Functional horizontal gene transfer from bacteria to eukaryotes

Key Points

  • Genome fragments are sometimes transferred from bacteria to eukaryotes via horizontal gene transfer (HGT).

  • When these DNA fragments contain genes, these genes can retain their functionality in some cases.

  • If these bacterial sequences are maintained for long periods of time, they can acquire eukaryotic features such as introns.

  • If the eukaryotic recipient retains a stable bacterial endosymbiont, these HGT events can compensate for genome reduction in the endosymbiont.

  • These HGT events can also enable the eukaryotic recipient to protect itself from other organisms, survive in new environments or use new food sources.

  • Further study of neglected eukaryotic groups will help to clarify the frequency of bacteria–eukaryote HGT.

Abstract

Bacteria influence eukaryotic biology as parasitic, commensal or beneficial symbionts. Aside from these organismal interactions, bacteria have also been important sources of new genetic sequences through horizontal gene transfer (HGT) for eukaryotes. In this Review, we focus on gene transfers from bacteria to eukaryotes, discuss how horizontally transferred genes become functional and explore what functions are endowed upon a broad diversity of eukaryotes by genes derived from bacteria. We classify HGT events into two broad types: those that maintain pre-existing functions and those that provide the recipient with new functionality, including altered host nutrition, protection and adaptation to extreme environments.

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Figure 1: Functional horizontal gene transfer events in eukaryotes.
Figure 2: How foreign DNA gains functionality in eukaryotes.
Figure 3: Horizontal gene transfer events targeting peptidoglycan bonds are common across eukaryotes.
Figure 4: Schematic diagrams of maintenance transfers and innovation transfers.

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Acknowledgements

F.H. was supported by the Fulbright Commission and a fellowship from the European Molecular Biology Organization (EMBO; ALTF 1260–2016) while writing this Review. J.P.M. was supported by grants from the US National Science Foundation (IOS-1256680 and IOS-1553529), the US National Aeronautics and Space Administration (NASA) Astrobiology Institute (NNA15BB04A) and the Gordon and Betty Moore Foundation (GBMF5602).

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F.H. and J.P.M. researched data for the article, made substantial contributions to discussions of the content, wrote the article and reviewed and/or edited the manuscript before submission.

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Correspondence to Filip Husnik or John P. McCutcheon.

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Supplementary information S1 (table)

HGT events from bacteria to eukaryotes. (XLSX 33 kb)

Glossary

Horizontal gene transfer

(HGT). Movement of genetic material between organisms (also called lateral gene transfer) via non-vertical (not parent-to-offspring) transmission.

Germ line

The specialized cellular lineage in multicellular sexual organisms that is used to pass on genetic material to the progeny.

Endosymbionts

Organisms living within the body or cells of another organism.

Long-branch attraction

A phylogenetic artefact that causes distantly related lineages (often on long branches) to be incorrectly inferred as closely related in phylogenetic trees.

Conjugation

Gene transfer from a donor to a recipient by direct cell-to-cell contact, such as plasmid transfer between two bacterial cells.

Transduction

Gene transfer carried out by a virus, such as a bacteriophage, transferring DNA from one bacterium to another.

Transformation

Direct acquisition of DNA from the environment through the cell membrane.

Gene transfer agents

Bacteriophage-like elements that package random DNA regions from a host cell and transfer them to a recipient cell.

Non-homologous end joining

(NHEJ). A pathway for the direct repair of double-strand DNA breaks without a homologous template.

Nuclear mitochondrial transfers

(numts). Transfers of mitochondrial DNA into the nuclear genome of a eukaryotic host; the encoded genes often become non-functional.

Nuclear plastid transfers

(nupts). Transfers of plastid DNA into the nuclear genome of a eukaryotic host; the encoded genes often become non-functional.

Transposable elements

DNA sequences (also known as jumping genes) that can move within a genome (and sometimes also between genomes) by a 'cut and paste' (DNA transposons) or a 'copy and paste' (retrotransposons) mechanism.

Organellogenesis

The process by which an endosymbiont becomes an organelle, in part by becoming (nearly) irreversibly integrated with its host cell at both a genetic and cell biological level.

Reproductive manipulators

Bacteria, such as Wolbachia spp., that are transmitted in the egg cytoplasm of arthropods and nematodes and shift the sex ratio of the host population.

Peptidoglycan

A structural matrix in bacterial cell walls formed by alternating N-acetylglucosamine (NAG) and N-acetylmuramic acid (NAM) residues, where peptide chains of up to five amino acids link NAM to other NAM-connected peptides.

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Husnik, F., McCutcheon, J. Functional horizontal gene transfer from bacteria to eukaryotes. Nat Rev Microbiol 16, 67–79 (2018). https://doi.org/10.1038/nrmicro.2017.137

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