Xenorhodopsins, an enigmatic new class of microbial rhodopsins horizontally transferred between archaea and bacteria

Ugalde, Juan A.; Podell, Sheila; Narasingarao, Priya; Allen, Eric E.

doi:10.1186/1745-6150-6-52

Cited by 51 publications

(51 citation statements)

References 21 publications

(45 reference statements)

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“…In nonmarine aquatic environments, 35 to 62% of genomes within metagenomic assemblies harbor a rhodopsin (14), while analysis of freshwater bacterioplankton metagenomic assemblies and single amplified genomes from the same locations suggested the presence of a rhodopsin in 37 to 56% and 8 to 20% of the samples, respectively (35). These studies have demonstrated that rhodopsins are both more abundant and more diverse than previously suspected (10,(36)(37)(38). However, metagenomic and metatranscriptomic data cannot demonstrate that a rhodopsin is functional, nor can they consistently identify the organism that hosts the rhodopsin.…”

mentioning

confidence: 70%

Using Total Internal Reflection Fluorescence Microscopy To Visualize Rhodopsin-Containing Cells

Keffer

Sabanayagam

Lee

et al. 2015

Appl Environ Microbiol

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e Sunlight is captured and converted to chemical energy in illuminated environments. Although (bacterio)chlorophyll-based photosystems have been characterized in detail, retinal-based photosystems, rhodopsins, have only recently been identified as important mediators of light energy capture and conversion. Recent estimates suggest that up to 70% of cells in some environments harbor rhodopsins. However, because rhodopsin autofluorescence is low-comparable to that of carotenoids and significantly less than that of (bacterio)chlorophylls-these estimates are based on metagenomic sequence data, not direct observation. We report here the use of ultrasensitive total internal reflection fluorescence (TIRF) microscopy to distinguish between unpigmented, carotenoid-producing, and rhodopsin-expressing bacteria. Escherichia coli cells were engineered to produce lycopene, ␤-carotene, or retinal. A gene encoding an uncharacterized rhodopsin, actinorhodopsin, was cloned into retinal-producing E. coli. The production of correctly folded and membrane-incorporated actinorhodopsin was confirmed via development of pink color in E. coli and SDS-PAGE. Cells expressing carotenoids or actinorhodopsin were imaged by TIRF microscopy. The 561-nm excitation laser specifically illuminated rhodopsin-containing cells, allowing them to be differentiated from unpigmented and carotenoid-containing cells. Furthermore, water samples collected from the Delaware River were shown by PCR to have rhodopsin-containing organisms and were examined by TIRF microscopy. Individual microorganisms that fluoresced under illumination from the 561-nm laser were identified. These results verify the sensitivity of the TIRF microscopy method for visualizing and distinguishing between different molecules with low autofluorescence, making it useful for analyzing natural samples.

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mentioning

confidence: 70%

Using Total Internal Reflection Fluorescence Microscopy To Visualize Rhodopsin-Containing Cells

Keffer

Sabanayagam

Lee

et al. 2015

Appl Environ Microbiol

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“…In addition, two of LTVLE3's best BLAST hits are to haloviruses. Interestingly, LTVLE3 contains a rhodopsin with high similarity to the nanohaloarchaeal "xenorhodopsins" (75).…”

Section: Resultsmentioning

confidence: 99%

“…The function of the xenorhodopsins is unknown, as they cluster separately from rhodopsins with known functions (i.e., proton pumps, chloride pumps, and sensory rhodopsins), though it has been suggested that they may be sensory rhodopsins, based on conserved amino acid motifs (23,75). As with the other xenorhodopsins, the LTVLE3 rhodopsin contains all of the conserved amino acid motifs predicted to be required for binding the retinal chromophore for light absorption (J. Ugalde, personal communication).…”

Section: Discussionmentioning

confidence: 99%

“…Interestingly, LTVLE3 contains a rhodopsin with high similarity to the nanohaloarchaeal "xenorhodopsins," which cluster with rhodopsins of bacteria from diverse environments and are phylogenetically distinct from bacteriorhodopsins of the class Halobacteria (75). The function of the xenorhodopsins is unknown, as they cluster separately from rhodopsins with known functions (i.e., proton pumps, chloride pumps, and sensory rhodopsins), though it has been suggested that they may be sensory rhodopsins, based on conserved amino acid motifs (23,75).…”

