Diurnal expression of SAR11 proteorhodopsin and 16S rRNA genes in coastal North Atlantic waters

Lami, Raphaël; Kirchman, David L.

doi:10.3354/ame01716

Cited by 11 publications

(10 citation statements)

References 44 publications

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“…Rhodopsin-associated genes were also significantly reduced under these nutrient-deplete conditions, including carotenoid biosynthesis and β-carotene monooxygenase genes, which encode the final step in retinal synthesis (Table 1). These results show that rhodopsin is not simply constitutively transcribed in an OM43 clade representative and match recent metatranscriptomic and quantitative PCR studies that show modulation of rhodopsin transcription in situ , particularly on diel time scales (39, 40). While the physiological drivers of these modulations in the environment are not well understood, studies of several marine isolates have shown that organisms may use proteorhodopsin-derived energy to survive periods of starvation (41).…”

Section: Resultssupporting

confidence: 88%

Quantitative Transcriptomics Reveals the Growth- and Nutrient-Dependent Response of a Streamlined Marine Methylotroph to Methanol and Naturally Occurring Dissolved Organic Matter

Gifford

Becker

Sosa

et al. 2016

mBio

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The members of the OM43 clade of Betaproteobacteria are abundant coastal methylotrophs with a range of carbon-utilizing capabilities. However, their underlying transcriptional and metabolic responses to shifting conditions or different carbon substrates remain poorly understood. We examined the transcriptional dynamics of OM43 isolate NB0046 subjected to various inorganic nutrient, vitamin, and carbon substrate regimes over different growth phases to (i) develop a quantitative model of its mRNA content; (ii) identify transcriptional markers of physiological activity, nutritional state, and carbon and energy utilization; and (iii) identify pathways involved in methanol or naturally occurring dissolved organic matter (DOM) metabolism. Quantitative transcriptomics, achieved through addition of internal RNA standards, allowed for analyses on a transcripts-per-cell scale. This streamlined bacterium exhibited substantial shifts in total mRNA content (ranging from 1,800 to 17 transcripts cell−1 in the exponential and deep stationary phases, respectively) and gene-specific transcript abundances (>1,000-fold increases in some cases), depending on the growth phase and nutrient conditions. Carbon metabolism genes exhibited substantial dynamics, including those for ribulose monophosphate, tricarboxylic acid (TCA), and proteorhodopsin, as well as methanol dehydrogenase (xoxF), which, while always the most abundant transcript, increased from 5 to 120 transcripts cell−1 when cultures were nutrient and vitamin amended. In the DOM treatment, upregulation of TCA cycle, methylcitrate cycle, vitamin, and organic phosphorus genes suggested a metabolic route for this complex mixture of carbon substrates. The genome-wide inventory of transcript abundances produced here provides insight into a streamlined marine bacterium’s regulation of carbon metabolism and energy flow, providing benchmarks for evaluating the activity of OM43 populations in situ.

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Section: Resultssupporting

confidence: 88%

Quantitative Transcriptomics Reveals the Growth- and Nutrient-Dependent Response of a Streamlined Marine Methylotroph to Methanol and Naturally Occurring Dissolved Organic Matter

Gifford

Becker

Sosa

et al. 2016

mBio

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“…Similarly, in Delaware coastal waters an elevated abundance of PR genes belonging to SAR11 clade bacteria and Flavobacteriia was observed during daylight hours (112). A follow-up study in the same waters confirmed that SAR11 PR gene expression is higher (ϳ2.5-fold) during the day at different seasons (113). Using metatranscriptomic analysis on samples collected in southeast U.S. coastal waters, it was recorded that, in general, PR genes are abundantly expressed by a multitude of taxa (114).…”

Section: Environmental Rhodopsin Gene Expression Analysessupporting

confidence: 51%

Marine Bacterial and Archaeal Ion-Pumping Rhodopsins: Genetic Diversity, Physiology, and Ecology

Pinhassi

DeLong

Béjà

et al. 2016

Microbiol Mol Biol Rev

175

172

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SUMMARYThe recognition of a new family of rhodopsins in marine planktonic bacteria, proton-pumping proteorhodopsin, expanded the known phylogenetic range, environmental distribution, and sequence diversity of retinylidene photoproteins. At the time of this discovery, microbial ion-pumping rhodopsins were known solely in haloarchaea inhabiting extreme hypersaline environments. Shortly thereafter, proteorhodopsins and other light-activated energy-generating rhodopsins were recognized to be widespread among marine bacteria. The ubiquity of marine rhodopsin photosystems now challenges prior understanding of the nature and contributions of “heterotrophic” bacteria to biogeochemical carbon cycling and energy fluxes. Subsequent investigations have focused on the biophysics and biochemistry of these novel microbial rhodopsins, their distribution across the tree of life, evolutionary trajectories, and functional expression in nature. Later discoveries included the identification of proteorhodopsin genes in all three domains of life, the spectral tuning of rhodopsin variants to wavelengths prevailing in the sea, variable light-activated ion-pumping specificities among bacterial rhodopsin variants, and the widespread lateral gene transfer of biosynthetic genes for bacterial rhodopsins and their associated photopigments. Heterologous expression experiments with marine rhodopsin genes (and associated retinal chromophore genes) provided early evidence that light energy harvested by rhodopsins could be harnessed to provide biochemical energy. Importantly, some studies with native marine bacteria show that rhodopsin-containing bacteria use light to enhance growth or promote survival during starvation. We infer from the distribution of rhodopsin genes in diverse genomic contexts that different marine bacteria probably use rhodopsins to support light-dependent fitness strategies somewhere between these two extremes.

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“…Quantitative PCR assays in the coastal North Atlantic showed a tight correlation between SAR11 PR expression and photosynthetically active radiation, whereas growth-related gene activity did not (Lami and Kirchman, 2014), suggesting that energy collected from PR may be directed toward other functional responses, besides growth. Altogether, the presence of PR during the Polar darkness seems to involve several mechanisms and more functional complexity than reported from experiments.…”

Section: Seasonal Trends In Pr Presence and Expressionmentioning

confidence: 99%

“…Patterns in PR expression would be expected to vary seasonally and covary as a function of light availability; however, such patterns have rarely been explored. Recently, a study using a quantitative PCR approach on SAR11 populations from North Atlantic waters showed a strong correlation between PR expression and photosynthetically active radiation; however, no obvious growth response was observed (Lami and Kirchman, 2014). In the Arctic ocean, although PR genes have been reported during both lightreplete summer and light-limited winter at a coastal site , detailed longterm seasonal dynamics of PR's presence or expression in Polar oceans have yet to be described.…”

Section: Introductionmentioning

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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Diurnal expression of SAR11 proteorhodopsin and 16S rRNA genes in coastal North Atlantic waters

Cited by 11 publications

References 44 publications

Quantitative Transcriptomics Reveals the Growth- and Nutrient-Dependent Response of a Streamlined Marine Methylotroph to Methanol and Naturally Occurring Dissolved Organic Matter

Quantitative Transcriptomics Reveals the Growth- and Nutrient-Dependent Response of a Streamlined Marine Methylotroph to Methanol and Naturally Occurring Dissolved Organic Matter

Marine Bacterial and Archaeal Ion-Pumping Rhodopsins: Genetic Diversity, Physiology, and Ecology

Winter diversity and expression of proteorhodopsin genes in a polar ocean

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