Widespread distribution of proteorhodopsins in freshwater and brackish ecosystems

Atamna-Ismaeel, Nof; Sabehi, Gazalah; Sharon, Itai; Witzel, Karl-Paul; Labrenz, Matthias; Jürgens, Klaus; Barkay, Tamar; Stomp, Maayke; Huisman, Jef; Béjà, Oded

doi:10.1038/ismej.2008.27

Cited by 102 publications

(99 citation statements)

References 30 publications

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“…The gene encoding the first discovered member of this group was detected in the genome sequence of an uncultured γ-proteobacterium from oceanic waters (5). Since then, PRs have turned out to be highly abundant in the oceans (6)(7)(8)(9), and organisms containing them, including a cyanobacterium (10) can be found in many other habitats as well (7,(11)(12)(13). In vivo experiments have shown that pumping of protons by PR can lead to increases in growth rate under nutrient-limited conditions (6,14,15), production of ATP (16), increased fixation of CO 2 (6,17), and/or survival under starvation or stress conditions (16,(18)(19)(20).…”

Section: Introductionmentioning

confidence: 99%

Expression of holo-proteorhodopsin in Synechocystis sp. PCC 6803

Chen

Steen

Dekker

et al. 2016

Metabolic Engineering

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Retinal-based photosynthesis may contribute to the free energy conversion needed for growth of an organism carrying out oxygenic photosynthesis, like a cyanobacterium. After optimization, this may even enhance the overall efficiency of phototrophic growth of such organisms in sustainability applications. As a first step towards this, we here report on functional expression of the archetype proteorhodopsin in Synechocystis sp. PCC 6803. Upon use of the moderate-strength psbA2 promoter, holo-proteorhodopsin is expressed in this cyanobacterium, at a level of up to 10 5 molecules per cell, presumably in a hexameric quaternary structure, and with approximately equal distribution (on a protein-content basis) over the thylakoid and the cytoplasmic membrane fraction. These results also demonstrate that Synechocystis sp. PCC 6803 has the capacity to synthesize alltrans-retinal. Expressing a substantial amount of a heterologous opsin membrane protein causes a substantial growth retardation Synechocystis, as is clear from a strain expressing PROPS, a nonpumping mutant derivative of proteorhodopsin. Relative to this latter strain, proteorhodopsin expression, however, measurably stimulates its growth.

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Section: Introductionmentioning

confidence: 99%

Expression of holo-proteorhodopsin in Synechocystis sp. PCC 6803

Chen

Steen

Dekker

et al. 2016

Metabolic Engineering

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“…In addition to ActR, proteorhodopsin-encoding gene fragments affiliated with proteobacterial and bacteroidetes sequences (Supplementary Table S2) were also amplified from the Great Lakes Superior and Erie. Several recent studies highlight the broad taxonomic and ecological distribution of microbial rhodopsin genes in diverse aquatic environments (Rusch et al, 2007;Atamna-Ismaeel et al, 2008;Sharma et al, 2008), suggesting they are important in the adaptation of microbes to life on the earth's surface. However, exploratory studies such as ours can only provide insight into sequence diversity, generating fundamental questions regarding rhodopsin function and its impact at both cellular and ecosystem levels.…”

Section: Isolate Mwh-uga1 Encodes An Lg1-actrmentioning

confidence: 99%

Actinorhodopsin genes discovered in diverse freshwater habitats and among cultivated freshwater Actinobacteria

et al. 2009

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Microbial rhodopsins are membrane proteins that utilize a retinal chromophore to harvest sunlight for energetic and photosensory functions. Recently, a group of novel rhodopsin sequences named 'actinorhodopsins' (ActRs) was hypothesized to exist among uncultured planktonic Actinobacteria. ActRs were discovered by mining metagenomic data obtained during the Venter Institute's Global Ocean Sampling expedition, from a hypersaline lagoon, two estuaries and a freshwater lake. On the basis of these findings, and many studies that show Actinobacteria are common inhabitants of lakes, we predicted that ActR genes would likely be present in other freshwater habitats and among the genomes of cultivated Actinobacteria. Using degenerate polymerase chain reaction primers, we discovered an ActR gene present in an actinobacterial isolate of the family Microbacteriaceae. Isolate MWH-Uga1 was cultivated prior to this study from a freshwater pond in Uganda and belongs to a group of Actinobacteria previously identified in freshwater ecosystems. ActR genes were also discovered present in numerous mixed cultures containing freshwater Actinobacteria and among environmental DNA samples obtained from three freshwater sources; a small woodland pond and the Laurentian Great Lakes Superior and Erie. An analysis of small subunit ribosomal RNA genes from metagenomic DNA samples harboring ActR genes suggests that organisms belonging to the acI lineage, an uncultured group of Actinobacteria commonly present in fresh waters, may utilize rhodopsins. The co-occurrence of an acI organism with a specific ActR variant in a mixed culture supports our hypothesis. The ISME Journal (2009) 3, 726-737; doi:10.1038/ismej.2009 published online 26 February 2009 Subject Category: microbial ecology and functional diversity of natural habitats

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“…Degenerated PR primers were modified from Atamna-Ismaeel et al (2008) and Koh et al (2010), with an expected PCR product size of B350 bp. An additional reverse primer (PR-R4) was created after in silico testing with the Fuzznuc web application (http://emboss.bioinformatics.nl/cgi-bin/emboss/ fuzznuc).…”

Section: Pr Primers and Pcr Amplificationmentioning

confidence: 99%

Winter diversity and expression of proteorhodopsin genes in a polar ocean

et al. 2015

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Mixotrophy is a valuable functional trait used by microbes when environmental conditions vary broadly or resources are limited. In the sunlit waters of the ocean, photoheterotrophy, a form of mixotrophy, is often mediated by proteorhodopsin (PR), a seven helices transmembrane protein binding the retinal chromophore. Altogether, they allow bacteria to capture photic energy for sensory and proton gradient formation cell functions. The seasonal occurrence and diversity of the gene coding for PR in cold oligotrophic polar oceans is not known and PR expression has not yet been reported. Here we show that PR is widely distributed among bacterial taxa, and that PR expression decreased markedly during the winter months in the Arctic Ocean. Gammaproteobacteria-like PR sequences were always dominant. However, within the second most common affiliation, there was a transition from Flavobacteria-like PR in early winter to Alphaproteobacteria-like PR in late winter. The phylogenetic shifts followed carbon dynamics, where patterns in expression were consistent with community succession, as identified by DNA community fingerprinting. Although genes for PR were always present, the trend in decreasing transcripts from January to February suggested reduced functional utility of PR during winter. Under winter darkness, sustained expression suggests that PR may continue to be useful for non-ATP forming functions, such as environmental sensing or small solute transport. The persistence of PR expression in winter among some bacterial groups may offer a competitive advantage, where its multifunctionality enhances microbial survival under harsh polar conditions.

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Widespread distribution of proteorhodopsins in freshwater and brackish ecosystems

Cited by 102 publications

References 30 publications

Expression of holo-proteorhodopsin in Synechocystis sp. PCC 6803

Expression of holo-proteorhodopsin in Synechocystis sp. PCC 6803

Actinorhodopsin genes discovered in diverse freshwater habitats and among cultivated freshwater Actinobacteria

Winter diversity and expression of proteorhodopsin genes in a polar ocean

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