Patrick Forterre

Pasteur Network · Department of Microbiology of Paris

The existence of LUCA in the distant past is the logical consequence of the binary mechanism of cell division. The biosphere in which LUCA and contemporaries were living was the product of a long cellular evolution from the origin of life to the second age of the RNA world. A parsimonious scenario suggests that the molecular fabric of LUCA was much...

Our perception of viruses has been drastically evolving since the inception of the field of virology over a century ago. In particular, the discovery of giant viruses from the Nucleocytoviricota phylum marked a pivotal moment. Their previously concealed diversity and abundance unearthed an unprecedented complexity in the virus world, a complexity t...

Quantitative phase microscopy (QPM) represents a non-invasive alternative to fluorescence microscopy for cell observation with high contrast and for the quantitative measurement of dry mass (DM) and growth rate at the single cell level. While DM measurements using QPM have been widely conducted on mammalian cells, bacteria have been less investigat...

Conjugative plasmids are self-transmissible mobile genetic elements that transfer DNA between host cells via type IV secretion systems (T4SS). While T4SS-mediated conjugation has been well-studied in bacteria, information is sparse in Archaea and known representatives exist only in the Sulfolobales order of Crenarchaeota. Here we present the first...

DNA viruses have a major influence on the ecology and evolution of cellular organisms, but their overall diversity and evolutionary trajectories remain elusive. Here we carried out a phylogeny-guided genome-resolved metagenomic survey of the sunlit oceans and discovered plankton-infecting relatives of herpesviruses that form a putative new phylum d...

Il est maintenant bien établi que les virus ont joué un rôle important dans l’évolution des eucaryotes modernes. Dans cette revue, nous commentons le rôle qu’ils ont pu jouer dans l’eucaryogenèse. Nous discutons les analyses phylogénétiques qui mettent en évidence l’origine virale de plusieurs protéines clés de la biologie moléculaire des eucaryote...

Type II DNA topoisomerases of the family A (Topo IIAs) are present in all Bacteria (DNA gyrase) and eukaryotes. In eukaryotes, they play a major role in transcription, DNA replication, chromosome segregation, and modulation of chromosome architecture. The origin of eukaryotic Topo IIA remains mysterious since they are very divergent from their bact...

The rebuttal of the prokaryote–eukaryote dichotomy and the elaboration of the three domains concept by Carl Woese and colleagues has been a breakthrough in biology. With the methodologies available at this time, they have shown that a single molecule, the 16S ribosomal RNA, could reveal the global organization of the living world. Later on, mining...

Thermophiles are microorganisms that thrive at high temperature. Studying them can provide valuable information on how life has adapted to extreme conditions. However, high temperature conditions are difficult to achieve on conventional optical microscopes. Some home-made solutions have been proposed, all based on local resistive electric heating,...

DNA gyrase is a type II topoisomerase with the unique capacity to introduce negative supercoiling in DNA. In bacteria, DNA gyrase has an essential role in the homeostatic regulation of supercoiling. While ubiquitous in Bacteria, DNA gyrase was previously reported to have a patchy distribution in Archaea but its emergent function and evolutionary hi...

Type II DNA topoisomerases of the family A (Topo IIA) are present in all bacteria (DNA gyrase) and eukaryotes. In eukaryotes, they play a major role in transcription, DNA replication, chromosome segregation and modulation of chromosome architecture. The origin of eukaryotic Topo IIA remains mysterious since they are very divergent from their bacter...

The discovery of Asgard archaea and the exploration of their diversity over the last 6 years have deeply impacted the scientific community working on eukaryogenesis, rejuvenating an intense debate on the topology of the universal tree of life (uTol). Here, we discuss how this debate is impacted by two recent publications that expand the number of A...

The emergence of the eukaryotic cytoskeleton is a critical yet puzzling step of eukaryogenesis. Actin and actin-related proteins (ARPs) are ubiquitous components of this cytoskeleton. The gene repertoire of the Last Eukaryotic Common Ancestor (LECA) would have therefore harbored both actin and various ARPs. Here, we report the presence and expressi...

