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1.  Biological Feedbacks as Cause and Demise of Neoproterozoic Icehouse: Astrobiological Prospects for Faster Evolution and Importance of Cold Conditions 
PLoS ONE  2007;2(2):e214.
Several severe glaciations occurred during the Neoproterozoic eon, and especially near its end in the Cryogenian period (630–850 Ma). While the glacial periods themselves were probably related to the continental positions being appropriate for glaciation, the general coldness of the Neoproterozoic and Cryogenian as a whole lacks specific explanation. The Cryogenian was immediately followed by the Ediacaran biota and Cambrian Metazoan, thus understanding the climate-biosphere interactions around the Cryogenian period is central to understanding the development of complex multicellular life in general. Here we present a feedback mechanism between growth of eukaryotic algal phytoplankton and climate which explains how the Earth system gradually entered the Cryogenian icehouse from the warm Mesoproterozoic greenhouse. The more abrupt termination of the Cryogenian is explained by the increase in gaseous carbon release caused by the more complex planktonic and benthic foodwebs and enhanced by a diversification of metazoan zooplankton and benthic animals. The increased ecosystem complexity caused a decrease in organic carbon burial rate, breaking the algal-climatic feedback loop of the earlier Neoproterozoic eon. Prior to the Neoproterozoic eon, eukaryotic evolution took place in a slow timescale regulated by interior cooling of the Earth and solar brightening. Evolution could have proceeded faster had these geophysical processes been faster. Thus, complex life could theoretically also be found around stars that are more massive than the Sun and have main sequence life shorter than 10 Ga. We also suggest that snow and glaciers are, in a statistical sense, important markers for conditions that may possibly promote the development of complex life on extrasolar planets.
PMCID: PMC1788933  PMID: 17299594
2.  Photooxidation of nucleic acids on metal oxides: physico-chemical and astrobiological perspectives 
Photocatalytic oxidation of nucleic acid components on aqueous metal oxides (TiO2, α-FeOOH, and α-Fe2O3) has been studied. The oxidation of purine nucleotides results in the formation of the purine radical cations and sugar-phosphate radicals, whereas the oxidation of pyrimidine nucleotides other than thymine results in the oxidation of only the sugar-phosphate. The oxidation of the thymine (and to a far less extent for the 5-methylcytosine) derivatives results in deprotonation from the methyl group of the base. Some single stranded (ss) oligoribonucleotides and wild-type ss RNA were oxidized at purine sites. In contrast, double stranded (ds) oligoribonucleotides and DNA were not oxidized. These results account for observations suggesting that cellular ds DNA is not damaged by exposure to photoirradiated TiO2 nanoparticles inserted into the cell, whereas ss RNA is extensively damaged. The astrobiological import of our observations is that the rapid degradation of monomer nucleotides make them poor targets as biosignatures, whereas duplex DNA is a better target as it is resilient to oxidative diagenesis. Another import of our studies is that ds DNA (as opposed to ss RNA) appears to be optimized to withstand oxidative stress both due to the advantageous polymer morphology and the subtle details of its radical chemistry. This peculiarity may account for the preference for DNA over RNA as a “molecule of life” provided that metal oxides served as the template for synthesis of polynucleotides, as suggested by Orgel and others.
PMCID: PMC3049938  PMID: 21399705
3.  Defining Life 
Astrobiology  2010;10(10):1021-1030.
Any definition is intricately connected to a theory that gives it meaning. Accordingly, this article discusses various definitions of life held in the astrobiology community by considering their connected “theories of life.” These include certain “list” definitions and a popular definition that holds that life is a “self-sustaining chemical system capable of Darwinian evolution.” We then act as “anthropologists,” studying what scientists do to determine which definition-theories of life they constructively hold as they design missions to seek non-terran life. We also look at how constructive beliefs about biosignatures change as observational data accumulate. And we consider how a definition centered on Darwinian evolution might itself be forced to change as supra-Darwinian species emerge, including in our descendents, and consider the chances of our encountering supra-Darwinian species in our exploration of the Cosmos. Last, we ask what chemical structures might support Darwinian evolution universally; these structures might be universal biosignatures. Key Words: Evolution—Life—Life detection—Biosignatures. Astrobiology 10, 1021–1030.
PMCID: PMC3005285  PMID: 21162682
4.  Raman spectroscopy as a potentialmethod for the detection of extremely halophilic archaea embedded in halite in terrestrial and possibly extraterrestrial samples 
Journal of Raman spectroscopy : JRS  2009;40(12):1996-2003.
