[Show abstract][Hide abstract] ABSTRACT: In a recent article, Nelson-Sathi et al. [NS] report that the origins of Major Archaeal Lineages [MAL] correspond to massive group-specific gene acquisitions via horizontal gene transfer (HGT) from bacteria (Nelson-Sathi et al., 2015, Nature 517(7532):77-80). If correct, this would have fundamental implications for the process of diversification in microbes. However, a re-examination of these data and results shows that the methodology used by NS systematically inflates the number of genes acquired at the root of each MAL, and incorrectly assumes bacterial origins for these genes. A re-analysis of their data with appropriate phylogenetic models accounting for the dynamics of gene gain and loss between lineages supports the continuous acquisition of genes over long periods in the evolution of Archaea.
Molecular Biology and Evolution 11/2015; DOI:10.1093/molbev/msv249 · 9.11 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Acid mine drainage (AMD) is a highly toxic environment for most living organisms due to the
presence of many lethal elements including arsenic (As). Thiomonas (Tm.) bacteria are found
ubiquitously in AMD and can withstand these extreme conditions, in part because they are
able to oxidize arsenite. In order to further improve our knowledge concerning the adaptive
capacities of these bacteria, we sequenced and assembled the genome of six isolates
derived fromthe Carnoulès AMD, and compared them to the genomes of Tm. arsenitoxydans
3As (isolated from the same site) and Tm. intermedia K12 (isolated from a sewage pipe). A
detailed analysis of the Tm. sp. CB2 genome revealed various rearrangements had occurred
in comparison to what was observed in 3As and K12 and over 20 genomic islands (GEIs)
were found in each of these three genomes.We performed a detailed comparison of the two
arsenic-related islands found in CB2, carrying the genes required for arsenite oxidation and
As resistance, with those found in K12, 3As, and five other Thiomonas strains also isolated
from Carnoulès (CB1, CB3, CB6, ACO3 and ACO7). Our results suggest that these arsenicrelated
islands have evolved differentially in these closely related Thiomonas strains, leading
to divergent capacities to survive in As rich environments.
PLoS ONE 09/2015; 10:e0139011. DOI:10.1371/journal.pone.0139011 · 3.23 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Understanding the principles underlying the plasticity of signal transduction networks is fundamental to decipher the functioning of living cells. In Myxococcus xanthus, a particular chemosensory system (Frz) coordinates the activity of two separate motility systems (the A- and S-motility systems), promoting multicellular development. This unusual structure asks how signal is transduced in a branched signal transduction pathway. Using combined evolution-guided and single cell approaches, we successfully uncoupled the regulations and showed that the A-motility regulation system branched-off an existing signaling system that initially only controlled S-motility. Pathway branching emerged in part following a gene duplication event and changes in the circuit structure increasing the signaling efficiency. In the evolved pathway, the Frz histidine kinase generates a steep biphasic response to increasing external stimulations, which is essential for signal partitioning to the motility systems. We further show that this behavior results from the action of two accessory response regulator proteins that act independently to filter and amplify signals from the upstream kinase. Thus, signal amplification loops may underlie the emergence of new connectivity in signal transduction pathways.
[Show abstract][Hide abstract] ABSTRACT: One of the most fundamental questions in evolutionary biology is the origin of the lineage leading to eukaryotes. Recent phylogenomic analyses have indicated an emergence of eukaryotes from within the radiation of modern Archaea and specifically from a group comprising Thaumarchaeota/"Aigarchaeota" (candidate phylum)/Crenarchaeota/Korarchaeota (TACK). Despite their major implications, these studies were all based on the reconstruction of universal trees and left the exact placement of eukaryotes with respect to the TACK lineage unclear. Here we have applied an original two-step approach that involves the separate analysis of markers shared between Archaea and eukaryotes and between Archaea and Bacteria. This strategy allowed us to use a larger number of markers and greater taxonomic coverage, obtain high-quality alignments, and alleviate tree reconstruction artifacts potentially introduced when analyzing the three domains simultaneously. Our results robustly indicate a sister relationship of eukaryotes with the TACK superphylum that is strongly associated with a distinct root of the Archaea that lies within the Euryarchaeota, challenging the traditional topology of the archaeal tree. Therefore, if we are to embrace an archaeal origin for eukaryotes, our view of the evolution of the third domain of life will have to be profoundly reconsidered, as will many areas of investigation aimed at inferring ancestral characteristics of early life and Earth.