Section: Discussionmentioning

confidence: 99%

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Dynamic Viral Populations in Hypersaline Systems as Revealed by Metagenomic Assembly

Emerson

Thomas

Andrade

et al. 2012

Appl Environ Microbiol

110

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ABSTRACTViruses of theBacteriaandArchaeaplay important roles in microbial evolution and ecology, and yet viral dynamics in natural systems remain poorly understood. Here, we createdde novoassemblies from 6.4 Gbp of metagenomic sequence from eight community viral concentrate samples, collected from 12 h to 3 years apart from hypersaline Lake Tyrrell (LT), Victoria, Australia. Through extensive manual assembly curation, we reconstructed 7 complete and 28 partial novel genomes of viruses and virus-like entities (VLEs, which could be viruses or plasmids). We tracked these 35 populations across the eight samples and found that they are generally stable on the timescale of days and transient on the timescale of years, with some exceptions. Cross-detection of the 35 LT populations in three previously described haloviral metagenomes was limited to a few genes, and most previously sequenced haloviruses were not detected in our samples, though 3 were detected upon reducing our detection threshold from 90% to 75% nucleotide identity. Similar results were obtained when we applied our methods to haloviral metagenomic data previously reported from San Diego, CA: 10 contigs that we assembled from that system exhibited a variety of detection patterns on a timescale of weeks to 1 month but were generally not detected in LT. Our results suggest that most haloviral populations have a limited or, possibly, a temporally variable global distribution. This study provides high-resolution insight into viral biogeography and dynamics and it places “snapshot” viral metagenomes, collected at a single time and location, in context.

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“…The other two, SRI (Bogomolni and Spudich 1982) and SRII (Takahashi et al 1985) are light sensors, being attractant and repellent phototactic receptors, respectively. All rhodopsins share a common architecture, consisting of seven transmembrane a-helices and contain a retinal-binding pocket (Ugalde et al 2011). The retinal chromophore forms a Schiff base with a conserved lysine residue.…”

Section: Cyanobacterial Rhodopsinsmentioning

confidence: 98%

Bioinformatic analysis of the distribution of inorganic carbon transporters and prospective targets for bioengineering to increase Ci uptake by cyanobacteria

et al. 2014

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Cyanobacteria have evolved a carbon-concentrating mechanism (CCM) which has enabled them to inhabit diverse environments encompassing a range of inorganic carbon (Ci: [Formula: see text] and CO2) concentrations. Several uptake systems facilitate inorganic carbon accumulation in the cell, which can in turn be fixed by ribulose 1,5-bisphosphate carboxylase/oxygenase. Here we survey the distribution of genes encoding known Ci uptake systems in cyanobacterial genomes and, using a pfam- and gene context-based approach, identify in the marine (alpha) cyanobacteria a heretofore unrecognized number of putative counterparts to the well-known Ci transporters of beta cyanobacteria. In addition, our analysis shows that there is a huge repertoire of transport systems in cyanobacteria of unknown function, many with homology to characterized Ci transporters. These can be viewed as prospective targets for conversion into ancillary Ci transporters through bioengineering. Increasing intracellular Ci concentration coupled with efforts to increase carbon fixation will be beneficial for the downstream conversion of fixed carbon into value-added products including biofuels. In addition to CCM transporter homologs, we also survey the occurrence of rhodopsin homologs in cyanobacteria, including bacteriorhodopsin, a class of retinal-binding, light-activated proton pumps. Because they are light driven and because of the apparent ease of altering their ion selectivity, we use this as an example of re-purposing an endogenous transporter for the augmentation of Ci uptake by cyanobacteria and potentially chloroplasts.

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Xenorhodopsins, an enigmatic new class of microbial rhodopsins horizontally transferred between archaea and bacteria

Cited by 51 publications

References 21 publications

Using Total Internal Reflection Fluorescence Microscopy To Visualize Rhodopsin-Containing Cells

Using Total Internal Reflection Fluorescence Microscopy To Visualize Rhodopsin-Containing Cells

Dynamic Viral Populations in Hypersaline Systems as Revealed by Metagenomic Assembly

Bioinformatic analysis of the distribution of inorganic carbon transporters and prospective targets for bioengineering to increase Ci uptake by cyanobacteria

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