Evidence for the widespread occurrence of extraterrestrial halite, particularly on Mars, has led to speculations on the possibility of halophilic microbial forms of life; these ideas have been strengthened by reports of viable haloarchaea from sediments of geological age (millions of years). Raman spectroscopy, being a sensitive detection method for future astrobiological investigations onsite, has been used in the current study for the detection of nine different extremely halophilic archaeal strains which had been embedded in laboratory-made halite crystals in order to simulate evaporitic conditions. The cells accumulated preferentially in tiny fluid inclusions, in simulation of the precipitation of salt in natural brines. FT-Raman spectroscopy using laser excitation at 1064 nm and dispersive micro Raman spectroscopy at 514.5 nm were applied. The spectra showed prominent peaks at 1507, 1152 and 1002 cm−1 which are attributed to haloarchaeal C50 carotenoid compounds (mainly bacterioruberins). Their intensity varied from strain to strain at 1064-nm laser excitation. Other distinguishable features were peaks due to peptide bonds (amide I, amide III) and to nucleic acids. No evidence for fatty acids was detected, consistent with their general absence in all archaea.
These results contribute to a growing database on Raman spectra of terrestrial microorganisms from hypersaline environments and highlight the influence of the different macromolecular composition of diverse strains on these spectra.
PMCID: PMC3207228  PMID: 22058585
Raman spectroscopy; extremely halophilic archaea; halite; astrobiology; fluid inclusions; carotenoids; bacterioruberins; Martian subsurface
5.  Remote automated multi-generational growth and observation of an animal in low Earth orbit 
The ultimate survival of humanity is dependent upon colonization of other planetary bodies. Key challenges to such habitation are (patho)physiologic changes induced by known, and unknown, factors associated with long-duration and distance space exploration. However, we currently lack biological models for detecting and studying these changes. Here, we use a remote automated culture system to successfully grow an animal in low Earth orbit for six months. Our observations, over 12 generations, demonstrate that the multi-cellular soil worm Caenorhabditis elegans develops from egg to adulthood and produces progeny with identical timings in space as on the Earth. Additionally, these animals display normal rates of movement when fully fed, comparable declines in movement when starved, and appropriate growth arrest upon starvation and recovery upon re-feeding. These observations establish C. elegans as a biological model that can be used to detect changes in animal growth, development, reproduction and behaviour in response to environmental conditions during long-duration spaceflight. This experimental system is ready to be incorporated on future, unmanned interplanetary missions and could be used to study cost-effectively the effects of such missions on these biological processes and the efficacy of new life support systems and radiation shielding technologies.
PMCID: PMC3262433  PMID: 22130552
Caenorhabditis elegans; spaceflight; astrobiology; interplanetary transfer
6.  The algorithmic origins of life 
Although it has been notoriously difficult to pin down precisely what is it that makes life so distinctive and remarkable, there is general agreement that its informational aspect is one key property, perhaps the key property. The unique informational narrative of living systems suggests that life may be characterized by context-dependent causal influences, and, in particular, that top-down (or downward) causation—where higher levels influence and constrain the dynamics of lower levels in organizational hierarchies—may be a major contributor to the hierarchal structure of living systems. Here, we propose that the emergence of life may correspond to a physical transition associated with a shift in the causal structure, where information gains direct and context-dependent causal efficacy over the matter in which it is instantiated. Such a transition may be akin to more traditional physical transitions (e.g. thermodynamic phase transitions), with the crucial distinction that determining which phase (non-life or life) a given system is in requires dynamical information and therefore can only be inferred by identifying causal architecture. We discuss some novel research directions based on this hypothesis, including potential measures of such a transition that may be amenable to laboratory study, and how the proposed mechanism corresponds to the onset of the unique mode of (algorithmic) information processing characteristic of living systems.
PMCID: PMC3565706  PMID: 23235265
origins of life; emergence; astrobiology; top-down causation
7.  Microbial community structure across the tree of life in the extreme Río Tinto 
The ISME journal  2010;5(1):42-50.
