multifariousness of recipient cells (56, 57). They are encoded by many bacterial species and are often involved in conjugation, i.e., transfer of genetic information between bacterial cells of the same or closely related species. However, T4SSs are too known to mediate macromolecular transport of Dna and/or proteins from bacteria to cells of their eukaryotic hosts. In fact, to date, T4SS represents the only demonstrated machinery of transfer of genetic material to eukaryotic cells from bacteria in nature or under laboratory conditions. Although the consign of macromolecules beyond the bacterial membranes and prison cell walls through the T4SS is well understood (57, 58), how the transported protein or DNA molecule passes across the eukaryotic recipient cell wall and membrane remains obscure. Past analogy to type Iii secretion systems (T3SSs) (59), the T4SS hair itself might pierce the host cell barriers to inject macromolecules directly into the host cytoplasm, but this machinery has never been directly observed. The bore of this aqueduct is compatible with the size of transported macromolecules (60), and ii studies take shown that DNA tin can be transferred by conjugation between bacterial cells without direct cell-to-prison cell contact, suggesting that Dna transits through the F pilus lumen (61, 62). Alternatively, the exported macromolecules first may be deposited at the surface of the recipient cell by the T4SS and then internalized by a split mechanism that may involve host receptors and/or endocytosis. Indeed, studies of direct transformation of yeast cells have shown that in one case Deoxyribonucleic acid molecules are placed at the surface of the host jail cell membrane, they may become internalized (e.thou., reference 63).

Our knowledge about the molecular reactions that occur later on the entry of the transferred Deoxyribonucleic acid into the host cell cytoplasm and lead to the transgene expression and integration derives largely from the studies of Agrobacterium-mediated genetic transformation, which point that they rely on interactions of the transferred bacterial DNA and proteins with host factors. Specifically, in a eukaryotic cell, the incoming single-stranded Dna molecule, which represents a mobile T-Deoxyribonucleic acid or a conjugative plasmid, should exist imported into the cell nucleus before farther processing. Nuclear uptake of the Agrobacterium T-Dna and its associated proteins is mediated by the host nuclear import machinery (35). In addition, it was suggested that, in some cases, the host cell division could exist required for expression or integration of the invading Dna, thereby circumventing the necessity for active nuclear import and allowing passive entry in the nucleus following disruption of the nuclear envelope (l). Inside the nucleus, replication of the DNA, imported as a single-stranded molecule via the bacterial T4SS, is idea to occur before plasmid circularization or before integration (64,–66) and is likely mediated by the host DNA replication machinery. In the case of Agrobacterium, the T-DNA circularization has been shown to occur, although it remains unclear whether these circles function as intermediates of integration (64,–66). Furthermore, the single-stranded T-DNA molecule is converted to a double-stranded molecule before integration (67, 68), whereas the beingness of other pathways of integration cannot be excluded. Finally, the host double-strand break (DSB) DNA repair pathways play a crucial role in integration of the transferred sequences (69).

EVOLUTIONARY IMPLICATIONS OF HGT

A few decades ago, the only demonstrated bacterium-to-eukaryote cistron transfer was represented by plant genetic transformation mediated by Agrobacterium. Subsequent studies showed that this capability could be observed in other related bacterial species, such as many Rhizobiaceae, including R. etli, Due east. coli, and Bartonella, and with a wider range of host species from all eukaryotic taxa. In addition, the ever-increasing corporeality of genomic data from both prokaryotes and eukaryotes led to the discovery of HGT genomic signatures in a broad spectrum of eukaryote species. Globally, the influence of bacterium-to-eukaryote HGT may take been more than important for evolution of eukaryotes than previously idea, to the extent that HGT has been proposed to underlie the emergence of several lineages of eukaryotic organisms equally opposed to the idea of all eukaryotes descending from a unmarried universal antecedent (seven).

It is of import to annotation that the presence of bacterial HGT signatures in eukaryotic genomes does not depend solely on the ability of bacteria to transfer DNA into the host cell. Instead, 4 additional major atmospheric condition should exist met. First, the transferred DNA must become integrated into the host genome. 2nd, the foreign sequence must not be lost after rearrangements of the genome during subsequent cell divisions. Third, for multicellular eukaryotes, the transformed prison cell must either be fixed in the germline for genetic modification of animals and establish germlines or regenerate into a viable organism when asexual reproduction is possible, for instance, via cell dedifferentiation in plants. Finally, the integrated sequence must be preserved in the course of evolution, which is more than likely to occur if the acquired cistron confers a selective reward or is at least neutral rather than deleterious. Thus, transient transformation events, which, by definition, are not retained in the genome, probably occur at a much higher rate than is suggested by the HGT signatures discovered in eukaryote genomes. Yet, this miracle of "transient expression," which is well known in the Agrobacterium-plant interaction, might play a role in promoting HGT. For example, hypothetically, transient genetic transformation could express putative effector proteins, which are coordinating to effectors translocated from many pathogenic or symbiotic bacteria to their eukaryotic hosts, which in turn volition facilitate subsequent rounds of bacterial infection.

