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Eukaryotic acquisition of a bacterial operon

Jacek Kominek, Drew T. Doering, Dana A. Opulente, Xing-Xing Shen, Xiaofan Zhou, Jeremy DeVirgilio, Amanda B. Hulfachor, Cletus P. Kurtzman, Antonis Rokas, Chris Todd Hittinger

Posted on: 5 October 2018 , updated on: 6 October 2018

Preprint posted on 24 August 2018

Article now published in Cell at http://dx.doi.org/10.1016/j.cell.2019.01.034

A HOT finding: iron uptake by budding yeast made possible through horizontal transfer of a bacterial operon.

Selected by Lauren Neves

Categories: evolutionary biology

Background

Horizontal gene transfer (HGT) is the movement of genetic material between organisms through processes other than by transmission from parent to offspring. HGT was first described in E. coli in 1947 (1) and has since been established as an important mechanism for environmental adaptation in prokaryotic organisms. Lateral transmission of genes conferring antibiotic resistance, virulence factors, and metabolic genes have allowed bacteria to thrive across many diverse conditions (2).

While HGT occurs frequently among prokaryotes, such transfer to eukaryotic organisms is far more rare. This is likely due to fundamental differences in genetic architecture and transcriptional regulation between these organisms. Eukaryotic transcription is spatially and temporally separated from translation and mRNAs must undergo extensive processing prior to release in to the cytosol. On the other hand, bacterial transcription and translation are tightly coupled in the cytosol and lack RNA processing signals present in eukaryotic genes. Additionally, bacterial genes are often transcribed as operons: physically linked clusters that share a single regulatory region and produce a single polycistronic (multi-gene) transcript. Ribosome binding sites within these transcripts allow for translation of all operon genes. Eukaryotes typically transcribe genes as individual RNA units and lack the machinery to recognize prokaryotic ribosome binding sites.

Although rare, horizontal transfer from prokaryotic to eukaryotic cells has played an important role eukaryotic adaptation. For example, the budding yeast URA1 gene, which is required for uracil biosynthesis, was likely acquired from lactic acid bacteria (3). However, until now, cases of bacteria-to-eukaryotic HGT have been limited to single genes. Kominek, Doering, and colleagues find evidence for the first known example of horizontal operon transfer (HOT) in which a functional bacterial operon is transmitted into budding yeast. They show that this operon, which encodes an iron chelator biosynthesis pathway, underwent structural and regulatory changes that allow yeast to maintain active expression as a set of linked genes.

 

Key findings

Iron functions as an essential cofactor in many cellular processes, including respiration, DNA synthesis and translation. Many fungi and bacteria sequester iron from their environments by synthesizing small molecule iron-chelators known as siderophores.

In order to assess the conservation of iron acquisition genes across fungi, the authors surveyed the genomes over 175 fungal species. As siderophore production was thought to be absent in budding yeasts, the authors were surprised to identify a group of siderophore biosynthesis genes present throughout one group of budding yeasts (Wickerhamiella/Starmerella clade). Even more intriguingly, these genes are arranged co-linearly in the genome and encode a siderophore pathway that is far more commonly found in bacteria than fungi. Through a series of phylogenetic reconstruction analyses, the authors establish that this yeast group likely acquired siderophore biosynthesis genes through transfer of a complete operon from the bacterial family Enterobacteriaceae.

These yeast species not only harbor bacterial operon genes but also produce functional siderophores, indicating that these genes are fully transcribed and translated. Given the significant differences between bacterial and eukaryotic transcription, the authors asked how an operon could be successfully incorporated into the yeast genome as functional genes. Transcriptome-wide analysis revealed that operon genes are largely transcribed as individual capped and poly-adenylated mRNA, suggesting that many sequence modifications must have occurred throughout the operon that enabled conventional eukaryotic expression. Intriguingly, RNA-sequencing also revealed that the operon in Candida versatilis, which is most similar to bacterial operons, produces some overlapping and potentially bicistronic transcripts. The authors speculate that eukaryotic translational processes, such as leaky ribosome scanning and internal ribosome entry sites, may have aided initial expression of a polycistronic operon by ancestral yeast species.

 

Thoughts and future directions

In this preprint, Kominek, Doering, and colleagues describe the transfer of a siderophore biosynthesis pathway between Enterobacteriaceae and yeast in first known example of bacterial-to-eukaryotic horizontal operon transfer. Despite fundamental differences in prokaryotic and eukaryotic gene regulation, this operon has been “domesticated” for yeast transcription. I find this work particularly exciting as it may elucidate the mechanisms by which prokaryotic operons can transition to eukaryotic single gene RNA transcripts and shed light on the evolution of transcriptional regulation during the rise of eukaryotic organisms.

Some questions I have:

  • Can yeast express siderophore biosynthesis genes from a bacterial operon or from genes with reduced intergenic space? This may provide evidence for how the operon was maintained in ancestral yeast species soon after the HOT event.
  • Are there any conditions under which these yeast species robustly produce bicistronic transcripts? Are there any conditions under which polycistronic transcription of siderophore genes be advantageous in yeast?

 

Further reading

  1. Tatum, E.L. and Lederberg, J. (1947) Gene Recombination in the Bacterium Escherichia coli. J Bacteriol, 53, 673-684.
  2. Ochman, H., Lawrence, J.G. and Groisman, E.A. (2000) Lateral gene transfer and the nature of bacterial innovation. Nature, 405, 299-304.
  3. Hall, C., Brachat, S. and Dietrich, F.S. (2005) Contribution of horizontal gene transfer to the evolution of Saccharomyces cerevisiae. Eukaryot Cell, 4, 1102-1115.

 

Tags: horizontal gene transfer, iron uptake, operon, siderophore, yeast

doi: https://doi.org/10.1242/prelights.5073

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