Xenorhodopsins, an enigmatic new class of microbial rhodopsins horizontally transferred between archaea and bacteria.
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ABSTRACT:
SUBMITTER: Ugalde JA
PROVIDER: S-EPMC3198991 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Metagenomics has provided access to genomes of as yet uncultivated microorganisms in natural environments, yet there are gaps in our knowledge-particularly for Archaea-that occur at relatively low abundance and in extreme environments. Ultrasmall cells (<500 nm in diameter) from lineages without cultivated representatives that branch near the crenarchaeal/euryarchaeal divide have been detected in a variety of acidic ecosystems. We reconstructed composite, near-complete approximately 1-Mb genomes for three lineages, referred to as ARMAN (archaeal Richmond Mine acidophilic nanoorganisms), from environmental samples and a biofilm filtrate. Genes of two lineages are among the smallest yet described, enabling a 10% higher coding density than found genomes of the same size, and there are noncontiguous genes. No biological function could be inferred for up to 45% of genes and no more than 63% of the predicted proteins could be assigned to a revised set of archaeal clusters of orthologous groups. Some core metabolic genes are more common in Crenarchaeota than Euryarchaeota, up to 21% of genes have the highest sequence identity to bacterial genes, and 12 belong to clusters of orthologous groups that were previously exclusive to bacteria. A small subset of 3D cryo-electron tomographic reconstructions clearly show penetration of the ARMAN cell wall and cytoplasmic membranes by protuberances extended from cells of the archaeal order Thermoplasmatales. Interspecies interactions, the presence of a unique internal tubular organelle [Comolli, et al. (2009) ISME J 3:159-167], and many genes previously only affiliated with Crenarchaea or Bacteria indicate extensive unique physiology in organisms that branched close to the time that Cren- and Euryarchaeotal lineages diverged.
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Project description:Because of methodological breakthroughs and the availability of an increasing amount of whole-genome sequence data, horizontal transfers (HTs) in eukaryotes have received much attention recently. Contrary to similar analyses in prokaryotes, most studies in eukaryotes usually investigate particular sequences corresponding to transposable elements (TEs), neglecting the other components of the genome. We present a new methodological framework for the genome-wide detection of all putative horizontally transferred sequences between two species that requires no prior knowledge of the transferred sequences. This method provides a broader picture of HTs in eukaryotes by fully exploiting complete-genome sequence data. In contrast to previous genome-wide approaches, we used a well-defined statistical framework to control for the number of false positives in the results, and we propose two new validation procedures to control for confounding factors. The first validation procedure relies on a comparative analysis with other species of the phylogeny to validate HTs for the nonrepeated sequences detected, whereas the second one built upon the study of the dynamics of the detected TEs. We applied our method to two closely related Drosophila species, Drosophila melanogaster and D. simulans, in which we discovered 10 new HTs in addition to all the HTs previously detected in different studies, which underscores our method's high sensitivity and specificity. Our results favor the hypothesis of multiple independent HTs of TEs while unraveling a small portion of the network of HTs in the Drosophila phylogeny.
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Project description:Ion-translocating retinylidene rhodopsins are widely distributed among marine and freshwater microbes. The translocation is light-driven, contributing to the production of biochemical energy in diverse microbes. Until today, most microbial rhodopsins had been detected using bioinformatics based on homology to other rhodopsins. In the past decade, there has been increased interest in microbial rhodopsins in the field of optogenetics since microbial rhodopsins were found to be most useful in vertebrate neuronal systems. Here we report on a functional metagenomic assay for detecting microbial rhodopsins. Using an array of narrow pH electrodes and light-emitting diode illumination, we were able to screen a metagenomic fosmid library to detect diverse marine proteorhodopsins and an actinorhodopsin based solely on proton-pumping activity. Our assay therefore provides a rather simple phenotypic means to enrich our understanding of microbial rhodopsins without any prior knowledge of the genomic content of the environmental entities screened.
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Project description:Rhodopsins are light-sensing proteins used in optogenetics. The word "rhodopsin" originates from the Greek words "rhodo" and "opsis," indicating rose and sight, respectively. Although the classical meaning of rhodopsin is the red-colored pigment in our eyes, the modern meaning of rhodopsin encompasses photoactive proteins containing a retinal chromophore in animals and microbes. Animal and microbial rhodopsins possess 11-cis and all-trans retinal, respectively, to capture light in seven transmembrane ?-helices, and photoisomerizations into all-trans and 13-cis forms, respectively, initiate each function. Ion-transporting proteins can be found in microbial rhodopsins, such as light-gated channels and light-driven pumps, which are the main tools in optogenetics. Light-driven pumps, such as archaeal H(+) pump bacteriorhodopsin (BR) and Cl(-) pump halorhodopsin (HR), were discovered in the 1970s, and their mechanism has been extensively studied. On the other hand, different kinds of H(+) and Cl(-) pumps have been found in marine bacteria, such as proteorhodopsin (PR) and Fulvimarina pelagi rhodopsin (FR), respectively. In addition, a light-driven Na(+) pump was found, Krokinobacter eikastus rhodopsin 2 (KR2). These light-driven ion-pumping microbial rhodopsins are classified as DTD, TSA, DTE, NTQ, and NDQ rhodopsins for BR, HR, PR, FR, and KR2, respectively. Recent understanding of ion-pumping microbial rhodopsins is reviewed in this paper.
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Project description:Horizontal gene transfer (HGT) is the process whereby an organism acquires exogenous genes (horizontally transferred genes or HT genes) that are not inherited from the parent, but are derived from another organism. In prokaryotes, HGT has been considered as one of the important driving forces of evolution. Previously, genome-wide analyses have been conducted for estimating the proportion of HT genes in prokaryotic genomes, but the number of species examined at the time was limited, and gene annotation was relatively poor. Currently, tens of thousands of prokaryotic genomes have been published and gene annotation resources have improved. In the present study, HT gene prediction method was modified so that the estimate was robust to gene length, conducting a comprehensive search using 3017 representative prokaryotic genomes belonging to 1348 species. The result showed that an average of 13% (ranging from 0% to 30% across species) of protein-coding genes was predicted as being of horizontal origin. The proportion of the predicted HT genes per species was associated with the species' habitat, while a positive correlation between the proportion and genomic nucleotide frequency was also observed. Moreover, the functions of the predicted HT genes were inferred and compared according to two popular databases, the Clusters of Orthologous Groups and the Kyoto Encyclopedia of Genes and Genomes. As a result, both databases indicated that many of the widely transferred genes were involved in mobile genetic elements (transposons, phages, and plasmids) as expected. Notably, the present study predicted that six as-yet-uncharacterized genes were widely distributed HT genes, and therefore, will be interesting targets for evolutionary studies. Thus, this study demonstrates that a data-driven approach using massive sequence data may contribute to a broader understanding of HGT in prokaryotes.
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