Researchers quantify rate of essential evolutionary process in the ocean

(Press-News.org) The movement of genetic material between organisms that aren’t directly related is a significant driver of evolution, especially among single-celled organisms like bacteria and archaea. A team led by researchers at Bigelow Laboratory for Ocean Sciences have now estimated that an average cell line acquires and retains roughly 13 percent of its genes every million years via this process of lateral gene transfer. That equates to about 250 genes swapped per liter of seawater every day.

The new study, recently published in The ISME Journal, provides the first quantitative analysis of gene transfer rates across an entire microbiome. It calls into question the strict classification lines drawn between individual species. It also confirms that many transferred genes have direct ecological benefits, highlighting how this process enables microbes to adapt to new environments and furnishes them with valuable capacities, such as the ability to access essential nutrients.

“All the processes that microbes drive on our planet have evolved, and that evolution, to a large extent, is driven by lateral gene transfer, but the process is very difficult to study, and no one has been able to put numbers to the process,” said Bigelow Laboratory Senior Research Scientist Ramunas Stepanauskas, the study’s lead author. “We know in general how it works, but we had no idea if you take a drop of seawater, are genes being exchanged once a minute or once a year or once a million years? That was completely unknown — until now.”

Genes can be transferred laterally through multiple mechanisms, including the uptake of floating genetic material in the environment, direct transfer between cells, and the injection of foreign DNA into a host by a virus.

Scientists have struggled to quantify those processes, though, given the immense diversity of microbial life. Traditional “evolutionary tree” approaches can be used to study the transfer of specific, widespread genes — a handful at a time — but are impractical for studying an entire ecosystem. Likewise, the common method for studying microbial genomes, metagenomics, works by stitching together assemblies of related, “typical” genes, meaning it actively excludes transferred genes that are rare or come from unrelated organisms.

Advances in computational modeling and single-cell genomics, though, have allowed scientists to begin answering these questions.

The team used genomes of 12,000 randomly-sampled microbial cells from the tropical and subtropical surface ocean sequenced by Stepanauskas’s team at the Single Cell Genomics Center (SCGC). The unique dataset is one of the largest compilations of microbial genomes ever produced. They compared the distribution of shared genes in that real-world data with a computer model that assumed that genes can only be transferred vertically between parents and offspring, not laterally.

“This project was an exciting opportunity to think differently about how to measure an essential yet elusive evolutionary process that shapes the microbial component of ecosystems globally,” said Siavash Mirarab, a professor at UC San Diego and a co-author on the study whose team led the development of the model.

The approach confirmed that most genes are exchanged between closely related cells, but not all. Some genes with obvious ecological value can be successfully transferred between microbes that are as distantly related to each other as humans to kangaroos. For example, they found evidence of microbes acquiring novel genes that enable them to uptake new sources of phosphorus in the phosphorus-limited Sargasso Sea.

The findings also show evidence of the exchange of genes that encode ribosomal RNA, the cellular machinery responsible for protein synthesis. That, Stepanauskas said, was surprising given that those genes are often used as metrics for biological diversity exactly because scientists assumed they were not engaged in lateral transfer.

In the future, the team hopes to expand this approach into new environments and tease apart differences between lineages, transfer mechanisms, and ecosystems. That work could have significant biotechnology implications by revealing how nature effectively and rapidly engineers cells for different environments and processes. To that end, SCGC is continually improving and scaling up its analytical capabilities to enable the large-scale studies that work will require.

“Answering these questions may have become possible, but only if we can continue to improve our modeling toolkit,” Mirabab said.

“I see this as just the beginning,” Stepanauskas added. “We finally have sufficient data to start doing this kind of quantitative analysis, but we still need to go much further to say how frequently specific kinds of microbes do it, what processes are involved, and how we can use this knowledge in environmental stewardship and bioeconomy.”

Funding for this work was provided by the Simons Foundation, National Science Foundation, and the National Institutes of Health. The study also features researchers from Woods Hole Oceanographic Institution, University of Pretoria, Wellesley College, and Massachusetts Institute of Technology.

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