Oeiras, 02.09.2015

American Palaeontologist and writer Stephen Jay Gould developed an idea early in his career that evolution would sometimes take great jumps, though most of the time evolution proceeded by small steps.  This theory, called “Punctuated Equilibrium”, significantly revised the standard idea that evolution proceeded exclusively by small changes over long periods of time and has kept scientists debating the importance of these jumps, over the past 50 years. In a paper recently published in Nature, scientists have carried out one of the biggest ever analyses of genomes of every kind of living organism and have been able to map the evolutionary history of eukaryotic genes in the greatest detail ever, showing that indeed there have been several evolutionary jumps in the early history of life on the planet. The study was coordinated by Bill Martin, Professor of the University of Dusseldorf, and a visiting professor at ITQB. ITQB Alumna Filipa Sousa is also a co-author.

“Eukaryotes (large cells with DNA packed into a nucleus) are one boring kind of carbon and energy metabolism in a million (more, actually) different shapes and sizes. Prokaryotes are a million (not quite that many, but figuratively) kinds of carbon and energy metabolism in one boring shape and size” said project leader, Bill Martin. “We asked the question, How have these differences come about, and what can genome sequences tell us about it?”

“What we find is that genes flow very differently in the two systems.  In prokaryotes, the genomes evolve by extensive gene spread without respect for species boundaries.  This is called lateral gene transfer (LGT for short) and this is how prokaryotes have such diversity in their metabolic systems.  The big surprise of the study was that eukaryotes, don’t engage in this kind of continuous gene swapping nearly as much – though when they do, it’s a really, really important event and in early evolution, it corresponded to the origin of organelles.  These events were huge evolutionary leaps”, explains Bill Martin.

Eukaryotes differ from prokaryotes in many ways, none more important than the circumstance that eukaryotes harbour organelles within their cells that are the remnants of endosymbiotic bacteria. All eukaryotes harbour mitochondria, also known as the powerhouse of the cell. In recent years scientists have learned that the origin of mitochondria traces to the origin of the eukaryotic lineage itself, an event that occurred perhaps 1.6 billion years ago. The study shows that when eukaryotes acquired their mitochondria, there was a massive influx of genes from that endosymbiont to the chromosomes of the host cell.

Later, at the origin of the plant lineage, it was the same story all over again. Chloroplasts also arose from an endosymbiosis, one that gave birth to the whole plant kingdom, and during that symbiosis, there was another massive influx of genes from the chloroplast ancestor (a cyanobacterium) to the nucleus. 

Thus, eukaryotes are chimaeras, hybrids of very different kinds of cells, which were forged into one by endosymbiosis and gene transfer. Furthermore, the new findings show that once those symbiotic mergers took place, a slow process of gene loss set in. But in different evolutionary lineages, different genes were lost. This is called "differential loss" and it gives rise to very sparse distributions of genes across lineages. 

So if chloroplasts and mitochondria were endosymbionts, who was the host? "An archaeon", says Giddy Landan, senior bioinformatician at the University of Kiel, Germany, "we just can't tell which one".  The study took a statistical approach to uncovering eukaryote gene origins, looking for strong trends in the data that stand out above background noise. The new study looks not only at gene trees, but also at gene distributions, setting it apart from earlier work on the topic. 

Bill Martin concludes: "The prokaryotes and the eukaryotes have coexisted in the same environments on Earth for over a billion and a half years, but they live in what are effectively two different and disconnected genetic worlds." The only significant level of gene mixing between prokaryotes and eukaryotes occurred at the origins of chloroplasts and mitochondria. Asked to sum up the importance of the study in one short sentence, he surmises: "Endosymbiosis made the difference between prokaryotes and eukaryotes".

Original Article

Nature 524, 427–432 (27 August 2015) doi:10.1038/nature14963

Endosymbiotic origin and differential loss of eukaryotic genes

Chuan Ku, Shijulal Nelson-Sathi, Mayo Roettger, Filipa L. Sousa, Peter J. Lockhart, David Bryant,  Einat Hazkani-Covo, James O. McInerney, Giddy Landan & William F. Martin    

See also News and Views: Evolution: Gene transfer in complex cells by J.M. Archibald