Thermococcales, a major order of archaea inhabiting the iron‐ and sulfur‐rich anaerobic parts of hydrothermal deep‐sea vents, have been shown to rapidly produce abundant quantities of pyrite FeS2 in iron–sulfur‐rich fluids at 85°C, suggesting that they may contribute to the formation of ‘low temperature’ FeS2 in their ecosystem. We show that this p...

Oligopeptide permease A (OppA) plays important roles in the nutrition of cells and various signaling processes. In archaea, OppA is a major protein present in membrane vesicles of Thermococcales. Due to there being no crystal structures of archaeal OppAs determined to date, we report the crystal structure of archaeal OppA from Thermococcus kodakara...

Eukaryotic topoisomerases I (TOP1) are ubiquitous enzymes removing DNA torsional stress. However, there is little data concerning the three-dimensional structure of TOP1 in the absence of DNA, nor how the DNA molecule can enter/exit its closed conformation. Here, we solved the structure of thermostable archaeal Caldiarchaeum subterraneum CsTOP1 in...

In all cells, DNA topoisomerases dynamically regulate DNA supercoiling allowing essential DNA processes such as transcription and replication to occur. How this complex system emerged in the course of evolution is poorly understood. Intriguingly, a single horizontal gene transfer event led to the successful establishment of bacterial gyrase in Arch...

Double-stranded DNA viruses of the realm Varidnaviria (formerly PRD1-adenovirus lineage) are characterized by homologous major capsid proteins (MCPs) containing one (kingdom: Helvetiavirae) or two β-barrel domains (kingdom: Bamfordvirae) known as the jelly roll folds. Most of them also share homologous packaging ATPases (pATPases). Remarkably, Vari...

Membrane-bound extracellular vesicles (EVs) are secreted by cells from all three domains of life and their implication in various biological processes is increasingly recognized. In this review, we summarize the current knowledge on archaeal EVs and nanotubes, and emphasize their biological significance. In archaea, the EVs and nanopods have been l...

Membrane-bound extracellular vesicles (EVs), secreted by cells from all three domains of life, transport various molecules and act as agents of intercellular communication in diverse environments. Here we demonstrate that EVs produced by a hyperthermophilic and acidophilic archaeon Sulfolobus islandicus carry not only a diverse proteome, enriched i...

Culturing cells confined in microscale geometries has been reported in many studies this last decade, in particular following the development of microfluidic-based applications and lab-on-a-chip devices. Such studies usually examine growth of Escherichia coli. In this article, we show that E. coli may be a poor model and that spatial confinement ca...

Background K-mer-based methods have greatly advanced in recent years, largely driven by the realization of their biological significance and by the advent of next-generation sequencing. Their speed and their independence from the annotation process are major advantages. Their utility in the study of the mobilome has recently emerged and they seem a...

Membrane-bound extracellular vesicles (EVs), secreted by cells from all three domains of life, transport various molecules and act as agents of intercellular communication in diverse environments. Here we demonstrate that EVs produced by a hyperthermophilic and acidophilic archaeon Sulfolobus islandicus carry not only diverse proteins but also chro...

Culturing cells confined in microscale geometries has been reported in many studies this last decade, in particular following the development of microfluidic-based applications and lab-on-a-chip devices. Such studies usually examine growth of Escherichia coli. In this article, we show that E. coli may be a poor model and that spatial confinement ca...

The biological carbon pump, in which carbon fixed by photosynthesis is exported to the deep ocean through sinking, is a major process in Earth’s carbon cycle. The proportion of primary production that is exported is termed the carbon export efficiency (CEE). Based on in-lab or regional scale observations, viruses were previously suggested to affect...

Deep-sea hydrothermal vents are inhabited by complex communities of microbes and their viruses. Despite the importance of viruses in controlling the diversity, adaptation and evolution of their microbial hosts, to date, only eight bacterial and two archaeal viruses isolated from abyssal ecosystems have been described. Thus, our efforts focused on g...

