Did an ancient chlamydial endosymbiosis facilitate the establishment of primary plastids?

© 2007 Huang and Gogarten. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. The definitive version was published in Genome Biology 8 (2007): R99, doi:10.1186/gb-2007-8-6-r99.Ancient endosymbioses are responsible for the origins of mitochondria and plastids, and they contribute to the divergence of several major eukaryotic groups. Although chlamydiae, a group of obligate intracellular bacteria, are not found in plants, an unexpected number of chlamydial genes are most similar to plant homologs, which, interestingly, often contain a plastid-targeting signal. This observation has prompted several hypotheses, including gene transfer between chlamydiae and plant-related groups and an ancestral relationship between chlamydiae and cyanobacteria. We conducted phylogenomic analyses of the red alga Cyanidioschyzon merolae to identify genes specifically related to chlamydial homologs. We show that at least 21 genes were transferred between chlamydiae and primary photosynthetic eukaryotes, with the donor most similar to the environmental Protochlamydia. Such an unusually high number of transferred genes suggests an ancient chlamydial endosymbiosis with the ancestral primary photosynthetic eukaryote. We hypothesize that three organisms were involved in establishing the primary photosynthetic lineage: the eukaryotic host cell, the cyanobacterial endosymbiont that provided photosynthetic capability, and a chlamydial endosymbiont or parasite that facilitated the establishment of the cyanobacterial endosymbiont. Our findings provide a glimpse into the complex interactions that were necessary to establish the primary endosymbiotic relationship between plastid and host cytoplasms, and thereby explain the rarity with which long-term successful endosymbiotic relationships between heterotrophs and photoautotrophs were established. Our data also provide strong and independent support for a common origin of all primary photosynthetic eukaryotes and of the plastids they harbor.This work was performed while JH held a National Research Council Associateship Award at the NASA Astrobiology Institute at the Marine Biological Laboratory in Woods Hole, Massachusetts (NCC2-1054). Additional support was provided through NSF (MCB-0237197) and NASA AISR (NNG04GP90G) grants to JPG

Multi site polyadenylation and transcriptional response to stress of a vacuolar type H(+)-ATPase subunit A gene in Arabidopsis thaliana

BACKGROUND: Vacuolar type H(+)-ATPases play a critical role in the maintenance of vacuolar homeostasis in plant cells. V-ATPases are also involved in plants' defense against environmental stress. This research examined the expression and regulation of the catalytic subunit of the vacuolar type H(+)-ATPase in Arabidopsis thaliana and the effect of environmental stress on multiple transcripts generated by this gene. RESULTS: Evidence suggests that subunit A of the vacuolar type H(+)-ATPase is encoded by a single gene in Arabidopsis thaliana. Genome blot analysis showed no indication of a second subunit A gene being present. The single gene identified was shown by whole RNA blot analysis to be transcribed in all organs of the plant. Subunit A was shown by sequencing the 3' end of multiple cDNA clones to exhibit multi site polyadenylation. Four different poly (A) tail attachment sites were revealed. Experiments were performed to determine the response of transcript levels for subunit A to environmental stress. A PCR based strategy was devised to amplify the four different transcripts from the subunit A gene. CONCLUSIONS: Amplification of cDNA generated from seedlings exposed to cold, salt stress, and etiolation showed that transcript levels for subunit A of the vacuolar type H(+)-ATPase in Arabidopsis were responsive to stress conditions. Cold and salt stress resulted in a 2–4 fold increase in all four subunit A transcripts evaluated. Etiolation resulted in a slight increase in transcript levels. All four transcripts appeared to behave identically with respect to stress conditions tested with no significant differential regulation

Leisingera sp. JC1, a Bacterial Isolate from Hawaiian Bobtail Squid Eggs, Produces Indigoidine and Differentially Inhibits Vibrios

Female members of many cephalopod species house a bacterial consortium that is part of their reproductive system, the accessory nidamental gland (ANG). These bacteria are deposited into eggs that are then laid in the environment where they must develop unprotected from predation, pathogens and fouling. In this study, we characterized the genome and secondary metabolite production of Leisingera sp. JC1, a member of the roseobacter clade (Rhodobacteraceae) of Alphaproteobacteria isolated from the jelly coat of eggs from the Hawaiian bobtail squid, Euprymna scolopes. Whole genome sequencing and MLSA analysis revealed that Leisingera sp. JC1 falls within a group of roseobacters associated with squid ANGs. Genome and biochemical analyses revealed the potential for and production of a number of secondary metabolites, including siderophores and acyl-homoserine lactones involved with quorum sensing. The complete biosynthetic gene cluster for the pigment indigoidine was detected in the genome and mass spectrometry confirmed the production of this compound. Furthermore, we investigated the production of indigoidine under co-culture conditions with Vibrio fischeri, the light organ symbiont of E. scolopes, and with other vibrios. Finally, both Leisingera sp. JC1 and secondary metabolite extracts of this strain had differential antimicrobial activity against a number of marine vibrios, suggesting that Leisingera sp. JC1 may play a role in host defense against other marine bacteria either in the eggs and/or ANG. These data also suggest that indigoidine may be partially, but not wholly, responsible for the antimicrobial activity of this squid-associated bacterium.

