Trends in Genetics
OpinionHorizontal Gene Transfer in Eukaryotes: Not if, but How Much?
Section snippets
Horizontal Gene Transfer in Eukaryotes and Prokaryotes
Horizontal gene transfer (HGT) (see Glossary) is the nonlineal movement of genetic material across the web of life that creates reticulate gene phylogenies. This process is of high interest because it can drive functional innovation through the introduction of novel genes and pathways [1]. HGT is a common occurrence across all domains of life; however, most transfers are ephemeral and not transmitted to the next generation. For example, they may be introduced into somatic tissue in a
HGT in Microbial Eukaryotes
Most microbial eukaryotes (protists and some fungi) are unicellular, predominantly asexual, and represent a taxonomically diverse assortment of organisms and lifestyles whose members comprise the earliest divergences within all major multicellular lineages, such as animals, plants, and seaweeds [13]. Protist and algal clades include a number of other major evolutionary transitions, such as from free-living to pathogenic (e.g., oomycetes [14]), mesophilic to extremophilic (ice algae [15]), and
Examples of HGT Driving Adaptive Evolution in Microbial Eukaryotes
With significantly more protist, algal, and yeast genomic data and associated studies available, it is possible to investigate robustly supported instances of HGT (Figure 1) to assess if they are adaptive gains associated with environmental shifts and, in some cases, to explore how HGT happens (Box 2). Here, we explore these cases and identify trends in terms of gain of function, recognizing that most HGTs are destined for loss and, in some cases, when neutral or nearly neutral, may later
HGTs and Major Evolutionary Transitions
Not only is HGT a ubiquitous process implicated in novel adaptations throughout the web of protist life, but HGT-driven adaptations are also an integral part of major evolutionary transitions. Two of the most noteworthy in this respect are the origin of primary plastids and the colonization of land by plants. The primary endosymbiosis of a cyanobacterium by a phagotrophic protist resulted in the canonical plastid in the ancestor of Archaeplastida [56., 57., 58.]. This endosymbiotic event is
Extent of HGT in Protist Genomes Based on Available Data
Although generally underrepresented in the literature, a majority of eukaryote diversity is microbial. Protists comprise a polyphyletic assemblage of many kingdom-level groupings of organisms, and due to their largely unicellular and asexual nature, they form the bridge between prokaryotes and more complex eukaryotes, maintaining genomic features and traits of each domain. Thus, focusing on them with respect to HGT is the logical next step to building on the many prokaryotic HGT studies and
Concluding Remarks
Although hotly disputed when it first rose to prominence, the hypothesis of HGT in eukaryotes, in particular protists, has been substantiated by multiple high-quality analyses of genomes across the tree of life. The time is ripe to move beyond the debate ‘if HGT’ to focusing on its adaptive and evolutionary implications and filling ‘genome gaps’ in the eukaryotic tree of life (see Outstanding Questions). Based on published analyses of HGT, the incidence of these gene transfers varies from 0.04
Acknowledgments
D.B. is supported by a research grant from the National Aeronautics and Space Administration (NASA; 80NSSC19K0462) and a National Institute of Food and Agriculture-US Department of Agriculture Hatch grant (NJ01170). J.V.E. is supported by the NASA Future Investigators in NASA Earth and Space Science and Technology (FINESST grant 80NSSC19K1542). We are grateful to three anonymous reviewers for their valuable comments on the manuscript.
Glossary
- CRASH
- an informal phylogenetic grouping [1] that includes a diverse collection of photosynthetic and nonphotosynthetic organisms from the following lineages: Cryptophyta, Rhizaria, Alveolata, Stramenopila, and Haptophyta.
- Dark genes
- genes that are either novel to science, that is, they do not share significant sequence identity with proteins in large databases such as the manually curated UniProt, or are too highly diverged to allow identification of putative homologs. These genes may confer
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