Proceedings of the National Academy of Sciences 05/2015; 112(21). DOI:10.1073/pnas.1420858112 · 9.67 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Mesotoga strain PhosAc3 was the first mesophilic cultivated member of the order Thermotogales. This genus currently contain two described species, M. prima and M. infera. Strain PhosAc3, isolated from a Tunisian digestor treating phosphogypsum, is phylogenetically closely related to M. prima strain MesG1.Ag.4.2 T. Strain PhosAc3 has a genome of 3.1 Mb with a G + C content of 45.2%. It contains 3,051 protein-coding genes of which 74.6% have their best reciprocal BLAST hit in the genome of the type species, strain MesG1.Ag.4.2 T. For this reason we propose to assign strain PhosAc3 as a novel ecotype of the Mesotoga prima species. However, in contrast with the M. prima type strain, (i) it does not ferment sugars but uses them only in the presence of elemental sulfur as terminal electron acceptor, (ii) it produces only acetate and CO 2 from sugars, whereas strain MesG1.Ag.4.2 T produces acetate, butyrate, isobutyrate, isovalerate, 2-methyl-butyrate and (iii) sulfides are also end products of the elemental sulfur reduction in theses growth conditions.
[Show abstract][Hide abstract] ABSTRACT: Studying the evolution of macromolecular assemblies is important to improve our understanding of how complex cellular structures evolved, and to identify the functional building blocks that are involved. Recent studies suggest that the macromolecular complexes that are involved in two distinct processes in Myxococcus xanthus - surface motility and sporulation - are derived from an ancestral polysaccharide capsule assembly system. In this Opinion article, we argue that the available data suggest that the motility machinery evolved from this capsule assembly system following a gene duplication event, a change in carbohydrate polymer specificity and the acquisition of additional proteins by the motility complex, all of which are key features that distinguish the motility and sporulation systems. Furthermore, the presence of intermediates of these systems in bacterial genomes suggests a testable evolutionary model for their emergence and spread.
[Show abstract][Hide abstract] ABSTRACT: In human pathogenic bacteria, nickel is required for the activation of two enzymes, urease and [NiFe]-hydrogenase, necessary for host infection. Acquisition of Ni(II) is mediated by either permeases or ABC-importers, the latter including a subclass that involves an extracytoplasmic nickel-binding protein, Ni-BP. This study reports on the structure of three Ni-BPs from a diversity of human pathogens and on the existence of three new nickel-binding motifs. These are different from that previously described for Escherichia coli Ni-BP NikA, known to bind nickel via a nickelophore, and indicate a variegated ligand selectivity for Ni-BPs. The structures are consistent with ligand affinities measured in solution by calorimetry and challenge the hypothesis of a general requirement of nickelophores for nickel uptake by canonical ABC importers. Phylogenetic analyses showed that Ni-BPs have different evolutionary origins and emerged independently from peptide-binding proteins, possibly explaining the promiscuous behavior of this class of Ni(II) carriers.
[Show abstract][Hide abstract] ABSTRACT: The seminal work of Carl Woese and co-workers has contributed to promote the RNA component of the small subunit of the ribosome (SSU rRNA) as a "gold standard" of modern prokaryotic taxonomy and systematics, and an essential tool to explore microbial diversity. Yet, this marker has a limited resolving power, especially at deep phylogenetic depth and can lead to strongly biased trees. The ever-larger number of available complete genomes now calls for a novel standard dataset of robust protein markers that may complement SSU rRNA. In this respect, concatenation of ribosomal proteins (r-proteins) is being growingly used to reconstruct large-scale prokaryotic phylogenies, but their suitability for systematic and/or taxonomic purposes has not been specifically addressed. Using Proteobacteria as a case study, we show that amino acid and nucleic acid r-protein sequences contain a reliable phylogenetic signal at a wide range of taxonomic depths, which has not been totally blurred by mutational saturation or horizontal gene transfer. The use of accurate evolutionary models and reconstruction methods allows overcoming most tree reconstruction artefacts resulting from compositional biases and/or fast evolutionary rates. The inferred phylogenies allow clarifying the relationships among most proteobacterial orders and families, along with the position of several unclassified lineages, suggesting some possible revisions of the current classification. In addition, we investigate the root of the Proteobacteria by considering the time-variation of nucleic acid composition of r-protein sequences and the information carried by horizontal gene transfers, two approaches that do not require the use of an outgroup and limit tree reconstruction artefacts. Altogether, our analyses indicate that r-proteins may represent a promising standard for prokaryotic taxonomy and systematics.
