The interplay between iron limitation, light and carbon in the proteorhodopsin-containing Photobacterium angustum S14

Koedooder, Coco; Geersdaële, Rémy Van; Guéneuguès, Audrey; Bouget, François‐Yves; Obernosterer, Ingrid; Blain, Stéphane

doi:10.1093/femsec/fiaa103

Cited by 4 publications

(10 citation statements)

References 65 publications

(79 reference statements)

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“…By stationary phase, iron-containing alcohol dehydrogenase YqhD, bacterioferritin Bfr, ferric iron ABC transporter, S -(hydroxymethyl)glutathione dehydrogenase FrmA, and a glutaredoxin were all more highly expressed under C limitation as well. While previous studies have observed PR expression regulation related to iron limitation ( 19 , 40 ), the iron-replete conditions in this study highlight that photoheterotrophs regulate Fe-containing proteins in response to C and N limitation as well.…”

Section: Resultscontrasting

confidence: 65%

“…The slightly enhanced transcription of PR in the dark under C limitation was reflected in modestly elevated protein abundance during stationary phase, but no light-dark difference in protein abundance was observed during N-limited growth. In contrast, in Photobacterium angustum S14, PR protein expression is clearly regulated by blue light ( 19 ). Prior work has shown that Vibrio campbellii BAA-1116 induces PR transcription with both light and nutrient starvation and Vibrio sp.…”

Section: Resultsmentioning

confidence: 99%

“…The iron storage protein ferritin was more highly expressed in the light during stationary phase in both media. Under the Fe-replete conditions of this experiment, this expression pattern may reflect light-induced ROS stress, as cells sought to better sequester intracellular Fe to avoid the damaging effects of Fenton radical chemistry ( 19 , 33 ). Ferritin expression exhibited a larger light response in the carbon-limited than in the nitrogen-limited stationary phase, perhaps due to curtailed protein production under N limitation.…”

Section: Resultsmentioning

confidence: 99%

“…That V. campbellii CAIM 519 gene expression does not broadly respond to light is distinct from the case for a number of other photoheterotrophs with PR: in V. campbellii BAA-1116, Photobacterium angustum S14, and Dokdonia sp. PRO95, DSW-1 and MED134 PR expression is light responsive ( 19 ), and in MED134, retinal biosynthesis, carbon fixation, glyoxylate shunt, transporters, electron transport chain, and bacterial cryptochrome and DNA photolyase, amounting to 20% of its genome, are all regulated (at least transcriptionally) in response to light availability ( 7 , 8 , 14 – 16 ). In the SAR11 HTCC1062 strain, where PR-driven ATP production can substitute for carbon respiration during energy starvation, 10% of its transcriptome was light responsive ( 2 , 18 ).…”

Section: Resultsmentioning

confidence: 99%

“…In V. campbellii BAA-1116, PR transcription is induced both by light and during stationary phase ( 13 ). PR protein expression was quantified in Photobacterium angustum S14 using a luciferase reporter construct, demonstrating that PR expression is responsive to light in that organism ( 19 ). To date, protein-level PR expression has been quantified only once by proteomics in a wild-type strain ( 20 ), likely due to the structure and membrane localization of proteorhodopsin, which comprises 7 transmembrane alpha-helices with only small extramembranal loops, leaving few portions of the protein readily protease accessible to generate the soluble peptides that are most detectable by liquid chromatography-mass spectrometry (LC-MS).…”

Section: Introductionmentioning

confidence: 99%

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Proteome Expression and Survival Strategies of a Proteorhodopsin-ContainingVibrioStrain under Carbon and Nitrogen Limitation

Gallagher

Waldbauer

2022

mSystems

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Understanding the nutrient stress responses of proteorhodopsin-bearing microbes like Vibrio campbellii yields insights into microbial contributions to nutrient cycling, lifestyles of emerging pathogens in aquatic environments, and protein-level adaptations implemented during times of nutrient limitation. In addition to its broad taxonomic and geographic prevalence, the physiological role of PR is diverse, so we developed a novel proteomics strategy to quantify its expression at the protein level.