B-family DNA polymerases (PolBs) represent the most common replicases. PolB enzymes that require RNA (or DNA) primed templates for DNA synthesis are found in all domains of life and many DNA viruses. Despite extensive research on PolBs, their origins and evolution remain enigmatic. Massive accumulation of new genomic and metagenomic data from diver...

The importance of unusual DNA structures in the regulation of basic cellular processes is an emerging field of research. Amongst local non-B DNA structures, G-quadruplexes (G4s) have gained in popularity during the last decade, and their presence and functional relevance at the DNA and RNA level has been demonstrated in a number of viral, bacterial...

Actin is a major component of the eukaryotic cytoskeleton. Many related actin homologues can be found in eukaryotes1, some of them being present in most or all eukaryotic lineages. The gene repertoire of the Last Eukaryotic Common Ancestor (LECA) therefore would have harbored both actin and various actin-related proteins (ARPs). A current hypothesi...

The control of DNA topology by DNA topoisomerases is essential for virtually all DNA transactions in the cell. These enzymes, present in every organism, exist as several non-homologous families. We previously identified a small group of atypical type IIB topoisomerases, called Topo VIII, mainly encoded by plasmids. Here, taking advantage of the rap...

Mobile genetic elements often encode integrases which catalyze the site-specific insertion of their genetic information into the host genome and the reverse reaction of excision. Hyperthermophilic archaea harbor integrases belonging to the SSV-family which carry the MGE recombination site within their open reading frame. Upon integration into the h...

If viruses are defined by their specific mode of reproduction, i.e., the production of virions, they should have originated after the emergence of the ribosome, since the simplest virion contains at least one protein. Viruses most likely evolved from RNA replicons that recruited genes encoding RNA-binding proteins suitable for capsid or nucleocapsi...

Maintaining an appropriate DNA topology with DNA‐based processes (DNA replication, transcription and recombination) is crucial for all three domains of life. In bacteria, the homeostatic regulation for controlling DNA supercoiling relies on antagonistic activities of two DNA topoisomerases, TopoI and gyrase. In hyperthermophilic crenarchaea, the pr...

Motivation: Comparative plasmid genome analyses require complex tools, the manipulation of large numbers of sequences and constitute a daunting task for the wet bench experimentalist. Dedicated plasmid databases are sparse, only comprise bacterial plasmids and provide exclusively access to sequence similarity searches. Results: We have developed...

Giant and large eukaryotic double-stranded DNA viruses from the Nucleo-Cytoplasmic Large DNA Virus (NCLDV) assemblage represent a remarkably diverse and potentially ancient component of the eukaryotic virome. However, their origin(s), evolution, and potential roles in the emergence of modern eukaryotes remain subjects of intense debate. Here we pre...

Reverse gyrase (RG) is the only protein found ubiquitously in hyperthermophilic organisms, but absent from mesophiles. As such, its simple presence or absence allows us to deduce information about the optimal growth temperature of long-extinct organisms, even as far as the last universal common ancestor of extant life (LUCA). The growth environment...

Double-stranded DNA viruses of the PRD1-adenovirus lineage are characterized by homologous major capsid proteins containing one or two β-barrel domains known as the jelly roll folds. Most of them also share homologous packaging ATPases of the FtsK/HerA superfamily P-loop ATPases. Remarkably, members of this lineage infect hosts from the three domai...

Casposons are a group of bacterial and archaeal DNA transposons encoding a specific integrase, termed casposase, which is homologous to the Cas1 enzyme responsible for the integration of new spacers into CRISPR loci. Here, we characterized the sequence motifs recognized by the casposase from a thermophilic archaeon Aciduliprofundum boonei. We ident...

The diversity of archaeal viruses is severely undersampled compared to that of viruses infecting bacteria and eukaryotes, limiting our understanding on their evolution and environmental impacts. Here we describe the isolation and characterization of four new viruses infecting halophilic archaea from the saline Lake Retba, located close to Dakar on...