[Show abstract][Hide abstract] ABSTRACT: The thermophilic sulfate-reducing archaeon Archaeoglobus fulgidus strain VC-16 (DSM 4304), which is known to oxidize fatty acids and n-alkenes, was shown to oxidize saturated hydrocarbons (n-alkanes in the range C10-C21) with thiosulfate or sulfate as a terminal electron acceptor. The amount of n-hexadecane degradation observed was in stoichiometric agreement with the theoretically expected amount of thiosulfate reduction. One of the pathways used by anaerobic microorganisms to activate alkanes is addition to fumarate that involves alkylsuccinate synthase as a key enzyme. A search for genes encoding homologous enzymes in A. fulgidus identified the pflD gene (locus-tag AF1449) that was previously annotated as a pyruvate formate lyase. A phylogenetic analysis revealed that this gene is of bacterial origin and was likely acquired by A. fulgidus from a bacterial donor through a horizontal gene transfer. Based on three-dimensional modeling of the corresponding protein and molecular dynamic simulations, we hypothesize an alkylsuccinate synthase activity for this gene product. The pflD gene expression was upregulated during the growth of A. fulgidus on an n-alkane (C16) compared with growth on a fatty acid. Our results suggest that anaerobic alkane degradation in A. fulgidus may involve the gene pflD in alkane activation through addition to fumarate. These findings highlight the possible importance of hydrocarbon oxidation at high temperatures by A. fulgidus in hydrothermal vents and the deep biosphere.The ISME Journal advance online publication, 24 April 2014; doi:10.1038/ismej.2014.58.
The ISME Journal 04/2014; 8(11). DOI:10.1038/ismej.2014.58 · 9.30 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: The evolutionary origin of eukaryotes is a question of great interest for which many different hypotheses have been proposed. These hypotheses predict distinct patterns of evolutionary relationships for individual genes of the ancestral eukaryotic genome. The availability of numerous completely sequenced genomes covering the three domains of life makes it possible to contrast these predictions with empirical data. We performed a systematic analysis of the phylogenetic relationships of ancestral eukaryotic genes with archaeal and bacterial genes. In contrast with previous studies, we emphasize the critical importance of methods accounting for statistical support, horizontal gene transfer and gene loss, and we disentangle the processes underlying the phylogenomic pattern we observe. We first recover a clear signal indicating that a fraction of the bacteria-like eukaryotic genes are of alphaproteobacterial origin. Then, we show that the majority of bacteria-related eukaryotic genes actually do not point to a relationship with a specific bacterial taxonomic group. We also provide evidence that eukaryotes branch close to the last archaeal common ancestor. Our results demonstrate that there is no phylogenetic support for hypotheses involving a fusion with a bacterium other than the ancestor of mitochondria. Overall, they leave only two possible interpretations, based respectively on the early-mitochondria hypotheses, which suppose an early endosymbiosis of an alphaproteobacterium in an archaeal host, and on the slow-drip autogenous hypothesis, in which early eukaryotic ancestors were particularly prone to horizontal gene transfers.
[Show abstract][Hide abstract] ABSTRACT: The archaeal machinery responsible for DNA replication is largely homologous to that of eukaryotes and is clearly distinct from its bacterial counterpart. Moreover, it shows high diversity in the various archaeal lineages, including different sets of components, heterogeneous taxonomic distribution, and a large number of additional copies that are sometimes highly divergent. This has made the evolutionary history of this cellular system particularly challenging to dissect. Here, we have carried out an exhaustive identification of homologs of all major replication components in over 140 complete archaeal genomes. Phylogenomic analysis allowed assigning them to either a conserved and probably essential 'core' of replication components that were mainly vertically inherited, or to a variable and highly divergent 'shell' of extra copies that have likely arisen from integrative elements. This suggests that replication proteins are frequently exchanged between extra-chromosomal elements and cellular genomes. Our study allowed clarifying the history that shaped this key cellular process (ancestral components, horizontal gene transfers, gene losses), providing important evolutionary and functional information. Finally, our precise identification of core components permitted to show that the phylogenetic signal carried by DNA replication is highly consistent with that harbored by two other key informational machineries (translation and transcription), strengthening the existence of a robust organismal tree for the Archaea.