Understanding biotic versus abiotic forces that shape community structure is a fundamental aim of microbial ecology. The acidic and heavy metal extreme Río Tinto (RT) in southwestern Spain provides a rare opportunity to conduct an ecosystem-wide biodiversity inventory at the level of all three domains of life, because diversity there is low and almost exclusively microbial. Despite improvements in high-throughput DNA sequencing, environmental biodiversity studies that use molecular metrics and consider entire ecosystems are rare. These studies can be prohibitively expensive if domains are considered separately, and differences in copy number of eukaryotic ribosomal RNA genes can bias estimates of relative abundances of phylotypes recovered. In this study we have overcome these barriers (1) by targeting all three domains in a single polymerase chain reaction amplification and (2) by using a replicated sampling design that allows for incidence-based methods to extract measures of richness and carry out downstream analyses that address community structuring effects. Our work showed that combined bacterial and archaeal richness is an order of magnitude higher than eukaryotic richness. We also found that eukaryotic richness was highest at the most extreme sites, whereas combined bacterial and archaeal richness was highest at less extreme sites. Quantitative community phylogenetics showed abiotic forces to be primarily responsible for shaping the RT community structure. Canonical correspondence analysis revealed co-occurrence of obligate symbionts and their putative hosts that may contribute to biotic forces shaping community structure and may further provide a possible mechanism for persistence of certain low-abundance bacteria encountered in the RT.
PMCID: PMC3105667  PMID: 20631808
community phylogenetics, astrobiology, CCA
8.  Microbial communities in the subglacial waters of the Vatnajökull ice cap, Iceland 
The ISME Journal  2012;7(2):427-437.
Subglacial lakes beneath the Vatnajökull ice cap in Iceland host endemic communities of microorganisms adapted to cold, dark and nutrient-poor waters, but the mechanisms by which these microbes disseminate under the ice and colonize these lakes are unknown. We present new data on this subglacial microbiome generated from samples of two subglacial lakes, a subglacial flood and a lake that was formerly subglacial but now partly exposed to the atmosphere. These data include parallel 16S rRNA gene amplicon libraries constructed using novel primers that span the v3–v5 and v4–v6 hypervariable regions. Archaea were not detected in either subglacial lake, and the communities are dominated by only five bacterial taxa. Our paired libraries are highly concordant for the most abundant taxa, but estimates of diversity (abundance-based coverage estimator) in the v4–v6 libraries are 3–8 times higher than in corresponding v3–v5 libraries. The dominant taxa are closely related to cultivated anaerobes and microaerobes, and may occupy unique metabolic niches in a chemoautolithotrophic ecosystem. The populations of the major taxa in the subglacial lakes are indistinguishable (>99% sequence identity), despite separation by 6 km and an ice divide; one taxon is ubiquitous in our Vatnajökull samples. We propose that the glacial bed is connected through an aquifer in the underlying permeable basalt, and these subglacial lakes are colonized from a deeper, subterranean microbiome.
PMCID: PMC3554413  PMID: 22975882
acetogenesis; astrobiology; extreme environments; psychrophiles; pyrosequencing; subglacial lakes
9.  Description of International Caenorhabditis elegans Experiment first flight (ICE-FIRST) 
Traveling, living and working in space is now a reality. The number of people and length of time in space is increasing. With new horizons for exploration it becomes more important to fully understand and provide countermeasures to the effects of the space environment on the human body. In addition, space provides a unique laboratory to study how life and physiologic functions adapt from the cellular level to that of the entire organism. Caenorhabditis elegans is a genetic model organism used to study physiology on Earth. Here we provide a description of the rationale, design, methods, and space culture validation of the ICE-FIRST payload, which engaged C. elegans researchers from four nations. Here we also show C. elegans growth and development proceeds essentially normally in a chemically defined liquid medium on board the International Space Station (10.9 day round trip). By setting flight constraints first and bringing together established C. elegans researchers second, we were able to use minimal stowage space to successfully return a total of 53 independent samples, each containing more than a hundred individual animals, to investigators within one year of experiment concept. We believe that in the future, bringing together individuals with knowledge of flight experiment operations, flight hardware, space biology, and genetic model organisms should yield similarly successful payloads.
PMCID: PMC2493420  PMID: 22146801
Caenorhabditis elegans; Spaceflight; Development; Axenic culture; Astrobiology
10.  Workshops without Walls: Broadening Access to Science around the World 
PLoS Biology  2011;9(8):e1001118.
The National Aeronautics and Space Administration (NASA) Astrobiology Institute (NAI) conducted two “Workshops Without Walls” during 2010 that enabled global scientific exchange—with no travel required. The second of these was on the topic “Molecular Paleontology and Resurrection: Rewinding the Tape of Life.” Scientists from diverse disciplines and locations around the world were joined through an integrated suite of collaborative technologies to exchange information on the latest developments in this area of origin of life research. Through social media outlets and popular science blogs, participation in the workshop was broadened to include educators, science writers, and members of the general public. In total, over 560 people from 31 US states and 30 other nations were registered. Among the scientific disciplines represented were geochemistry, biochemistry, molecular biology and evolution, and microbial ecology. We present this workshop as a case study in how interdisciplinary collaborative research may be fostered, with substantial public engagement, without sustaining the deleterious environmental and economic impacts of travel.
