LUCA, ses contemporains et leurs virus, 20 ans après / LUCA, its contemporaries and their viruses: 20 years after

Séminaire organisé par Patrick Forterre, David Prangishvili et Mart Krupovic (Institut Pasteur, Paris, France) du 9 au 14 mai 2016

Participants

Tamara Basta-Le Berre, Ryan Catchpole, Violette Da Cunha, Matthias Fischer, Patrick Forterre, Georges E. Fox, Morgan Gaia, Manolo Gouy, Matti Jalasvuori, Eugene V. Koonin, Mart Krupovic, Carlos Mariscal, Armen Y. Mulkidjanian, Jacques Oberto, Anthony M. Poole, David Prangishvili
Et François-Xavier Vives et Arnaud Mansir pour Transparences Production

Résumé

L’acronyme LUCA (the Last Universal Common Ancestor) a été créé lors d’un colloque organisé aux Treilles en 1996. Ce terme a été rapidement adopté par la communauté scientifique et a permis de populariser les recherches sur les premières étapes de l’évolution du vivant auprès du grand public et des journalistes. Cette année, le colloque organisé à l’occasion du vingtième anniversaire de LUCA a regroupé 18 participants, dont six chercheurs juniors venant de huit pays différents et de trois continents. Ce colloque a regroupé des évolutionnistes, des biochimistes, des spécialistes du génome, des virologistes et deux philosophes. Par rapport aux précédents colloques dédiés à LUCA (1996, 2006), le colloque de 2016 s’est également intéressé aux virus qui infectaient LUCA et ses contemporains. Nous savons en effet aujourd’hui, grâce à la biologie structurale comparative, que des virus infectant des bactéries, des archées ou des eucaryotes peuvent dériver de virus déjà présents au moment de la séparation de ces trois domaines. Si LUCA ne doit pas être confondu avec la première cellule, les données de génomique comparative montrent que LUCA était sans doute beaucoup plus simple que les cellules actuelles. Plus de la moitié des participants (11/18) n’étaient encore jamais venus aux Treilles et ont été enthousiasmés par l’organisation et l’environnement. La décision été prise de rédiger pour la revue « Biology Direct », dont l’un des participants est éditeur, un article de fond qui ferait le point sur les recherches concernant LUCA et qui serait cosigné par l’ensemble des participants. Cette rencontre a donc donné toute satisfaction à ces derniers qui ont souhaité que l’organisation du prochain colloque ait lieu à l’occasion des 25 ans de LUCA.

Summary

It has been twenty years since the term Last Universal Common Ancestor (LUCA) was coined during a meeting held at the Fondation des Treilles in 1996 (http://www-archbac.u-psud.fr/Meetings/LesTreilles/LesTreilles_e.html) and a key strand of the 2016 meeting celebrating this birthday focused on what we have learned in the past two decades. One of the central themes arising from the meeting is that our community better recognises the difficulty in reconstruction of very deep ancestral states. Consequently, the focus was has largely shifted away from trying to flesh out the parts list of genes or features possibly present in LUCA. Instead, the questions focused more on understanding relevant evolutionary processes or events at a much broader scale. In clear parallel to the study of human origins, it has become clear that we cannot easily trace features back to a singularity in time, but we are thinking of ways to understand an epoch that concluded with the emergence of the primary lineages of life.

Compte-rendu (en anglais)

The LUCA 2016 meeting gathered 18 participants, including 6 junior scientists, eight different countries and three continents. These include evolutionists, geneticists, biochemists and two philosophers.

After an historical perspective presented by Patrick Forterre who discussed how ideas have changed in the last two decades, the meeting started with the keynote lecture of George Fox, who discovered one of the three domains of life, the Archaea, together with Carl Woese in 1977. George Fox discussed how reconstruction of the evolution of the ribosome has made progress with the availability of structural data on the ribosome, and this provides a strong case in point. Comparative data do help to unravel the evolutionary steps leading to modern ribosomes, such that one can see beyond LUCA. Tamara Basta provided another layer of details, explaining how the minimal translation apparatus likely also included modifications to tRNA that are universal, some of which improve the fidelity of translation. Similarly, Ryan Catchpole presented data supporting a role for mobile elements in shaping bacterial translation, where it seems that formylation of methionine is best understood as having evolved via a gene addiction system rather than some inherent advantage to translation. The progress presented helps to flesh out in stunning details earlier stepwise models for the evolution of the ribosome that span from the late stages of an RNA world through to the early diversification of the domains of life.

As Patrick Forterre duly noted, there is a resurgence of interest in a much simpler LUCA, possibly more akin to Carl Woese and George Fox’s progenote. Indeed, few protein-coding genes unequivocally trace back to the LUCA, and results presented by Anthony Poole show that much the same picture arises if one instead focuses on noncoding RNA genes. In discussion, the amusing though insightful analogy was made by Mart Krupovic that the ribosome is a bit like finding an iPad in the middle ages – surely there was greater cellular complexity given the sophistication of translation by the time of LUCA, but perhaps much of the historical signal has been lost. In this regard, the insights from the philosopher Carlos Mariscal provided much food for thought; rather than bemoaning the lack of epistemic access to this deep past, he noted that the field itself has changed. In some areas, perhaps there has been a change in the explanatory project, away from the original goal of explaining the similarities across all life.

Both Violette Da Cunha and Morgan Gaia focused on this latter topic, which is still very much alive as a result of the revived debate on whether eukaryotes are just a derived group of Archaea (meaning there are only two primary domains) or whether the three primary domains of life that Carl Woese recognised remain relevant. Both focused on the impact of new sequence data, particularly from metagenomic data from Loki’s Castle, and whether these might in fact support the three-domain tree of life, not the two-domain tree, as proposed, when fast evolving species are removed from phylogenetic analysis of universal proteins.