[Show abstract][Hide abstract] ABSTRACT: A moderately halophilic, Gram negative, non-sporulating bacterium designed as strain TYRC17T was isolated from olive-processing effluents. The organism is a straight rod, motile by peritrichous flagella, able to respire both oxygen and nitrate. Growth occurred with 0-25 % (w/v) NaCl (optimum, 7 %), at pH 5-11 (optimum, pH 7.0) and at 4-50 °C (optimally at 35 °C). It accumulates poly-β-hydroxyalkanoate granules and produces exopolysaccharides. The predominant fatty acids are C18:1w7c (42.2 %), C16:1w7c (15.6 %), C16:0 (14.2 %). Ubiquinone 9 (Q-9) is the only respiratory quinone. The DNA G+C content of TYRC17T is 53.9 mol%. Phylogenetic analyses of 16S rRNA gene sequences revealed that the strain falls within the genus Halomonas, and more precisely within the subgroup containing Halomonas sulfidaeris, H. titanicae, H. variabilis, H. zhanjiangensis, H. alkaliantarctica, H. boliviensis and H. neptunia. TYRC17T showed high 16S-rRNA sequence identities in particular with the three last species (99.4-99.5 %). However, a Multilocus Sequence Analysis (MLSA) using the 23S rRNA, gyrB, rpoD and secA genes allowed clarifying the phylogenetic position of TYRC17T. This, combined to the level of DNA-DNA hybridization between TYRC17T and its closest relatives ranging only from 21.6 % to 48.4 %, indicated that TYRC17T does not belong to any of these species. On the basis of phenotypic and genotypic characteristics, and also genomic and phylogenetic evidences, strain TYRC17T represents a novel species of the genus Halomonas. The name Halomonas olivaria sp. nov. is proposed with TYRC17T (= DSM 19074T = CCUG 53850BT) as the type strain.
International Journal of Systematic and Evolutionary Microbiology 09/2013; 64(Pt 1). DOI:10.1099/ijs.0.049007-0 · 2.51 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: During meiosis, the stable pairing of the homologous chromosomes is mediated by the assembly of the synaptonemal complex (SC). Its tripartite structure is well conserved in Metazoa and consists of two lateral elements (LEs) and a central region (CR) that in turn is formed by several transverse filaments (TFs) and a central element (CE). In a previous paper we have shown that not only the structure, but also the major structural proteins SYCP1 (TFs) and SYCP3 (LEs) of the mammalian SC are conserved in metazoan evolution. In continuation of this work, we now investigated the evolution of the mammalian CE-specific proteins using phylogenetic and biochemical/cytological approaches. In analogy to the observations made for SYCP1 and SYCP3, we did not detect homologues of the mammalian CE proteins in insects or nematodes, but in several other metazoan clades. We were able to identify homologues of three mammalian CE proteins in several vertebrate and invertebrate species, for two of these proteins down to the basal-branching phylum of Cnidaria. Our approaches indicate that the SC arose only once, but evolved dynamically during diversification of Metazoa. Certain proteins appear to be ancient in animals, but successive addition of further components as well as protein loss and/or replacements have also taken place in some lineages.
[Show abstract][Hide abstract] ABSTRACT: Arsenic is widespread in the environment and its presence is a result of natural or anthropogenic activities. Microbes have developed different mechanisms to deal with toxic compounds such as arsenic and this is to resist or metabolise the compound. Here we present the first reference set of genomic, transcriptomic and proteomic data of an Alphaproteobacterium isolated from an arsenic-containing goldmine: Rhizobium sp. NT-26. Although phylogenetically related to the plant-associated bacteria, this organism has lost the major colonising capabilities needed for symbiosis with legumes. In contrast, the genome of Rhizobium sp. NT-26 comprises a megaplasmid containing the various genes which enable it to metabolise arsenite. Remarkably, although the genes required for arsenite oxidation and flagellar motility/biofilm formation are carried by the megaplasmid and the chromosome, respectively, a coordinate regulation of these two mechanisms was observed. Taken together, these processes illustrate the impact environmental pressure can have on the evolution of bacterial genomes, improving the fitness of bacterial strains by the acquisition of novel functions.