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Horizontal Gene Transfer and Endophytes
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This entry is adapted from the peer-reviewed paper 10.3390/plants9030305

Horizontal gene transfer (HGT), an important evolutionary mechanism observed in prokaryotes, is the transmission of genetic material across phylogenetically distant species. The availability of complete genomes has facilitated the comprehensive analysis of HGT and highlighted its emerging role in the adaptation and evolution of eukaryotes. Endophytes represent an ecologically favored association, which highlights its beneficial attributes to the environment, in agriculture and in healthcare. The HGT phenomenon in endophytes, which features an important biological mechanism for their evolutionary adaptation within the host plant and simultaneously confers “novel traits” to the associated microbes, is not yet completely understood. With a focus on the emerging implications of HGT events in the evolution of biological species.

Endophytes, Horizontal gene transfer, novel traits

1. Introduction

Horizontal gene transfer (HGT) refers to the transmission of genetic material across the genomes of biological organisms by processes other than fertilization. HGT is a universal phenomenon observed in bacterial, fungal, and eukaryotic genomes [1][2]. However, it occurs infrequently and only serves as an alternative process for the exchange of genetic material between distantly related species. HGT is relatively more common in prokaryotes than eukaryotes [3][4][5]; studies have shown that approximately 81% of genes have transferred through HGT, in 181 sequenced prokaryotic genomes [6].
In the past decade, the availability of eukaryotic genomes through high-throughput sequencing has promoted the research on the occurrence and mechanism of HGT in eukaryotes [7]. Additionally, information about whole prokaryotic genomes has made it convenient to study HGT between distantly related species [8], specifically in terms of organismal evolution and ecological adaptation for survival [9][10]. HGT has been observed previously between Alternaria and Fusarium fungi [11], nematodes and insects [12][13], humans and bacterial pathogens [14], plants and silkworms (Bombyx mori) [15], and plants and fungi [16]. Extensive investigations on the significance of the HGT phenomenon in prokaryotic evolution (e.g., archaea and bacteria) revealed a possible mechanism for acquiring novel traits during the evolutionary course [17]; however, in eukaryotes, this phenomenon was presumed to be uncommon [18][19]. Moreover, the transmission and integration of the transferred genes might provide several beneficial attributes, including prokaryotic adaptation during environmental changes [20][21], acquisition of new traits/functions [22], and evolutionary adaptation in eukaryotes [23][24].

2. HGT in Nature: An Overview

The phenomenon of HGT differs from the vertical transmission of genetic material from parent to offspring [25][26]. Distinct patterns in HGT were observed through endosymbiosis and introgressive hybridization [27]. HGT was first discovered in 1928 by Griffith, who demonstrated that virulence factor was transferred between pneumococcal strains in mice. Since this discovery, the accessibility to “big data” provided by the sequencing of complete genomes has led to the identification of transferred genes in multiple taxonomic groups [28]. However, the importance of HGT in eukaryotic genome evolution [29][30][31], is an emerging research area in the present time and is extensively explored.
The discovery of HGT across diverse biological species suggests its strong evolutionary role and highlights its significance in species adaptation and survival. For example, fungi and ciliates acquired the genes for carbohydrate metabolism from a ruminant animal [32][33]. Studies have suggested the role of HGT in facilitating microbial adaptation to adverse conditions in the environment [34] and inside the host plant [35]. In the past few years, the information on HGT events in whole eukaryotic genomes was limited and genomic information at the taxonomic level was unavailable. However, studies utilizing whole genome sequences and high throughput technologies revealed that HGT events in eukaryotic genomes, particularly in the plant kingdom, have a crucial impact on plant evolution [36]. In particular, the comprehensive phylogenetic analyses of genomes in 6 plant species, together with other prokaryotic and eukaryotic genomes, identified 1,689 genes that were similar to fungi, indicating the exchange of genetic material between plants and fungi [36], consequently resulting in novel traits arising in plant genomes. Moreover, studies reviewed the possibilities of HGT occurring from plants to endophytes, to determine potential applications for the production of bioactive secondary metabolites via the endophytic fungi [37]. Endophytic fungi can produce secondary metabolites, hence, it was hypothesized that HGT between the host plant and associated fungi was responsible for the production of bioactive secondary metabolites [38]. The study also discussed the possibilities of different mechanisms on how an endophytic fungus acquired genetic traits from the host plant and whether HGT was beneficial for the adaptation and survival of the organisms in association [37][38].