Home and away- the evolutionary dynamics of homing endonucleases

<p>Abstract</p> <p>Background</p> <p>Homing endonucleases (HEases) are a large and diverse group of site-specific DNAases. They reside within self-splicing introns and inteins, and promote their horizontal dissemination. In recent years, HEases have been the focus of extensive research due to their promising potential use in gene targeting procedures for the treatment of genetic diseases and for the genetic engineering of crop, animal models and cell lines.</p> <p>Results</p> <p>Using mathematical analysis and computational modeling, we present here a novel account for the evolution and population dynamics of HEase genes (HEGs). We describe HEGs as paradoxical selfish elements whose long-term persistence in a single population relies on low transmission rates and a positive correlation between transmission efficiency and toxicity.</p> <p>Conclusion</p> <p>Plausible conditions allow HEGs to sustain at high frequency through long evolutionary periods, with the endonuclease frequency being either at equilibrium or periodically oscillating. The predictions of our model may prove important not only for evolutionary theory but also for gene therapy and bio-engineering applications of HEases.</p

Ancient horizontal gene transfer and the last common ancestors

Background The genomic history of prokaryotic organismal lineages is marked by extensive horizontal gene transfer (HGT) between groups of organisms at all taxonomic levels. These HGT events have played an essential role in the origin and distribution of biological innovations. Analyses of ancient gene families show that HGT existed in the distant past, even at the time of the organismal last universal common ancestor (LUCA). Most gene transfers originated in lineages that have since gone extinct. Therefore, one cannot assume that the last common ancestors of each gene were all present in the same cell representing the cellular ancestor of all extant life. Results Organisms existing as part of a diverse ecosystem at the time of LUCA likely shared genetic material between lineages. If these other lineages persisted for some time, HGT with the descendants of LUCA could have continued into the bacterial and archaeal lineages. Phylogenetic analyses of aminoacyl-tRNA synthetase protein families support the hypothesis that the molecular common ancestors of the most ancient gene families did not all coincide in space and time. This is most apparent in the evolutionary histories of seryl-tRNA synthetase and threonyl-tRNA synthetase protein families, each containing highly divergent “rare” forms, as well as the sparse phylogenetic distributions of pyrrolysyl-tRNA synthetase, and the bacterial heterodimeric form of glycyl-tRNA synthetase. These topologies and phyletic distributions are consistent with horizontal transfers from ancient, likely extinct branches of the tree of life. Conclusions Of all the organisms that may have existed at the time of LUCA, by definition only one lineage is survived by known progeny; however, this lineage retains a genomic record of heterogeneous genetic origins. The evolutionary histories of aminoacyl-tRNA synthetases (aaRS) are especially informative in detecting this signal, as they perform primordial biological functions, have undergone several ancient HGT events, and contain many sites with low substitution rates allowing deep phylogenetic reconstruction. We conclude that some aaRS families contain groups that diverge before LUCA. We propose that these ancient gene variants be described by the term “hypnologs”, reflecting their ancient, reticulate origin from a time in life history that has been all but erased”.National Science Foundation (U.S.) (Grant DEB 0830024)Exobiology Program (U.S.) (Grant NNX10AR85G)United States. National Aeronautics and Space Administration (Postdoctoral Program

AST: An Automated Sequence-Sampling Method for Improving the Taxonomic Diversity of Gene Phylogenetic Trees

A challenge in phylogenetic inference of gene trees is how to properly sample a large pool of homologous sequences to derive a good representative subset of sequences. Such a need arises in various applications, e.g. when (1) accuracy-oriented phylogenetic reconstruction methods may not be able to deal with a large pool of sequences due to their high demand in computing resources; (2) applications analyzing a collection of gene trees may prefer to use trees with fewer operational taxonomic units (OTUs), for instance for the detection of horizontal gene transfer events by identifying phylogenetic conflicts; and (3) the pool of available sequences is biased towards extensively studied species. In the past, the creation of subsamples often relied on manual selection. Here we present an Automated sequence-Sampling method for improving the Taxonomic diversity of gene phylogenetic trees, AST, to obtain representative sequences that maximize the taxonomic diversity of the sampled sequences. To demonstrate the effectiveness of AST, we have tested it to solve four problems, namely, inference of the evolutionary histories of the small ribosomal subunit protein S5 of E. coli, 16 S ribosomal RNAs and glycosyl-transferase gene family 8, and a study of ancient horizontal gene transfers from bacteria to plants. Our results show that the resolution of our computational results is almost as good as that of manual inference by domain experts, hence making the tool generally useful to phylogenetic studies by non-phylogeny specialists. The program is available at http://csbl.bmb.uga.edu/~zhouchan/AST.php