PMCID: PMC3149038  PMID: 21829326
11.  Gause's Principle and the Effect of Resource Partitioning on the Dynamical Coexistence of Replicating Templates 
PLoS Computational Biology  2013;9(8):e1003193.
Models of competitive template replication, although basic for replicator dynamics and primordial evolution, have not yet taken different sequences explicitly into account, neither have they analyzed the effect of resource partitioning (feeding on different resources) on coexistence. Here we show by analytical and numerical calculations that Gause's principle of competitive exclusion holds for template replicators if resources (nucleotides) affect growth linearly and coexistence is at fixed point attractors. Cases of complementary or homologous pairing between building blocks with parallel or antiparallel strands show no deviation from the rule that the nucleotide compositions of stably coexisting species must be different and there cannot be more coexisting replicator species than nucleotide types. Besides this overlooked mechanism of template coexistence we show also that interesting sequence effects prevail as parts of sequences that are copied earlier affect coexistence more strongly due to the higher concentration of the corresponding replication intermediates. Template and copy always count as one species due their constraint of strict stoichiometric coupling. Stability of fixed-point coexistence tends to decrease with the length of sequences, although this effect is unlikely to be detrimental for sequences below 100 nucleotides. In sum, resource partitioning (niche differentiation) is the default form of competitive coexistence for replicating templates feeding on a cocktail of different nucleotides, as it may have been the case in the RNA world. Our analysis of different pairing and strand orientation schemes is relevant for artificial and potentially astrobiological genetics.
Author Summary
The dynamical theory of competing templates has not yet taken the effect of sequences explicitly into account. One might think that complementary sequences have very limited competition only. We show that, despite interesting sequence effects, competing template replicators yield to Gause's principle of competitive exclusion so that the number of stably coexisting template species cannot exceed the number of nucleotide species on which they grow, although one of the findings is that plus and minus strands together count as one species. Thus up to four different templates/ribozymes can constitute the first steps to an early, segmented genome: we suggest that other mechanisms build on this baseline mechanism.
PMCID: PMC3749944  PMID: 23990769
12.  The origin of modern terrestrial life 
HFSP Journal  2007;1(3):156-168.
The study of the origin of life covers many areas of expertise and requires the input of various scientific communities. In recent years, this research field has often been viewed as part of a broader agenda under the name of “exobiology” or “astrobiology.” In this review, we have somewhat narrowed this agenda, focusing on the origin of modern terrestrial life. The adjective “modern” here means that we did not speculate on different forms of life that could have possibly appeared on our planet, but instead focus on the existing forms (cells and viruses). We try to briefly present the state of the art about alternative hypotheses discussing not only the origin of life per se, but also how life evolved to produce the modern biosphere through a succession of steps that we would like to characterize as much as possible.
PMCID: PMC2640990  PMID: 19404443
13.  At the crossroads of biomacromolecular research: highlighting the interdisciplinary nature of the field 
Due to their complexity and wide-ranging utility, biomacromolecular research is an especially interdisciplinary branch of chemistry. It is my goal that the Biomacromolecules subject area of Chemistry Central Journal will parallel this richness and diversity. In this inaugural commentary, I attempt to set the stage for achieving this by highlighting several areas where biomacromolecular research overlaps more traditional chemistry sub-disciplines. Specifically, it is discussed how Materials Science and Biotechnology, Analytical Chemistry, Cell Biology and Chemical Theory are each integral to modern biomacromolecular research. Investigators with reports in any of these areas, or any other dealing with biomacromolecules, are encouraged to submit their research papers to Chemistry Central Journal.
PMCID: PMC1975824  PMID: 17939851
14.  Boron Enrichment in Martian Clay 
PLoS ONE  2013;8(6):e64624.
We have detected a concentration of boron in martian clay far in excess of that in any previously reported extra-terrestrial object. This enrichment indicates that the chemistry necessary for the formation of ribose, a key component of RNA, could have existed on Mars since the formation of early clay deposits, contemporary to the emergence of life on Earth. Given the greater similarity of Earth and Mars early in their geological history, and the extensive disruption of Earth's earliest mineralogy by plate tectonics, we suggest that the conditions for prebiotic ribose synthesis may be better understood by further Mars exploration.
PMCID: PMC3675118  PMID: 23762242
15.  The Enzymatic and Metabolic Capabilities of Early Life 
PLoS ONE  2012;7(9):e39912.
