The evolution and functional repertoire of translation proteins following the origin of life

<p>Abstract</p> <p>Background</p> <p>The RNA world hypothesis posits that the earliest genetic system consisted of informational RNA molecules that directed the synthesis of modestly functional RNA molecules. Further evidence suggests that it was within this RNA-based genetic system that life developed the ability to synthesize proteins by translating genetic code. Here we investigate the early development of the translation system through an evolutionary survey of protein architectures associated with modern translation.</p> <p>Results</p> <p>Our analysis reveals a structural expansion of translation proteins immediately following the RNA world and well before the establishment of the DNA genome. Subsequent functional annotation shows that representatives of the ten most ancestral protein architectures are responsible for all of the core protein functions found in modern translation.</p> <p>Conclusions</p> <p>We propose that this early robust translation system evolved by virtue of a positive feedback cycle in which the system was able to create increasingly complex proteins to further enhance its own function.</p> <p>Reviewers</p> <p>This article was reviewed by Janet Siefert, George Fox, and Antonio Lazcano (nominated by Laura Landweber)</p

Biogeography and ecology of the rare and abundant microbial lineages in deep-sea hydrothermal vents

Author Posting. © The Author(s), 2014. This is the author's version of the work. It is posted here by permission of Oxford University Press for personal use, not for redistribution. The definitive version was published in FEMS Microbiology Ecology 91 (2015): 1-11, doi:10.1093/femsec/fiu016.Environmental gradients generate countless ecological niches in deep-sea hydrothermal vent systems, which foster diverse microbial communities. The majority of distinct microbial lineages in these communities occur in very low abundance. However, the ecological role and distribution of rare and abundant lineages, particularly in deep, hot subsurface environments, remains unclear. Here, we use 16S rRNA tag sequencing to describe biogeographic patterning and microbial community structure of both rare and abundant archaea and bacteria in hydrothermal vent systems. We show that while rare archaeal lineages and almost all bacterial lineages displayed geographically restricted community structuring patterns, the abundant lineages of archaeal communities displayed a much more cosmopolitan distribution. Finally, analysis of one high-volume, high-temperature fluid sample representative of the deep hot biosphere described a unique microbial community that differed from microbial populations in diffuse flow fluid or sulfide samples, yet the rare thermophilic archaeal groups showed similarities to those that occur in sulfides. These results suggest that while most archaeal and bacterial lineages in vents are rare and display a highly regional distribution, a small percentage of lineages, particularly within the archaeal domain, are successful at widespread dispersal and colonization.Funding for this work was provided by a grant from the NASA Astrobiology Institute to the Carnegie Institution of Washington.2015-12-0

Is the genetic landscape of the deep subsurface biosphere affected by viruses?

Viruses are powerful manipulators of microbial diversity, biogeochemistry, and evolution in the marine environment. Viruses can directly influence the genetic capabilities and the fitness of their hosts through the use of fitness factors and through horizontal gene transfer. However, the impact of viruses on microbial ecology and evolution is often overlooked in studies of the deep subsurface biosphere. Subsurface habitats connected to hydrothermal vent systems are characterized by constant fluid flux, dynamic environmental variability, and high microbial diversity. In such conditions, high adaptability would be an evolutionary asset, and the potential for frequent host-virus interactions would be high, increasing the likelihood that cellular hosts could acquire novel functions. Here, we review evidence supporting this hypothesis, including data indicating that microbial communities in subsurface hydrothermal fluids are exposed to a high rate of viral infection, as well as viral metagenomic data suggesting that the vent viral assemblage is particularly enriched in genes that facilitate horizontal gene transfer and host adaptability. Therefore, viruses are likely to play a crucial role in facilitating adaptability to the extreme conditions of these regions of the deep subsurface biosphere. We also discuss how these results might apply to other regions of the deep subsurface, where the nature of virus-host interactions would be altered, but possibly no less important, compared to more energetic hydrothermal systems

Submarine hydrothermal systems : a probable site for the origin of life

Submarine hydrothermal systems provide all of the conditions necessary for the abiotic synthesis of organic compounds, polymers, and simple cell-like organisms. An analysis of the Archaean rock and fossil record shows that fossils of simple organisms are found in rocks deposited in hydrothermal environments. Biochemical experiments have shown that thermal energy is an efficient means for the abiotic synthesis of 11protocell 11 structures. The continuous flow of circulating fluids in a hydrothermal system provides the thermal and chemical gradients which create the variation in cond'itions necessary for the successive reactions to take place. Other models for the origin of life fail to fulfill one or more of these requirements

Archaea and bacteria with surprising microdiversity show shifts in dominance over 1,000-year time scales in hydrothermal chimneys

