Giovannoni, S. J. et al. Proteorhodopsin in the ubiquitous marine bacterium SAR11. Nature 438, 82-85

Department of Microbiology.
Nature (Impact Factor: 41.46). 12/2005; 438(7064):82-5. DOI: 10.1038/nature04032
Source: PubMed


Proteorhodopsins are light-dependent proton pumps that are predicted to have an important role in the ecology of the oceans by supplying energy for microbial metabolism. Proteorhodopsin genes were first discovered through the cloning and sequencing of large genomic DNA fragments from seawater. They were later shown to be widely distributed, phylogenetically diverse, and active in the oceans. Proteorhodopsin genes have not been found in cultured bacteria, and on the basis of environmental sequence data, it has not yet been possible to reconstruct the genomes of uncultured bacterial strains that have proteorhodopsin genes. Although the metabolic effect of proteorhodopsins is uncertain, they are thought to function in cells for which the primary mode of metabolism is the heterotrophic assimilation of dissolved organic carbon. Here we report that SAR11 strain HTCC1062 ('Pelagibacter ubique'), the first cultivated member of the extraordinarily abundant SAR11 clade, expresses a proteorhodopsin gene when cultured in autoclaved seawater and in its natural environment, the ocean. The Pelagibacter proteorhodopsin functions as a light-dependent proton pump. The gene is expressed by cells grown in either diurnal light or in darkness, and there is no difference between the growth rates or cell yields of cultures grown in light or darkness.

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    • "PR, together with its membranebound retinal chromophore, mediates light-activated proton pumping for both energy production and sensory function in bacteria. Rhodopsins have been associated with light-enhanced growth and survival for some cultivated strains (Gómez- Consarnau et al., 2007, 2010), but not for others (Giovannoni et al., 2005; Stingl et al., 2007; Riedel and Tomasch, 2010; Riedel et al., 2013). Although PR activity is commonly associated with photoheterotrophy , the gene likely possesses broader functional roles (Furhman et al., 2008) and support for the diversity of PR functions has been reported (Mongodin et al., 2005; Riedel et al., 2013; Bamman et al., 2014; Yoshizawa et al., 2014). "
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    ABSTRACT: 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.The ISME Journal advance online publication, 20 February 2015; doi:10.1038/ismej.2015.1.
    The ISME Journal 02/2015; 9(8). DOI:10.1038/ismej.2015.1 · 9.30 Impact Factor
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    • "Recent observations from culture and environmental studies suggest a potential role of light in the regulation of the isocitrate lyase gene. SAR11 cells as proteorhodopsin-containing organisms (Giovannoni et al., 2005a) could increase the transcription of the isocitrate lyase gene in the light analogously to Dokdonia sp. MED 134 (Palovaara et al., 2014). "
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    ABSTRACT: The tricarboxylic acid (TCA) cycle is a central metabolic pathway that is present in all aerobic organisms and initiates the respiration of organic material. The glyoxylate cycle is a variation of the TCA cycle, where organic material is recycled for subsequent assimilation into cell material instead of being released as carbon dioxide. Despite the importance for the fate of organic matter, the environmental factors that induce the glyoxylate cycle in microbial communities remain poorly understood. In this study we assessed the expression of isocitrate lyase, the enzyme that induces the switch to the glyoxylate cycle, of the ubiquitous SAR11 clade in response to natural iron fertilization in the Southern Ocean. The cell-specific transcriptional regulation of the glyoxylate cycle, as determined by the ratio between copy numbers of isocitrate lyase gene transcripts and isocitrate genes, was consistently lower in iron fertilized than in High Nutrient Low Chlorophyll waters (by 2.4- to 16.5-fold). SAR11 cell-specific isocitrate lyase gene transcription was negatively correlated to chlorophyll a, and bulk bacterial heterotrophic metabolism. We conclude that the glyoxylate cycle is a metabolic strategy for SAR11 that is highly sensitive to the degree of iron and carbon limitation in the marine environment.
    Environmental Microbiology Reports 01/2015; 7(3). DOI:10.1111/1758-2229.12267 · 3.29 Impact Factor
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    • "The genome of strain MWH-Ta8 T represented a strongly streamlined genome sharing an equally small genome size with 'Candidatus Pelagibacter ubique' (Giovannoni et al., 2005b) a member of the marine SAR11 cluster (Alphaproteobacteria). Interestingly, both organisms also share the presence of proteorhodopsin/actinorhodopsin genes (Giovannoni et al., 2005a), but they differ strongly in their ability to grow in artificial media at high substrate concentrations or on the surface of agar plates (Carini et al., 2013). "
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    ABSTRACT: A pure culture of an actinobacterium previously described as ‘Candidatus Rhodoluna lacicola’ strain MWH-Ta8 was established and deposited in two public culture collections. Strain MWH-Ta8T represents a free-living planktonic freshwater bacterium obtained from hypertrophic Meiliang Bay, Lake Taihu, PR China. The strain was characterized by phylogenetic and taxonomic investigations, as well as by determination of its complete genome sequence. Strain MWH-Ta8T is noticeable due to its unusually low values of cell size (0.05 µm3), genome size (1.43 Mbp), and DNA G+C content (51.5 mol%). Phylogenetic analyses based on 16S rRNA gene and RpoB sequences suggested that strain MWH-Ta8T is affiliated with the family Microbacteriaceae with Pontimonas salivibrio being its closest relative among the currently described species within this family. Strain MWH-Ta8T and the type strain of Pontimonas salivibrio shared a 16S rRNA gene sequence similarity of 94.3 %. The cell-wall peptidoglycan of strain MWH-Ta8T was of type B2β (B10), containing 2,4-diaminobutyric acid as the diamino acid. The predominant cellular fatty acids were anteiso-C15 : 0 (36.5 %), iso-C16 : 0 (16.5 %), iso-C15 : 0 (15.6 %) and iso-C14 : 0 (8.9 %), and the major (>10 %) menaquinones were MK-11 and MK-12. The major polar lipids were diphosphatidylglycerol, phosphatidylglycerol and two unknown glycolipids. The combined phylogenetic, phenotypic and chemotaxonomic data clearly suggest that strain MWH-Ta8T represents a novel species of a new genus in the family Microbacteriaceae, for which the name Rhodoluna lacicola gen. nov., sp. nov. is proposed. The type strain of the type species is MWH-Ta8T ( = DSM 23834T = LMG 26932T).
    International Journal of Systematic and Evolutionary Microbiology 07/2014; 64(Pt 9). DOI:10.1099/ijs.0.065292-0 · 2.51 Impact Factor
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