Prokaryotic Contributions to Eukaryote Evolution: Sharing is Caring

June 29, 2023

Galdieria sulphuraria under microscopy.
Galdieria sulphuraria has acquired many genes from bacteria and archaea.
Source: Wikipedia
Horizontal gene transfer (HGT) between prokaryotic organisms, such as bacteria, is a common way to generate evolutionary innovations. The transfer is termed horizontal because it occurs between coexisting cells, rather than vertically to progeny during replication. Notably, HGT can help antibiotic resistance genes sweep through a population, which, in part, perpetuates antimicrobial resistance (AMR).

HGT can have other outcomes and is by no means restricted to gene transfers between bacteria. Transfer of genetic material from bacteria, as well as archaea, to eukaryotes is also possible, and scientists are discovering that such inter-kingdom HGT has led to amazing eukaryotic innovations and adaptations. These events are more common than originally believed and are gaining greater appreciation for their contributions to shaping the evolution of eukaryotic organisms.

Getting By in Extreme Environments

Horizontal gene transfer from bacteria is thought to be especially prevalent in extremophiles, organisms that can thrive under ‘extreme’ environmental conditions. For example, the single-celled eukaryotic alga Galdieria sulphuraria thrives in hot, salty, acidic springs. When researchers sequenced its genome, they identified at least 75 genes that were probably acquired from bacteria and archaea. However, the alga didn’t just acquire these genes—it made them its own through a process called gene expansion.

Gene expansion occurs when genes undergo duplications, during which mutations can accumulate in 1 of the pairs. As a result of these mutations, the expressed protein may develop a new function in a process known as neofunctionalization. In eukaryotes, functional novelty usually results from the independent duplication of existing genes. However, eukaryotic cells can also acquire new genes from bacteria. In this case, proteins develop new functions quickly, allowing evolutionary leaps to occur.

G. sulphuraria has many traits that allow it to live under extremely hot, salty and acidic conditions, and many seem to have come from a taxonomically diverse range of bacteria and archaea; altogether, researchers estimate that at least 5% of G. sulphuraria’s protein-coding genes were acquired horizontally. For example, its adaptation to heat may have occurred partially by acquiring an archaeal ATPase gene family, which the alga subsequently duplicated and diversified into separate gene families. ATPases allow cells to harness energy from ATP for use in myriad chemical reactions. Although the function of archaeal ATPase is unclear, researchers identified that heat tolerance increases with the number of ATPase gene copies in archaea, hinting at the importance of these genes for life at high temperatures.

Besides heat tolerance, G. sulphuraria also has a highly versatile metabolic profile, allowing it to thrive in the presence of heavy metals, under very salty conditions and on many energy sources. For example, it has acquired enzymes to detoxify arsenic and mercury, and an enzyme to produce betaine, a compound that can protect bacteria from salty surroundings. It can also produce energy using photosynthesis, or by respiring over 50 different carbon sources, thanks to transporter proteins and entire pathways acquired from both bacteria and archaea. Indeed, the researchers showed that G. sulphuraria’s pool of gene donors included many extremophiles that are used to the challenging conditions that G. sulphuraria has evolved to inhabit.

A Helping Hand for Herbivores

Tetranychus urticae, the spider mite.
Tetranychus urticae, the spider mite, can detoxify plant compounds using an enzyme of bacterial origin.
Source: Wikimedia Commons
Besides facilitating extremophilic adaptation, bacterial genes can also help organisms gain the upper hand in evolutionary arms races, where 2 organisms evolve in parallel, always thwarting each other’s latest innovations. A classic example of this is plants and their arthropod ‘pests,’ like mites, moths and butterflies. Plants protect themselves from herbivory by producing chemical defenses such as hydrogen cyanide (HCN), while arthropods evolve elaborate ways to evade these defenses and keep munching on their plant food.

For a long time, the enzyme that arthropods use to detoxify HCN was unknown. In 2014, researchers discovered that the enzyme was transferred from bacteria, where its original function was to synthesize sulphur-containing amino acids. Herbivorous arthropods appear to have co-opted the enzyme to detoxify cyanide. This allows them to eat plants that produce protective HCN compounds. 

In the study, which was published in eLife, researchers used the spider mite Tetranychus urticae to isolate the enzyme responsible for cyanide detoxification, named Tu-CAS. When they searched the already-published arthropod genomes for the enzyme’s genetic sequence, they could only detect close homologues in the genomes of moths and butterflies, collectively known as lepidopterans, which are distant relatives to T. urticae. However, the researchers were uncertain whether the transfer happened once, in an ancestor of both mites and lepidopterans, or whether both groups experienced a transfer event independently. Close relatives of mites and lepidopterans do not have versions of Tu-CAS, meaning that over 13 gene losses would have had to occur if the ancestor had the Tu-CAS gene. According to the principle of parsimony in biology, 2 transfers are more likely to occur than 13 losses; thus, the researchers hypothesized that the transfer probably occurred at least twice.

HGT is also being increasingly appreciated as a force in the evolution of herbivorous arthropods to withstand and adapt to their plant hosts and food sources. Besides the case of Tu-CAS, many other examples of HGT from prokaryotes to arthropods have been documented, allowing them to expand into new plant organs, degrade tough plant cell walls and assimilate plant-derived compounds.

Suddenly I See: Bacteria and the Vertebrate Eye 

Another striking example of gene transfers leading to evolutionary innovations involves bacteria, vertebrates and the eye. Evolution by natural selection is thought to proceed step-by-step, but how this could happen with complex structures such as the vertebrate eye is unclear.

Diagram of vertebrate eye.
The vertebrate eye is dazzlingly complex, and how it evolved remains a puzzle.
Source: Wikimedia Commons

By analyzing over 900 genomes from organisms spanning the tree of life, researchers showed how a bacterial gene helped the vertebrate eye to evolve into its modern glory. One key feature of the vertebrate eye, compared to the eyes of invertebrates, is the interphotoreceptor retinoid-binding protein (IRBP). By transporting retinoids (compounds derived from vitamin A, such as retinol and retinal, that are continuously broken down and regenerated to maintain working vision) between photoreceptors and the retinal pigment endothelium, IRBP enables cells in the vertebrate eye to become physically separated and thus specialized in function.

The gene that facilitated the evolution of IRBP appears to have come from bacteria, though researchers could not pinpoint the exact strain or group. In bacteria, the gene encodes a peptidase, an enzyme that breaks down proteins. After the transfer event, parts of the gene mutated so that the protein underwent duplications and neofunctionalizations, giving rise to vertebrate IRBP. During the Cambrian explosion 538 million years ago, vertebrates underwent major diversification over a period of around 20 million years. The gene transfer event is thought to have occurred before the Cambrian explosion, which may explain why IRBP is found in all extant vertebrates.

What Else Do We Owe to Prokaryotes?

The contributions of prokaryotic organisms to eukaryotic evolution are becoming increasingly well-understood, as more and more sequencing data become available for a greater variety of organisms. However, these inferences are not always easy to make, as contamination of samples with DNA from the environment can lead to misguided conclusions about the prevalence of foreign genes. Nevertheless, it appears that eukaryotes have prokaryotes to thank for some very important evolutionary innovations, some of which we have yet to discover.
Microbes are amazing, inhabiting some of the most diverse ecosystems and metabolizing some of the most unlikely products. Learn more about ecology, evolution and biodiversity at the microbial level by browsing additional content. 

Author: Vilhelmiina Haavisto

Vilhelmiina Haavisto
Vilhelmiina Haavisto is a Ph.D. student at ETH Zürich in Switzerland, where she works with marine microbial communities.