Author Posting. © The Author(s), 2009. This is the author's version of the work. It is posted here by permission of National Academy of Sciences for personal use, not for redistribution. The definitive version was published in Proceedings of the National Academy of Sciences 107 (2010): 1612-1617, doi:10.1073/pnas.0905369107.The Lost City Hydrothermal Field, an ultramafic-hosted system located 15 km west of the Mid-Atlantic Ridge, has experienced at least 30,000 years of hydrothermal activity. Previous studies have shown that its carbonate chimneys form by mixing of ~90ºC, pH 9-11 hydrothermal fluids and cold seawater. Flow of methane and hydrogen-rich hydrothermal fluids in the porous interior chimney walls supports archaeal biofilm communities dominated by a single phylotype of Methanosarcinales. In this study, we have extensively sampled the carbonate-hosted archaeal and bacterial communities by obtaining sequences of >200,000 amplicons of the 16S rRNA V6 region and correlated the results with isotopic (230Th) ages of the chimneys over a 1200 year period. Rare sequences in young chimneys were often more abundant in older chimneys, indicating that members of the rare biosphere can become dominant members of the ecosystem when environmental conditions change. These results suggest that a long history of selection over many cycles of chimney growth has resulted in numerous closely related species at Lost City, each of which is pre-adapted to a particular set of re-occurring environmental conditions. Due to the unique characteristics of the Lost City Hydrothermal Field, these data offer an unprecedented opportunity to study the dynamics of a microbial ecosystem's rare biosphere over a thousand-year time scale.This research was supported by the W.M. Keck Foundation to MLS, the NASA Astrobiology Institute through the Carnegie Institution for Science to JAB and through the MBL to MLS, NSF Grant OCE0137206 and NOAA Ocean Exploration support to DSK, and grants 96-2116-M002-003 and 97-2752-M004-PAE to C.-C. Shen

Metagenomic Comparison of Two Thiomicrospira Lineages Inhabiting Contrasting Deep-Sea Hydrothermal Environments

Background: The most widespread bacteria in oxic zones of carbonate chimneys at the serpentinite-hosted Lost City hydrothermal field, Mid-Atlantic Ridge, belong to the Thiomicrospira group of sulfur-oxidizing chemolithoautotrophs. It is unclear why Thiomicrospira-like organisms thrive in these chimneys considering that Lost City hydrothermal fluids are notably lacking in hydrogen sulfide and carbon dioxide. Methodology/Principal Findings: Here we describe metagenomic sequences obtained from a Lost City carbonate chimney that are highly similar to the genome of Thiomicrospira crunogena XCL-2, an isolate from a basalt-hosted hydrothermal vent in the Pacific Ocean. Even though T. crunogena and Lost City Thiomicrospira inhabit different types of hydrothermal systems in different oceans, their genomic contents are highly similar. For example, sequences encoding the sulfur oxidation and carbon fixation pathways (including a carbon concentration mechanism) of T. crunogena are also present in the Lost City metagenome. Comparative genomic analyses also revealed substantial genomic changes that must have occurred since the divergence of the two lineages, including large genomic rearrangements, gene fusion events, a prophage insertion, and transposase activity. Conclusions/Significance: Our results show significant genomic similarity between Thiomicrospira organisms inhabiting different kinds of hydrothermal systems in different oceans, suggesting that these organisms are widespread and highl

Diversity and distribution of subseafloor Thermococcales populations in diffuse hydrothermal vents at an active deep-sea volcano in the northeast Pacific Ocean

Author Posting. © American Geophysical Union, 2006. This article is posted here by permission of American Geophysical Union for personal use, not for redistribution. The definitive version was published in Journal of Geophysical Research 111 (2006): G04016, doi:10.1029/2005JG000097.The presence, diversity, and distribution of a key group of subseafloor archaea, the Thermococcales, was examined in multiple diffuse flow hydrothermal vents at Axial Seamount, an active deep-sea volcano located in the northeast Pacific Ocean. A polymerase chain reaction (PCR) approach was used to determine if this group of subseafloor indicator organisms showed any phylogenetic distribution that may indicate distinct subseafloor communities at vents with different physical and chemical characteristics. Targeted primers for the Thermococcales 16S rRNA (small subunit ribosomal RNA) gene and intergenic transcribed spacer (ITS) region were designed and applied to organisms filtered in-situ directly from a variety of diffuse flow vents. Thermococcales were amplified from 9 of 11 samples examined, and it was determined that the ITS region is a better phylogenetic marker than the 16S rRNA in defining consistent groups of closely related sequences. Results show a relationship between environmental clone distribution and source vent chemistry. The most highly diluted vents with elevated iron and alkalinity contained a distinct group of Thermococcales as defined by the ITS region, suggesting separate subseafloor Thermococcales populations at diffuse vents within the Axial caldera.This work was supported by Washington Sea Grant (NA76RG0119), National Science Foundation (OCE 9816491), NSF IGERT (DGE- 9870713), NASA Astrobiology Institute through the Carnegie Geophysical Institute, the NOAA/PMEL Vents Program, NOAA West Coast and Polar Undersea Research Center, and by the Joint Institute for the Study of the Atmosphere and Ocean under NOAA Cooperative Agreement No. NA117RJ1232