Trends in Genetics
Volume 36, Issue 12, December 2020, Pages 915-925
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Opinion
Horizontal Gene Transfer in Eukaryotes: Not if, but How Much?

https://doi.org/10.1016/j.tig.2020.08.006Get rights and content

Highlights

  • Horizontal gene transfer (HGT) is emerging as a significant contributor to eukaryotic genomes, challenging previous assertions that HGT is restricted to prokaryotes and only relevant to eukaryotes during organellogenesis.

  • HGTs often confer an adaptive advantage to the ‘host’ organism, and many of these adaptations significantly enhance metabolic pathways, leading to lifestyle shifts or survival in highly fluctuating environments.

  • Protists that exhibit a range of lifestyles, including photosynthesis, mixotrophy, polyextremophily, and parasitism, comprise the earliest divergences in major multicellular lineages, making them models for understanding the role of HGT in evolutionary transitions.

  • HGT represents, on average, about 1% of protist gene inventories, although this ‘rule’ needs to be tested in the future using more data and a standardized pipeline for HGT quantification.

Horizontal gene transfer (HGT), the movement of genetic material across branches of the tree of life, is well established in prokaryotes and uncontroversial. This is explained in part by relatively compact prokaryote genomes that facilitate assembly and gene prediction, resulting in thousands of complete genomes for analysis. By contrast, their large and often complex genome structure have thwarted HGT studies of eukaryotes. The tide has recently turned with the availability of sufficient high-quality genome data to address quantity and quality of HGT in these taxa. Here, we argue that HGT is a small but significant player in the evolution of microbial eukaryotes and provide examples where HGT has facilitated gain of adaptive functions and in some cases, underpinned major lifestyle transitions.

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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