We introduce the concept of metaconsensus and employ it to make high confidence predictions of early enzyme functions and the metabolic properties that they may have produced. Several independent studies have used comparative bioinformatics methods to identify taxonomically broad features of genomic sequence data, protein structure data, and metabolic pathway data in order to predict physiological features that were present in early, ancestral life forms. But all such methods carry with them some level of technical bias. Here, we cross-reference the results of these previous studies to determine enzyme functions predicted to be ancient by multiple methods. We survey modern metabolic pathways to identify those that maintain the highest frequency of metaconsensus enzymes. Using the full set of modern reactions catalyzed by these metaconsensus enzyme functions, we reconstruct a representative metabolic network that may reflect the core metabolism of early life forms. Our results show that ten enzyme functions, four hydrolases, three transferases, one oxidoreductase, one lyase, and one ligase, are determined by metaconsensus to be present at least as late as the last universal common ancestor. Subnetworks within central metabolic processes related to sugar and starch metabolism, amino acid biosynthesis, phospholipid metabolism, and CoA biosynthesis, have high frequencies of these enzyme functions. We demonstrate that a large metabolic network can be generated from this small number of enzyme functions.
PMCID: PMC3438178  PMID: 22970111
16.  Grazers and Phytoplankton Growth in the Oceans: an Experimental and Evolutionary Perspective 
PLoS ONE  2013;8(10):e77349.
The taxonomic composition of phytoplankton responsible for primary production on continental shelves has changed episodically through Earth history. Geological correlations suggest that major changes in phytoplankton composition correspond in time to changes in grazing and seawater chemistry. Testing hypotheses that arise from these correlations requires experimentation, and so we carried out a series of experiments in which selected phytoplankton species were grown in treatments that differed with respect to the presence or absence of grazers as well as seawater chemistry. Both protistan (Euplotes sp.) and microarthropod (Acartia tonsa) grazers changed the growth dynamics and biochemical composition of the green alga Tetraselmis suecica, the diatom Thalassiosira weissflogii, and the cyanobacterium Synechococcus sp., increasing the specific growth rate and palatability of the eukaryotic algae, while decreasing or leaving unchanged both parameters in the cyanobacteria. Synechococcus (especially) and Thalassiosira produced toxins effective against the copepod, but ciliate growth was unaffected. Acartia induced a 4-6 fold increase of Si cell quota in the diatom, but Euplotes had no similar effect. The differential growth responses of the eukaryotic algae and cyanobacteria to ciliate grazing may help to explain the apparently coeval radiation of eukaryophagic protists and rise of eukaryotes to ecological prominence as primary producers in Neoproterozoic oceans. The experimental results suggest that phytoplankton responses to the later radiation of microarthropod grazers were clade-specific, and included changes in growth dynamics, toxin synthesis, encystment, and (in diatoms) enhanced Si uptake.
PMCID: PMC3811990  PMID: 24204815
17.  Cultivation and Complete Genome Sequencing of Gloeobacter kilaueensis sp. nov., from a Lava Cave in Kīlauea Caldera, Hawai'i 
PLoS ONE  2013;8(10):e76376.
The ancestor of Gloeobacter violaceus PCC 7421T is believed to have diverged from that of all known cyanobacteria before the evolution of thylakoid membranes and plant plastids. The long and largely independent evolutionary history of G. violaceus presents an organism retaining ancestral features of early oxygenic photoautotrophs, and in whom cyanobacteria evolution can be investigated. No other Gloeobacter species has been described since the genus was established in 1974 (Rippka et al., Arch Microbiol 100:435). Gloeobacter affiliated ribosomal gene sequences have been reported in environmental DNA libraries, but only the type strain's genome has been sequenced. However, we report here the cultivation of a new Gloeobacter species, G. kilaueensis JS1T, from an epilithic biofilm in a lava cave in Kīlauea Caldera, Hawai'i. The strain's genome was sequenced from an enriched culture resembling a low-complexity metagenomic sample, using 9 kb paired-end 454 pyrosequences and 400 bp paired-end Illumina reads. The JS1T and G. violaceus PCC 7421T genomes have little gene synteny despite sharing 2842 orthologous genes; comparing the genomes shows they do not belong to the same species. Our results support establishing a new species to accommodate JS1T, for which we propose the name Gloeobacter kilaueensis sp. nov. Strain JS1T has been deposited in the American Type Culture Collection (BAA-2537), the Scottish Marine Institute's Culture Collection of Algae and Protozoa (CCAP 1431/1), and the Belgian Coordinated Collections of Microorganisms (ULC0316). The G. kilaueensis holotype has been deposited in the Algal Collection of the US National Herbarium (US# 217948). The JS1T genome sequence has been deposited in GenBank under accession number CP003587. The G+C content of the genome is 60.54 mol%. The complete genome sequence of G. kilaueensis JS1T may further understanding of cyanobacteria evolution, and the shift from anoxygenic to oxygenic photosynthesis.