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Section: Resultscontrasting

confidence: 65%

Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Proteome Expression and Survival Strategies of a Proteorhodopsin-ContainingVibrioStrain under Carbon and Nitrogen Limitation

Gallagher

Waldbauer

2022

mSystems

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Bacterial Analogs to Cholesterol Affect Dimerization of Proteorhodopsin and Modulates Preferred Dimer Interface

Sefah

Mertz

2021

J. Chem. Theory Comput.

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Hopanoids, the bacterial analogues of sterols, are ubiquitous in bacteria and play a significant role in organismal survival under stressful environments. Unlike sterols, hopanoids have a high degree of variation in the size and chemical nature of the substituent attached to the ring moiety, leading to different effects on the structure and dynamics of biological membranes. While it is understood that hopanoids can indirectly tune membrane physical properties, little is known on the role that hopanoids may play in affecting the organization and behavior of bacterial membrane proteins. In this work we used coarse-grained molecular dynamics simulations to characterize the effects of two hopanoids, diploptene (DPT) and bacteriohopanetetrol (BHT), on the oligomerization of proteorhodopsin (PR) in a model membrane composed of 1-palmitoyl-2-oleoyl-sn-glycero-3-phophoethanolamine (POPE) and 1-palmitoyl-2-oleoyl-sn-3-phosphoglycerol (POPG). PR is a bacterial membrane protein that functions as a light-activated proton pump. We chose PR based on its ability to adopt a distribution of oligomeric states in different membrane environments. Furthermore, the efficiency of proton pumping in PR is intimately linked to its organization into oligomers. Our results reveal that both BHT and DPT indirectly affect dimerization by tuning membrane properties in a fashion that is concentration-dependent. Variation in their interaction with PR in the membrane-embedded and the cytoplasmic regions leads to distinctly different effects on the plasticity of the dimer interface. BHT has the ability to intercalate between monomers in the dimeric interface, whereas DPT shifts dimerization interactions via packing of the interleaflet region of the membrane. Our results show a direct relationship between hopanoid structure and lateral organization of PR, providing a first glimpse at how these bacterial analogues to eukaryotic sterols produce very similar biophysical effects within the cell membrane.

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Seasonal patterns in microbial carbon and iron transporter expression in the Southern Ocean

Debeljak,

Bayer,

Sun

et al. 2023

Microbiome

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Background Heterotrophic microbes in the Southern Ocean are challenged by the double constraint of low concentrations of organic carbon (C) and iron (Fe). These essential elements are tightly coupled in cellular processes; however, the prokaryotic requirements of C and Fe under varying environmental settings remain poorly studied. Here, we used a combination of metatranscriptomics and metaproteomics to identify prokaryotic membrane transporters for organic substrates and Fe in naturally iron-fertilized and high-nutrient, low-chlorophyll waters of the Southern Ocean during spring and late summer. Results Pronounced differences in membrane transporter profiles between seasons were observed at both sites, both at the transcript and protein level. When specific compound classes were considered, the two approaches revealed different patterns. At the transcript level, seasonal patterns were only observed for subsets of genes belonging to each transporter category. At the protein level, membrane transporters of organic compounds were relatively more abundant in spring as compared to summer, while the opposite pattern was observed for Fe transporters. These observations suggest an enhanced requirement for organic C in early spring and for Fe in late summer. Mapping transcripts and proteins to 50 metagenomic-assembled genomes revealed distinct taxon-specific seasonal differences pointing to potentially opportunistic clades, such as Pseudomonadales and Nitrincolaceae, and groups with a more restricted repertoire of expressed transporters, such as Alphaproteobacteria and Flavobacteriaceae. Conclusion The combined investigations of C and Fe membrane transporters suggest seasonal changes in the microbial requirements of these elements under different productivity regimes. The taxon-specific acquisition strategies of different forms of C and Fe illustrate how diverse microbes could shape transcript and protein expression profiles at the community level at different seasons. Our results on the C- and Fe-related metabolic capabilities of microbial taxa provide new insights into their potential role in the cycling of C and Fe under varying nutrient regimes in the Southern Ocean.

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The interplay between iron limitation, light and carbon in the proteorhodopsin-containing Photobacterium angustum S14

Cited by 4 publications

References 65 publications

Proteome Expression and Survival Strategies of a Proteorhodopsin-ContainingVibrioStrain under Carbon and Nitrogen Limitation

Proteome Expression and Survival Strategies of a Proteorhodopsin-ContainingVibrioStrain under Carbon and Nitrogen Limitation

Bacterial Analogs to Cholesterol Affect Dimerization of Proteorhodopsin and Modulates Preferred Dimer Interface

Seasonal patterns in microbial carbon and iron transporter expression in the Southern Ocean

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