To explore the diversity of mobile genetic elements (MGE) associated with archaea of the phylum Thaumarchaeota, we exploited the property of most MGE to integrate into the genomes of their hosts. Integrated MGE (iMGE) were identified in 20 thaumarchaeal genomes amounting to 2 Mbp of mobile thaumarchaeal DNA. These iMGE group into five major classes...

Viruses modulate ecosystems by directly altering host metabolisms through auxiliary metabolic genes. However, viral genomes are not known to encode the core components of translation machinery, such as ribosomal proteins (RPs). Here, using reference genomes and global-scale viral metagenomic datasets, we identify 14 different RPs across viral genom...

Reverse gyrase (RG) is the only protein found ubiquitously in hyperthermophilic organisms, but absent from mesophiles. As such, its simple presence or absence allows us to deduce information about the optimal growth temperature of long-extinct organisms, even as far as the last universal common ancestor of extant life (LUCA). The growth environment...

Diverse DNA repair mechanisms are essential to all living organisms. Some of the most widespread repair systems allow recovery of genome integrity in the face of UV radiation. Here, we show that the hyperthermophilic archaeon Thermococcus nautili possesses a remarkable ability to recovery from extreme chromosomal damage. Immediately following UV ir...

Cells from all three domains of life, Archaea, Bacteria and Eukarya, produce extracellular vesicles (EVs) which are sometimes associated to filamentous structures known as nanopods or nanotubes. The mechanisms of EV biogenesis in the three domains remain poorly understood, although studies in Bacteria and Eukarya indicate that the regulation of lip...

Giant and large eukaryotic double-stranded DNA viruses from the Nucleo-Cytoplasmic Large DNA Virus (NCLDV) assemblage represent a remarkably diverse and potentially ancient component of the eukaryotic virome. However, their origin(s), evolution and potential roles in the emergence of modern eukaryotes remain a subject of intense debate. Since the c...

Archaeal RNA:pseudouridine-synthase (PUS) Cbf5 in complex with proteins L7Ae, Nop10 and Gar1, and guide box H/ACA sRNAs forms ribonucleoprotein (RNP) catalysts that insure the conversion of uridines into pseudouridines (Ψs) in ribosomal RNAs (rRNAs). Nonetheless, in the absence of guide RNA, Cbf5 catalyzes the in vitro formation of Ψ2603 in Pyro...

Interactions between hyperthermophilic archaea and minerals occur in hydrothermal deep-sea vents, one of the most extreme environments for life on Earth. These interactions occur in the internal pores and at surfaces of active hydrothermal chimneys. In this study, we show that, at 85°C, Thermococcales, the predominant hyperthermophilic microorganis...

Calculated mineralization of pyrite using our mineralization conditions (Neutral pH, Temperature of 85°C, excess of sulfur). Results of modeling by using Chess software (version: 3.9.6). (DOCX)

Calculated mineralization of greigite in the same previous mineralization conditions with restriction to precipitate pyrite. Results of modeling by using Chess software (version: 3.9.6). (DOCX)

Hyperthermophilic microorganisms are an important asset in the toolkits of biotechnologists, biochemists and evolutionary biologists. The anaerobic archaeon, Thermococcus kodakarensis, has become one of the most useful hyperthermophilic model species, not least due to its natural competence and genetic tractability. Despite this, the range of genet...

The first tree of life based on the comparison of ribosomal RNA (ribonucleic acid) allowed classifying all ribosome‐encoding organisms into three domains: Archaea, Bacteria and Eukarya. Phylogenomics analyses later on show that these domains probably emerged from a last universal common ancestor (LUCA) simpler than modern organisms. Different resul...

N6-threonyl-carbamoyl adenosine (t6A) is a universal tRNA modification found at position 37, next to the anticodon, in almost all tRNAs decoding ANN codons (where N = A, U, G or C). t6A stabilizes the codon-anticodon interaction and hence promotes translation fidelity. The first step of the biosynthesis of t6A, the production of threonyl-carbamoyl...