PMCID: PMC3806779  PMID: 24194836
18.  A Low Temperature Limit for Life on Earth 
PLoS ONE  2013;8(6):e66207.
There is no generally accepted value for the lower temperature limit for life on Earth. We present empirical evidence that free-living microbial cells cooling in the presence of external ice will undergo freeze-induced desiccation and a glass transition (vitrification) at a temperature between −10°C and −26°C. In contrast to intracellular freezing, vitrification does not result in death and cells may survive very low temperatures once vitrified. The high internal viscosity following vitrification means that diffusion of oxygen and metabolites is slowed to such an extent that cellular metabolism ceases. The temperature range for intracellular vitrification makes this a process of fundamental ecological significance for free-living microbes. It is only where extracellular ice is not present that cells can continue to metabolise below these temperatures, and water droplets in clouds provide an important example of such a habitat. In multicellular organisms the cells are isolated from ice in the environment, and the major factor dictating how they respond to low temperature is the physical state of the extracellular fluid. Where this fluid freezes, then the cells will dehydrate and vitrify in a manner analogous to free-living microbes. Where the extracellular fluid undercools then cells can continue to metabolise, albeit slowly, to temperatures below the vitrification temperature of free-living microbes. Evidence suggests that these cells do also eventually vitrify, but at lower temperatures that may be below −50°C. Since cells must return to a fluid state to resume metabolism and complete their life cycle, and ice is almost universally present in environments at sub-zero temperatures, we propose that the vitrification temperature represents a general lower thermal limit to life on Earth, though its precise value differs between unicellular (typically above −20°C) and multicellular organisms (typically below −20°C). Few multicellular organisms can, however, complete their life cycle at temperatures below ∼−2°C.
PMCID: PMC3686811  PMID: 23840425
19.  ExtremeDB: A Unified Web Repository of Extremophilic Archaea and Bacteria 
PLoS ONE  2013;8(5):e63083.
Extremophiles are the microorganisms which can survive under extreme conditions of temperature, pressure, pH, salinity etc. They have gained much attention for their potential role in biotechnological and industrial applications. The large amount of experimental data in the literature is so diverse, that it becomes difficult and time consuming for the researcher to implement it in various areas of research. Therefore, a systematic arrangement of data and redirection in a similar fashion through web interface can assist researchers in analyzing the data as per their requirement. ExtremeDB is a freely available web based relational database which integrates general characteristics, genome-proteome information, industrial applications and recent scientific investigations of the seven major groups of 865 extremophillic microorganisms. The search options are user friendly and analyses tools such as Compare and Extreme BLAST have been incorporated for comparative analysis of two or more extremophiles and determining the sequence similarity of a given protein/nucleotide in relation to other extremophiles respectively. The effort put forth herein in the form of database, would open up new avenues on the potential utility of extremophiles in applied research. ExtremeDB is freely accessible via
PMCID: PMC3656046  PMID: 23696792
20.  Amino Acid Substitutions in Cold-Adapted Proteins from Halorubrum lacusprofundi, an Extremely Halophilic Microbe from Antarctica 
PLoS ONE  2013;8(3):e58587.
The halophilic Archaeon Halorubrum lacusprofundi, isolated from the perennially cold and hypersaline Deep Lake in Antarctica, was recently sequenced and compared to 12 Haloarchaea from temperate climates by comparative genomics. Amino acid substitutions for 604 H. lacusprofundi proteins belonging to conserved haloarchaeal orthologous groups (cHOGs) were determined and found to occur at 7.85% of positions invariant in proteins from mesophilic Haloarchaea. The following substitutions were observed most frequently: (a) glutamic acid with aspartic acid or alanine; (b) small polar residues with other small polar or non-polar amino acids; (c) small non-polar residues with other small non-polar residues; (d) aromatic residues, especially tryptophan, with other aromatic residues; and (e) some larger polar residues with other similar residues. Amino acid substitutions for a cold-active H. lacusprofundi β-galactosidase were then examined in the context of a homology modeled structure at residues invariant in homologous enzymes from mesophilic Haloarchaea. Similar substitutions were observed as in the genome-wide approach, with the surface accessible regions of β-galactosidase displaying reduced acidity and increased hydrophobicity, and internal regions displaying mainly subtle changes among smaller non-polar and polar residues. These findings are consistent with H. lacusprofundi proteins displaying amino acid substitutions that increase structural flexibility and protein function at low temperature. We discuss the likely mechanisms of protein adaptation to a cold, hypersaline environment on Earth, with possible relevance to life elsewhere.