3. The Mechanisms of HGT

HGT differs from other mechanism of genetic transmission since it does not involve parent–offspring inheritance, and therefore, might occur between distantly related species. Furthermore, the transfer of genetic material is rapid, rendering it an important mechanism for microbial adaptation to new environmental niches [39][40]. There are several mechanisms for HGT across different taxonomic groups (with different frequencies) as determined by the genetic distance between two biological organisms [41]. Several studies have shown HGT across biological species, specifically in archaea [42], bacteria [2][39], and eukaryotes [43]. The HGT phenomenon has been widely studied in bacteria and archaeal genomes; however, this is not the case in eukaryotes.
The HGT mechanisms in prokaryotes, including transformation, conjugation, and transduction, have been well documented; however, HGT in eukaryotes might be more complex, particularly in plants, and might involve vector-mediated or direct pathways [44]. The direct pathway might occur through direct DNA exchange [18], while vector-mediated pathway requires the use of vectors such as bacteria, fungi, virus, etc. [45][46]. Moreover, HGT between nuclear and plastid genomes have been reported [47], i.e., between plant mitochondrial genomes [48] via bacteria-mediated [40][49] and parasitic insect-mediated HGT [50]. Studies have also suggested the possibility of virus-mediated HGT from plants to other genomes via pathogen, transgenic bacteria (e.g., Agrobacterium tumefaciens), virus [51], fungi [52], and nematodes [53].
Studies have shown that adaptation of bacteria to host plant involves diversification and evolutionary processes, while switching from parasitism to mutualism [54]. The bacterial transition to intracellular lifestyle induce various ecological changes. The sequencing of bacterial genomes has yielded significant insights about bacterial population dynamics and evolution, by highlighting gene recombination, deletion and gene amplification events [54]. Moreover, it has been seen that bacteria classified in different phylogenetic clades differ in host adaptation. The co-integration of endosymbiont into host and adaptation to intracellular lifestyle render changes in bacterial genes, conferring the function of mutualism to bacteria. The endophytic association further makes the bacterial genome to co-evolve with the host genome, characterized by reduction in bacterial genome evolution [54]. Moreover, studies have shown that the HGT event occurring in symbiotic and pathogenic bacteria is responsible for functional divergence in different phylogenetic clades [55][56]. The host adaptation by endophytes confers distinct advantages to associated microbes and helps in its adaptation and survival. The inclusion of new functions via HGT (gene duplication and functional divergence) facilitates greater interaction with the respective host organism [57].

4. Recent Approaches to Detect HGT in Genomes

The identification and annotation of complete genomes in biological organisms have shown the frequent occurrence of HGT events, resulting in a chimeric organism, with multiple DNA from different genomes. Considering the emerging importance of HGT events in the evolutionary process [58], understanding the HGT phenomenon is crucial to learn about novel functions, such as the emergence of antibiotic resistance [59] and prediction of gene functions [60]. Several approaches are available for the identification of HGT events in whole genomes, depending on the type of HGT process. These methods are enumerated below:
Studying gene distribution patterns: Gene transfer between different species results in the acquisition of new genes. Therefore, studying gene distribution patterns with uneven occurrence might lead to the identification of HGT events. However, uneven distribution patterns might also be caused by processes such as sequence divergence or gene loss [58]. Additionally, analysis of gene distribution patterns can be used to detect homologous gene recombination.
Comparison of phylogenetic trees: One possible method to determine the occurrence of HGT event is the analysis of phylogenetic trees of different genes, based on the assumption that HGT events might lead different genes to have different evolutionary trees. However, this method is not accurate since various factors, such as ortholog/paralog misidentification, occurrence of convergence, and incorrect alignment of gene sequences [61][62][63], might lead to incorrect conclusions. Although the phylogenetic methods do not always correctly predict the HGT events among closely related species, it is still a method of choice in analyzing the genomes of biological organisms. Moreover, this method is based on extensive information about the number of genes.
Studying unusual genome composition: A consistent uniformity is present in genome composition and phenotype and the presence of foreign genes due to HGT events can be detected by identifying genomic regions with unusual composition (e.g., codon usage) [64]. This method requires the complete genome sequence of one species for the estimation of HGT events. However, since non-uniform genome composition might also result due to mutation, natural selection, and HGT [65], as well as the presence of biological vectors (e.g., bacteriophages), this method is not reliable for predicting HGT events between species with similar genome composition and HGT events that occurred long ago [58].
Similarity search between genomes: A common method for the identification of HGT events in genomes is to search for maximum similarity between genes. HGT is very likely between genes of distantly related species. This is a common and fast method, however, its disadvantages include less accuracy and uncertainty regarding the number of best matches to search for, identification of orthologs, and uncertainty with multi-domain proteins [58][66]. For an effective and methodical study to identify HGT events in biological species, one or more of the above mentioned methods were used in combination. However, the methods depend on the different type of gene transfer and their occurrence during the course of evolution.

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Subjects: Biotechnology & Applied Microbiology
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Pragya Tiwari
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Hanhong Bae
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