Evolution of proton pumping ATPases: rooting the tree of life

Abstract Proton pumping ATPases are found in all groups of present day organisms. The F-ATPases of eubacteria, mitochondria and chloroplasts also function as ATP synthases, i.e., they catalyze the final step that transforms the energy available from reduction/oxidation reactions (e.g., in photosynthesis) into ATP, the usual energy currency of modern cells. The primary structure of these ATPases/ATP synthases was found to be much more conserved between different groups of bacteria than other parts of the photosynthetic machinery, e.g., reaction center proteins and redox carrier complexes. These F-ATPases and the vacuolar type ATPase, which is found on many of the endomembranes of eukaryotic cells, were shown to be homologous to each other; i.e., these two groups of ATPases evolved from the same enzyme present in the common ancestor. (The term eubacteria is used here to denote the phylogenetic group containing all bacteria except the archaebacteria.) Sequences obtained for the plasmamembrane ATPase of various archaebacteria revealed that this ATPase is much more similar to the eukaryotic than to the eubacterial counterpart. The eukaryotic cell of higher organisms evolved from a symbiosis between eubacteria (that evolved into mitochondria and chloroplasts) and a host organism. Using the vacuolar type ATPase as a molecular marker for the cytoplasmic component of the eukaryotic cell reveals that this host organism was a close relative of the archaebacteria. A unique feature of the evolution of the ATPases is the presence of a non-catalytic subunit that is paralogous to the catalytic subunit, i.e., the two types of subunits evolved from a common ancestral gene. Since the gene duplication that gave rise to these two types of subunits had already occurred in the last common ancestor of all living organisms, this non-catalytic subunit can be used to root the tree of life by means of an outgroup; that is, the location of the last common ancestor of the major domains of living organisms (archaebacteria, eubacteria and eukaryotes) can be located in the tree of life without assuming constant or equal rates of change in the different branches. A correlation between structure and function of ATPases has been established for present day organisms. Implications resulting from this correlation for biochemical pathways, especially photosynthesis, that were operative in the last common ancestor and preceding life forms are discussed. The concept of chemi-osmotic coupling Photosynthetic energy transduction requires the formation of an energy-rich compound that can be utilized by other biochemical reactions. Pete

Data from: The effects of model choice and mitigating bias on the ribosomal tree of life

Deep-level relationships within Bacteria, Archaea, and Eukarya as well as the relationships of these three domains to each other require resolution. The ribosomal machinery, universal to all cellular life, represents a protein repertoire resistant to horizontal gene transfer, which provides a largely congruent signal necessary for reconstructing a tree suitable as a backbone for life’s reticulate history. Here, we generate a ribosomal tree of life from a robust taxonomic sampling of Bacteria, Archaea, and Eukarya to elucidate deep-level intra-domain and inter-domain relationships. Lack of phylogenetic information and systematic errors caused by inadequate models (that cannot account for substitution rate or compositional heterogeneities) or improper model selection compound conflicting phylogenetic signals from HGT and/or paralogy. Thus, we tested several models of varying sophistication on three different datasets, performed removal of fast-evolving or long-branched Archaea and Eukarya, and employed three different strategies to remove compositional heterogeneity to examine their effects on the topological outcome. Our results support a two-domain topology for the tree of life, where Eukarya emerges from within Archaea as sister to a Korarchaeota/Thaumarchaeota (KT) or Crenarchaeota/KT clade for all models under all or at least one of the strategies employed. Taxonomic manipulation allows single-matrix and certain mixture models to vacillate between two-domain and three-domain phylogenies. We find that models vary in their ability to resolve different areas of the tree of life, which does not necessarily correlate with model complexity. For example, both single-matrix and some mixture models recover monophyletic Crenarchaeota and Euryarchaeota archaeal phyla. In contrast, the most sophisticated model recovers a paraphyletic Euryarchaeota but detects two large clades that comprise the Bacteria, which were recovered separately but never together in the other models. Overall, models recovered consistent topologies despite dataset modifications due to the removal of compositional bias, which reflects either ineffective bias reduction or robust datasets that allow models to overcome reconstruction artifacts. We recommend a comparative approach for evolutionary models to identify model weaknesses as well as consensus relationships

aeb2 phylogenies

Aeb2 includes members of Bacteria, Archaea, and Eukarya. Methods of tree inference included maximum likelihood as implemented in RAxML, PhyML-4X (Le et al., 2012), and PhyML-Structure (Le and Gascuel, 2010) or Bayesian inference as implemented in PhyloBayes v. 3.3 or 3.3e (Lartillot et al., 2009). Aeb2 includes “Archezoan” (polyphyletic group of long branched eukaryotes such as Giardia, Trichomonas, Microsporidia, and Entamoeba) sequences; the subset “aeb2 Arch+” refers to the presence of Archezoa without Korarchaeota and Thaumarchaeota and the subset, “aeb2 KT+” refers to the presence of Korarchaeota and Thaumarchaeota without Archezoa. Aeb2 Arch+ and KT+ attempt to mitigate long-branch attraction (LBA) artifacts due to substitution rate saturation and allow us to assess the influence of taxonomic sampling on phylogenetic outcome. Gap removal occurred after the creation of the supermatrix (resulting in 13929 positions for aeb2 Arch+ and 13941 positions for aeb2 KT+)