PMCID: PMC3594186  PMID: 23536799
21.  In Vitro Secondary Structure of the Genomic RNA of Satellite Tobacco Mosaic Virus 
PLoS ONE  2013;8(1):e54384.
Satellite tobacco mosaic virus (STMV) is a T = 1 icosahedral virus with a single-stranded RNA genome. It is widely accepted that the RNA genome plays an important structural role during assembly of the STMV virion. While the encapsidated form of the RNA has been extensively studied, less is known about the structure of the free RNA, aside from a purported tRNA-like structure at the 3′ end. Here we use selective 2′-hydroxyl acylation analyzed by primer extension (SHAPE) analysis to examine the secondary structure of in vitro transcribed STMV RNA. The predicted secondary structure is unusual in the sense that it is highly extended, which could be significant for protecting the RNA from degradation. The SHAPE data are also consistent with the previously predicted tRNA-like fold at the 3′ end of the molecule, which is also known to hinder degradation. Our data are not consistent with the secondary structure proposed for the encapsidated RNA by Schroeder et al., suggesting that, if the Schroeder structure is correct, either the RNA is packaged as it emerges from the replication complex, or the RNA undergoes extensive refolding upon encapsidation. We also consider the alternative, i.e., that the structure of the encapsidated STMV RNA might be the same as the in vitro structure presented here, and we examine how this structure might be organized in the virus. This possibility is not rigorously ruled out by the available data, so it remains open to examination by experiment.
PMCID: PMC3551766  PMID: 23349871
22.  Comparative Analysis of RNA Families Reveals Distinct Repertoires for Each Domain of Life 
PLoS Computational Biology  2012;8(11):e1002752.
The RNA world hypothesis, that RNA genomes and catalysts preceded DNA genomes and genetically-encoded protein catalysts, has been central to models for the early evolution of life on Earth. A key part of such models is continuity between the earliest stages in the evolution of life and the RNA repertoires of extant lineages. Some assessments seem consistent with a diverse RNA world, yet direct continuity between modern RNAs and an RNA world has not been demonstrated for the majority of RNA families, and, anecdotally, many RNA functions appear restricted in their distribution. Despite much discussion of the possible antiquity of RNA families, no systematic analyses of RNA family distribution have been performed. To chart the broad evolutionary history of known RNA families, we performed comparative genomic analysis of over 3 million RNA annotations spanning 1446 families from the Rfam 10 database. We report that 99% of known RNA families are restricted to a single domain of life, revealing discrete repertoires for each domain. For the 1% of RNA families/clans present in more than one domain, over half show evidence of horizontal gene transfer (HGT), and the rest show a vertical trace, indicating the presence of a complex protein synthesis machinery in the Last Universal Common Ancestor (LUCA) and consistent with the evolutionary history of the most ancient protein-coding genes. However, with limited interdomain transfer and few RNA families exhibiting demonstrable antiquity as predicted under RNA world continuity, our results indicate that the majority of modern cellular RNA repertoires have primarily evolved in a domain-specific manner.
Author Summary
In cells, DNA carries recipes for making proteins, and proteins perform chemical reactions, including replication of DNA. This interdependency raises questions for early evolution, since one molecule seemingly cannot exist without the other. A resolution to this problem is the RNA world, where RNA is postulated to have been both genetic material and primary catalyst. While artificially selected catalytic RNAs strengthen the chemical plausibility of an RNA world, a biological prediction is that some RNAs should date back to this period. In this study, we ask to what degree RNAs in extant organisms trace back to the common ancestor of cellular life. Using the Rfam RNA families database, we systematically screened genomes spanning the three domains of life (Archaea, Bacteria, Eukarya) for RNA genes, and examined how far back in evolution known RNA families can be traced. We find that 99% of RNA families are restricted to a single domain. Limited conservation within domains implies ongoing emergence of RNA functions during evolution. Of the remaining 1%, half show evidence of horizontal transfer (movement of genes between organisms), and half show an evolutionary history consistent with an RNA world. The oldest RNAs are primarily associated with protein synthesis and export.