The very wide range of eukaryotic cells that can be transformed past Agrobacterium suggests that the Dna transfer involves central biological processes common to most, if not all, eukaryotes and is not dependent on host species-specific factors (37). Indeed, in improver to numerous plant species that can exist transformed by Agrobacterium either naturally or nether laboratory conditions, other, evolutionarily distant eukaryotes such as yeast (70, 71) and many other fungi (72, 73) and arachnid (74) and homo cultured (75) cells are amenable to Agrobacterium-mediated transformation. Moreover, nether laboratory conditions, DNA transfer via conjugation-related mechanisms is possible between other bacteria, e.g., E. coli, and several eukaryote species. Thus, the combined potential of different bacterial species to alter genetically cells of virtually all eukaryotes supports the notion of HGT as a widespread mechanism in evolution.

POTENTIAL APPLICATIONS

Also its importance for understanding the evolution of mod eukaryotes, the bacterium-to-eukaryote cistron transfer has a unique and highly significant awarding potential, which lies mainly in two major areas, research and biotechnology. Inquiry applications mainly aim at discovering new protein functions and cellular pathways past expressing specific genes of involvement, delivering cistron-targeting systems, such as CRISPR/Cas9 (76), or insertional mutagenesis of genomes of interest, for example, by generating T-Dna insertion mutant libraries of the model found Arabidopsis thaliana (77). Biotechnological applications aim at expressing traits of interest, such as pathogen and abiotic stress resistance genes, genetically engineered pathways for production of biofuels and pharmaceuticals, or generation of desired phenotypes, east.1000., colour and fragrance of flowers and fruits in agronomics or restoration of normal cellular functions in cistron therapy. To reach these full general goals, it is of import to conform and optimize unlike bacterial Deoxyribonucleic acid transfer systems—or even discover new bacterial species capable of Deoxyribonucleic acid transfer to eukaryotes—for use as vectors for genetic transformation of specific eukaryotic cells or organisms, allowing development of highly efficient "custom-tailored" DNA transfer tools for each specific application.

In plants, Agrobacterium-mediated genetic transformation already is efficient for some species, but many other institute species or cultivars, especially those of agronomical importance, are still considered "recalcitrant to transformation" and might become more amenable to gene transfer past a unlike bacterial vector, for example, belonging to the rhizobial grouping, with a more advisable natural host range. Indeed, the early steps of plant genetic transformation rely on close interactions between the bacterium and plant cells, which may be more efficient between plant-associated rhizobia and their hosts than Agrobacterium interactions with the same host species. The aforementioned approach also may lead to improving the efficiency of transformation of fungal and other eukaryotic species. In fact, the Agrobacterium-mediated transformation has become a technique of choice for genetic modification of different species of fungi (73); furthermore, information technology was likewise suggested that methods based on bacterium-yeast cell conjugation, using, for instance, E. coli, could exist extended to other species of fungi (78). Plainly, these approaches could exist adapted to other eukaryotic cells, such as fauna or algal cells.

In animals, 2 main types of vectors are employed to introduce Dna of interest into homo cells for cistron therapy: biologicals, such as viruses or bacteria, and biomaterials (79). To date, viruses represent the overwhelmingly predominant vector for use in factor therapy; withal, our increasing cognition about bacterial DNA transfer systems positions bacteria as a promising alternative for viral vectors (80). Bacterial vectors possess specific features that could exist advantageous nether specific circumstances: for example, bacterial vectors may exist introduced into a tissue for transformation and so easily eliminated by application of antibiotics; many bacteria remain extracellular during DNA transfer, thereby avoiding transfer of Deoxyribonucleic acid sequences other than the gene of interest; and some bacterial strains tin can target a specific cell blazon or be engineered for that purpose (80).

Conversely, it is also necessary to investigate and empathise potential implications of natural cases of bacterium-to-eukaryote Dna transfer in evolution of animal and human diseases, such as cancer. Indeed, it is estimated that about xx% of cancers are acquired by bacterial or viral infection (81). For instance, ane of the best-characterized cases of cancer acquired by or associated with bacterial infection is the consecration of gastric carcinoma by Helicobacter pylori (82). In most cases, it is thought that carcinogenesis results from stress, e.g., tissue inflammation, caused by the infection process (83). Yet, it has been besides proposed that the transfer and insertion of bacterial Dna sequences into the host cell genome may represent some other and more specific cause of cancer evolution (84, 85). If this hypothesis is confirmed, our accumulating knowledge of bacterium-eukaryote DNA transfer volition represent an invaluable tool for providing novel insights into early stages of carcinogenesis.

CONCLUSION

Transfer of genetic information from bacteria to eukaryote cells, in one case believed to occur exclusively during infection of plants by Agrobacterium, probably occurs in many other bacterium-host jail cell interactions, which include a wide multifariousness of combinations of donor bacterial species and recipient eukaryote species, at least under laboratory weather. Studies of these factor transfer systems are critical for agreement their potential ecological and evolutionary significance besides every bit for their utilization for development of new biological tools for fundamental and applied purposes.

ACKNOWLEDGMENTS

Due to space constraints, we relied largely on citing review articles, and nosotros repent to our colleagues whose original publications, therefore, take not been cited.

The work in the V.C. laboratory is supported by grants from NIH, NSF, NIFA/USDA, BARD, and BSF.

Footnotes

Citation Lacroix B, Citovsky V. 2016. Transfer of DNA from bacteria to eukaryotes. mBio 7(four):e00863-xvi. doi:x.1128/mBio.00863-16.

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Articles from mBio are provided here courtesy of American Order for Microbiology (ASM)

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Source: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4958254/

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