Interestingly, a broader range signals may help to reconstruct the key stages in early evolution, with two exciting avenues being explored that linked LUCA to its environment. In considering the nature of the cellular membrane that would have separated LUCA from the environment, we are not closer to determine the likely chemical nature of the ancestral membrane, but Armen Mulkidjanian noted that the ionic composition of the cytoplasm suggests life arose in a potassium-rich environment, with rotary ATPases and development of ion-tight membranes being needed before cells could move into sodium-rich marine environments. Extending previous work on the temperature constraints of LUCA using ancestral reconstruction techniques, Manolo Gouy further fleshed out the environmental context of LUCA, with data showing that LUCA lived at moderate temperatures, and that thermophily likely evolved twice independently. This certainly raises the possibility that the membranes of Archaea are not some evolutionary relic of the transition to membranes, but are instead a result of thermoreduction.

For these later stages in evolution, we have good reason to expect that the details can be understood with reference to evolutionary processes currently in action. Jacques Oberto, Eugene Koonin and Ryan Catchpole all presented results that bring us closer to understand the interplay between cellular interactions, mobile elements and gene transfer. Ryan Catchpole’s microscopy work indicated that the outer envelope of the bacterium Thermotoga and the nanopod protrusions of the archaeon Thermococcus likely mediate the interactions that drive gene transfer, and Jacques Oberto’s analysis of Thermococcus genomes illustrates how transfer events may drive genome rearrangement through mobile element acquisition. More generally, both Eugene Koonin and Carlos Mariscal considered the implications of expanding our focus from LUCA as a single cell to the wider context in which LUCA existed, presumably as a population within a community. This discussion, together with consideration of the renewed interest in Carl Woese and George Fox’s progenote model, provided a helpful platform for engagement with the viral research presented, which, by definition, is predicated on host-viral interactions, gene transfer and the process of coevolution.

Indeed, the possibility of understanding early evolution in terms of processes rather than historical reconstruction was a key thrust of Eugene Koonin’s thinking, and was echoed by the move towards uniting the tools of synthetic biology and experimental evolution, which featured in Ryan Catchpole’s and Anthony Poole’s work on assessing whether DNA could have evolved through an alternative route, favoured by chemists. This opens up the field to more exploratory avenues where multiple possible paths to modern life can be studied, rather than focusing exclusively on those for which there may be a faint historical trace. In the spirit of a changing modus operandi, this is an interesting development, as it takes focus away from LUCA as a ‘parts list’, and broadens the subject to one where the goal is to understand the possible paths to complex cellular life.

In contrast to previous LUCA meetings held in 1996 and 2006, the 2016 meeting not only considers LUCA and its contemporaries, but also viruses infecting them, a testimony of a growing interest for virus origin and evolution in the community of evolutionists. Comparative analysis of capsid proteins and packaging ATPases have indeed clearly revealed that Viruses were already around at the time of LUCA. Patrick Forterre introduced the concept of virocell to remind us that viruses can be cradles of new genes during their intracellular stage of reproduction, explaining why a huge part of the genetic information in the biosphere has a viral origin. He suggested that proteins that first originated in the virosphere and later on transferred to cells had a major impact at different critical stages of life evolution, for instance in the transition from RNA to DNA.

Eugene Koonin presented the virus world as an evolutionary network of viruses and capsidless selfish elements – he developed the concept of a greater virus world which forms an evolutionary network that is held together by shared conserved genes and includes both bona fide capsid-encoding viruses and different classes of capsidless replicons. According to him, viruses have evolved from capsidless selfish elements, and vice versa, on multiple occasions during evolution. At the earliest stage of life’s evolution, capsidless genetic parasites most likely emerged first and subsequently gave rise to different classes of viruses.

Mart Krupovic has explored the possible origins of the viral capsid proteins, which would all suggest the transformation of capsidless selfish elements into bona fide viruses (ne manque-t-il pas un verbe ?). He provided a global overview of the structural diversity of viral capsid proteins and their possible origin from different cellular proteins. David Prangishvili summarized the present state of the research on viruses of hyperthermophilic archaea and put forward the hypothesis suggesting that these viruses represent living fossils of the virosphere contemporary of the LUCA.

Matti Jalasvuori posed the question whether the origin of the capsid coincide with the origin of viruses, or is it possible that capsid-like functionalities emerged before the appearance of true viral entities. Based on the results of the computational simulation he provided a possible scenario for explaining the origin of viral capsids before the emergence of genuine viruses: in the absence of other means of horizontal gene transfer between compartments, evolution of capsid-like functionalities may have been necessary for early life to prevail.

Matthias Fischer provided an overview of giant eukaryotic viruses, which are considered by some scientists to represent descendants of ancient cellular organisms. However, Dr. Fischer refuted this possibility based on available comparative genomics analyses. He also presented a unique tripartite virus-host system consisting of a protist cell, a giant virus infecting it and a satellite virus, the virophage, parasitizing the giant virus. Morgan Gaia explored the evolutionary relationships among big and giant dsDNA viruses and presented the results of phylogenetic analysis based on the RNA polymerase encoded by the majority of these viruses. His results show a complex evolutionary history of this large group of viruses that predated the origin of modern eukaryotes.

In conclusion, participants were so excited by this unique meeting that several of them suggest to organise the next one to celebrate LUCA 25th birthday, instead of waiting 10 years more.