PMCID: PMC3486863  PMID: 23133357
23.  An Intertwined Evolutionary History of Methanogenic Archaea and Sulfate Reduction 
PLoS ONE  2012;7(9):e45313.
Hydrogenotrophic methanogenesis and dissimilatory sulfate reduction, two of the oldest energy conserving respiratory systems on Earth, apparently could not have evolved in the same host, as sulfite, an intermediate of sulfate reduction, inhibits methanogenesis. However, certain methanogenic archaea metabolize sulfite employing a deazaflavin cofactor (F420)-dependent sulfite reductase (Fsr) where N- and C-terminal halves (Fsr-N and Fsr-C) are homologs of F420H2 dehydrogenase and dissimilatory sulfite reductase (Dsr), respectively. From genome analysis we found that Fsr was likely assembled from freestanding Fsr-N homologs and Dsr-like proteins (Dsr-LP), both being abundant in methanogens. Dsr-LPs fell into two groups defined by following sequence features: Group I (simplest), carrying a coupled siroheme-[Fe4-S4] cluster and sulfite-binding Arg/Lys residues; Group III (most complex), with group I features, a Dsr-type peripheral [Fe4-S4] cluster and an additional [Fe4-S4] cluster. Group II Dsr-LPs with group I features and a Dsr-type peripheral [Fe4-S4] cluster were proposed as evolutionary intermediates. Group III is the precursor of Fsr-C. The freestanding Fsr-N homologs serve as F420H2 dehydrogenase unit of a putative novel glutamate synthase, previously described membrane-bound electron transport system in methanogens and of assimilatory type sulfite reductases in certain haloarchaea. Among archaea, only methanogens carried Dsr-LPs. They also possessed homologs of sulfate activation and reduction enzymes. This suggested a shared evolutionary history for methanogenesis and sulfate reduction, and Dsr-LPs could have been the source of the oldest (3.47-Gyr ago) biologically produced sulfide deposit.
PMCID: PMC3448663  PMID: 23028926
24.  Bone Turnover in Wild Type and Pleiotrophin-Transgenic Mice Housed for Three Months in the International Space Station (ISS) 
PLoS ONE  2012;7(3):e33179.
Bone is a complex dynamic tissue undergoing a continuous remodeling process. Gravity is a physical force playing a role in the remodeling and contributing to the maintenance of bone integrity. This article reports an investigation on the alterations of the bone microarchitecture that occurred in wild type (Wt) and pleiotrophin-transgenic (PTN-Tg) mice exposed to a near-zero gravity on the International Space Station (ISS) during the Mice Drawer System (MDS) mission, to date, the longest mice permanence (91 days) in space. The transgenic mouse strain over-expressing pleiotrophin (PTN) in bone was selected because of the PTN positive effects on bone turnover. Wt and PTN-Tg control animals were maintained on Earth either in a MDS payload or in a standard vivarium cage. This study revealed a bone loss during spaceflight in the weight-bearing bones of both strains. For both Tg and Wt a decrease of the trabecular number as well as an increase of the mean trabecular separation was observed after flight, whereas trabecular thickness did not show any significant change. Non weight-bearing bones were not affected. The PTN-Tg mice exposed to normal gravity presented a poorer trabecular organization than Wt mice, but interestingly, the expression of the PTN transgene during the flight resulted in some protection against microgravity’s negative effects. Moreover, osteocytes of the Wt mice, but not of Tg mice, acquired a round shape, thus showing for the first time osteocyte space-related morphological alterations in vivo. The analysis of specific bone formation and resorption marker expression suggested that the microgravity-induced bone loss was due to both an increased bone resorption and a decreased bone deposition. Apparently, the PTN transgene protection was the result of a higher osteoblast activity in the flight mice.
PMCID: PMC3305296  PMID: 22438896
25.  Origination and Immigration Drive Latitudinal Gradients in Marine Functional Diversity 
PLoS ONE  2014;9(7):e101494.
Global patterns in the functional attributes of organisms are critical to understanding biodiversity trends and predicting biotic responses to environmental change. In the first global marine analysis, we find a strong decrease in functional richness, but a strong increase in functional evenness, with increasing latitude using intertidal-to-outer-shelf bivalves as a model system (N = 5571 species). These patterns appear to be driven by the interplay between variation in origination rates among functional groups, and latitudinal patterns in origination and range expansion, as documented by the rich fossil record of the group. The data suggest that (i) accumulation of taxa in spatial bins and functional categories has not impeded continued diversification in the tropics, and (ii) extinctions will influence ecosystem function differentially across latitudes.
PMCID: PMC4103801  PMID: 25036112

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