Decomposers are crucial for keeping Earth habitable, breaking down dead biomass and returning key nutrients, like carbon, nitrogen and phosphorus, back into the ecosystem. Most decomposers, including fungi, survive through osmotrophy — a means of feeding by absorbing dissolved nutrients rather than engulfing prey. But how this method of feeding repeatedly arose across the eukaryotic tree of life remains unclear.
Now, researchers from the Okinawa Institute of Science and Technology (OIST) in Japan, the University of Oxford in the UK, the Barcelona Supercomputing Center, the Institute of Research in Biomedicine (IRB Barcelona), and the Universitat Oberta de Catalunya in Spain, among other institutions, have reconstructed the deep history of osmotrophic specialization in eukaryotes (organisms with complex cells). Their findings suggest that four groups of eukaryotes which have specialized in osmotrophy first arose between 720 million and 1 billion years ago and that they share a toolkit of genes involved in osmotrophic functions. Their results also indicate that horizontal gene transfer, that is, the process by which genes move from one species to another, played an important role in the evolution of these functions.
The paper, recently published in Nature Ecology and Evolution , adds to the slow shift in how biologists think about how life evolves and how genes are inherited.
"Horizontal gene transfer used to be framed as just a peculiarity that happens in bacteria, with eukaryotes passing genes down vertically to their offspring," says Professor Gergely Szöllősi, who leads the Model-based Evolutionary Genomics Unit at OIST. "Instead, we show that even in eukaryotes, the branches of the tree of life can, and do, exchange genetic material, and those exchanges can allow entirely new ways of making a living to take hold."
Digging deep into the history of decomposers
In this research, the team compared the genomes of species within four distantly related osmotrophic groups. Apart from Fungi, which is the most well known and studied of these groups, three other eukaryotic lineages also transitioned towards a specialised osmotrophic lifestyle: Pseudofungi, Labyrinthulea and Teretosporea.
"Despite siting at opposite sides of the eukaryotic tree, a suite of traits have repeatedly evolved in these groups as an adaptation to an osmotrophic lifestyle, including filamentous networks and tough cell walls," says lead author, Eduard Ocaña-Pallarès, a former post-doc in Szöllősi's Unit, now a Ramón y Cajal research fellow at Universitat Oberta de Catalunya. "Importantly, they also share a common metabolic toolkit necessary for osmotrophy, including genes involved in nutrient uptake, ion regulation and anabolic metabolism. We wanted to know where these shared genes came from."
By analyzing hundreds of gene trees, the researchers identified 166 cases where horizontal gene transfer was likely to have occurred between these groups, involving genes mostly related to metabolic functions. In particular, horizontal gene transfer occurred predominantly between Fungi and Pseudofungi, and between Labyrinthulea and Teretosporea.
"It could be that we see 'transfer highways' between these groups due to their shared terrestrial and aquatic ecology, respectively," suggests Szöllősi.
Unanswered questions
Looking forward, the researchers pinpoint important directions for future research, including deciphering the actual function of these shared genes within each group.
A further mystery to solve is how horizontal gene transfer happened between these lineages. "For example, was it driven by the acquisition of foreign DNA directly from the environment or through viral intermediates?" says Ocaña-Pallarès. "The main question is not anymore if horizontal gene transfer takes place in eukaryotes, but how it occurs. We still know very little about the mechanisms driving this process in eukaryotes."
