Chromatin is the ensemble of genomic DNA and a large number of proteins. Despite its fundamental role in biology of eukaryotic cells, scientists lack a comprehensive understanding of chromatin evolution.
In almost every human cell, two meters-long DNA has to fit within a nucleus that is just 8 millionths of a meter wide.
Like wool around a spool, the extreme space challenge requires DNA to wrap around structural proteins called histones.
This coiled genetic architecture, known as chromatin, protects DNA from damage and has a key role in gene regulation.
Histones are present in both eukaryotes, living organisms that have specialized cellular machinery such as nuclei and microtubules, and archaea, another branch of the tree of life consisting of single-celled microbes that are prokaryotic, meaning they lack a nucleus.
In eukaryotic cells, histones are modified by enzymes, continuously shapeshifting the genomic landscape to regulate gene expression and other genomic processes.
Despite this fundamental role, the exact origin of chromatin has been shrouded in mystery.
“To infer the origin and evolutionary diversification of eukaryotic chromatin, we performed a joint comparative analysis of histone proteomics data from 30 different eukaryotic and archaeal species, including new data for 23 species,” said Dr. Xavier Grau-Bové, a postdoctoral researcher in the Centre for Genomic Regulation at the Barcelona Institute of Science and Technology, and his colleagues from Spain, Austria, France and Canada.
“In parallel, we analyzed the complement of chromatin-associated gene families in an additional 172 eukaryotic genomes and transcriptomes.”
They found that prokaryotes lack the machinery necessary to modify histones, suggesting archaeal chromatin at the time could have played a basic structural role but did not regulate the genome.
In contrast, they found ample evidence of proteins that read, write and erase histone modifications in early diverging eukaryotic lineages such as the malawimonad Gefionella okellyi, the ancyromonad Fabomonas tropica, or the discoban Naegleria gruberi, microbes that had not been sampled until now.
“Our results underscore that the structural and regulatory roles of chromatin are as old as eukaryotes themselves,” Dr. Grau-Bové said.
“These functions are essential for eukaryotic life — since chromatin first appeared, it’s never been lost again in any life form.”
“We are now a bit closer to understanding its origin, thanks to the power of comparative analyses to uncover evolutionary events that occurred billions of years ago.”
Using the sequence data, the researchers reconstructed the repertoire of genes held by the last eukaryotic common ancestor, the cell that gave rise to all eukaryotes.
This living organism had dozens of histone-modifying genes and lived between one and two billion years ago on Earth.
The scientists hypothesize that chromatin evolved in this microbe as a result of selective pressures in the primordial environment of Earth.
“Viruses and transposable elements are genome parasites that regularly attack DNA of single-celled organisms,” said Dr. Arnau Sebe-Pedrós, a researcher in the Centre for Genomic Regulation at the Barcelona Institute of Science and Technology.
“This could have led to an evolutionary arms-race to protect the genome, resulting in the development of chromatin as a defensive mechanism in the cell that gave rise to all known eukaryotic life on Earth.”
“Later on, these mechanisms were co-opted into elaborate gene regulation, as we observe in modern eukaryotes, particularly multicellular organisms.”
The team’s paper was published in the journal Nature Ecology and Evolution.
X. Grau-Bové et al. A phylogenetic and proteomic reconstruction of eukaryotic chromatin evolution. Nat Ecol Evol, published online June 9, 2022; doi: 10.1038/s41559-022-01771-6
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