Ornithine lipid is required for optimal steady‐state amounts of <i>c</i>‐type cytochromes in <i>Rhodobacter capsulatus</i>

Aygun‐Sunar, Semra; Mandaci, Sevnur; Koch, Hans-George; Murray, Ian V.J.; Goldfine, Howard; Daldal, Fevzi

doi:10.1111/j.1365-2958.2006.05253.x

Cited by 40 publications

(52 citation statements)

References 54 publications

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“…The second step of ornithine lipid biosynthesis is catalyzed by the protein product of olsA (Fig. S1), which is frequently found downstream of olsB (30,31). Unexpectedly, the amino acid sequence of HTCC7211_00011010 did not cluster with OlsA sequences from characterized enzymes, despite all three having phospholipid/glycerol acyltransferase domain (IPR002123) signatures.…”

Section: Resultsmentioning

confidence: 97%

SAR11 lipid renovation in response to phosphate starvation

Carini

Mooy

Thrash

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

124

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Phytoplankton inhabiting oligotrophic ocean gyres actively reduce their phosphorus demand by replacing polar membrane phospholipids with those lacking phosphorus. Although the synthesis of nonphosphorus lipids is well documented in some heterotrophic bacterial lineages, phosphorus-free lipid synthesis in oligotrophic marine chemoheterotrophs has not been directly demonstrated, implying they are disadvantaged in phosphate-deplete ecosystems, relative to phytoplankton. Here, we show the SAR11 clade chemoheterotroph Pelagibacter sp. str. HTCC7211 renovates membrane lipids when phosphate starved by replacing a portion of its phospholipids with monoglucosyl-and glucuronosyl-diacylglycerols and by synthesizing new ornithine lipids. Lipid profiles of cells grown with excess phosphate consisted entirely of phospholipids. Conversely, up to 40% of the total lipids were converted to nonphosphorus lipids when cells were starved for phosphate, or when growing on methylphosphonate. Cells sequentially limited by phosphate and methylphosphonate transformed >75% of their lipids to phosphorus-free analogs. During phosphate starvation, a four-gene cluster was significantly up-regulated that likely encodes the enzymes responsible for lipid renovation. These genes were found in Pelagibacterales strains isolated from a phosphate-deficient ocean gyre, but not in other strains from coastal environments, suggesting alternate lipid synthesis is a specific adaptation to phosphate scarcity. Similar gene clusters are found in the genomes of other marine α-proteobacteria, implying lipid renovation is a common strategy used by heterotrophic cells to reduce their requirement for phosphorus in oligotrophic habitats.marine phosphorus cycle | lipids | glucuronic acid | cyanobacteria | methylphosphonate M icrobes primarily assimilate phosphorus (P) in its +5 valence state (phosphate; P i ), which comprises ∼3% of total cellular mass as a structural constituent of nucleic acids and phospholipids, and is intimately involved in energy metabolism and some transport functions (via ATP hydrolysis) (1). In oligotrophic ocean gyres, P i concentrations are extremely low (0.2-1.0 nM in the Sargasso Sea; ref.2) and the availability of P i can limit bacterial and primary production (2-5). Microbes inhabiting these low P i environments have evolved numerous strategies to maintain growth and enhance their competitiveness for trace amounts of P i . These mechanisms are commonly induced by P i starvation and include one or more of the following: (i) expression of high affinity P i transporters (6); (ii) reduction of cellular P i quotas (7, 8); (iii) utilization of alternate phosphorus sources (9, 10); and (iv) polyphosphate storage and breakdown (11,12). Such strategies facilitate survival in the face of P i insufficiency.

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Section: Resultsmentioning

confidence: 97%

SAR11 lipid renovation in response to phosphate starvation

Carini

Mooy

Thrash

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

124

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“…1B). The cbb 3 -Cox-negative phenotype of these mutants on Cu-containing media was not complemented with wild-type copies of olsAB (24), senC (25), or dsbA (26), genes known to affect cbb 3 -Cox biogenesis (data not shown), suggesting that the mutation(s) in XJ3 and XJ11 was located elsewhere. The Cu 2ϩ tolerance (up to 1 mM) of XJ3 and XJ11 was comparable to that of SE8 (⌬ccoA) or wild-type R. capsulatus, and thus different from those of previously identified ⌬ccoA suppressor mutants (11) showing enhanced Cu 2ϩ sensitivity.…”

Section: Resultsmentioning

confidence: 99%

Missense Mutations in Cytochrome c Maturation Genes Provide New Insights into Rhodobacter capsulatus cbb ₃ -Type Cytochrome c Oxidase Biogenesis

et al. 2013

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bThe Rhodobacter capsulatus cbb 3 -type cytochrome c oxidase (cbb 3 -Cox) belongs to the heme-copper oxidase superfamily, and its subunits are encoded by the ccoNOQP operon. Biosynthesis of this enzyme is complex and needs dedicated biogenesis genes (ccoGHIS). It also relies on the c-type cytochrome maturation (Ccm) process, which requires the ccmABCDEFGHI genes, because two of the cbb 3 -Cox subunits (CcoO and CcoP) are c-type cytochromes. Recently, we reported that mutants lacking CcoA, a major facilitator superfamily type transporter, produce very small amounts of cbb 3 -Cox unless the growth medium is supplemented with copper. In this work, we isolated "Cu-unresponsive" derivatives of a ccoA deletion strain that exhibited no cbb 3 -Cox activity even upon Cu supplementation. Molecular characterization of these mutants revealed missense mutations in the ccmA or ccmF gene, required for the Ccm process. As expected, Cu-unresponsive mutants lacked the CcoO and CcoP subunits due to Ccm defects, but remarkably, they contained the CcoN subunit of cbb 3 -Cox. Subsequent construction and examination of single ccm knockout mutants demonstrated that membrane insertion and stability of CcoN occurred in the absence of the Ccm process. Moreover, while the ccm knockout mutants were completely incompetent for photosynthesis, the Cu-unresponsive mutants grew photosynthetically at lower rates and produced smaller amounts of cytochromes c 1 and c 2 than did a wild-type strain due to their restricted Ccm capabilities. These findings demonstrate that different levels of Ccm efficiency are required for the production of various c-type cytochromes and reveal for the first time that maturation of the heme-Cu-containing subunit CcoN of R. capsulatus cbb 3 -Cox proceeds independently of that of the c-type cytochromes during the biogenesis of this enzyme.

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“…Our previous studies on c-type cyt biogenesis led us to the identification of the OL biosynthesis genes, olsA and olsB, of R. capsulatus (3) and indicated that the identity of the gene carrying out PA biosynthesis was unclear. The evidence that OlsA Ϫ mutants still produced quasi-normal amounts of PA and glycerophospholipids and the occurrence of at least two additional PlsC homologues on the R. capsulatus genome led us to investigate the gene responsible for the AGPAT activity dedicated to PA biosynthesis.…”

Section: Discussionmentioning

confidence: 99%

“…Initially, olsA was misannotated as plsC138 encoding an AGPAT homologue based on its high degree of similarity to acyl-acyltransferases (http://www.ergo-light.com). Mutants lacking an active olsA (or olsB) were unable to produce OL, but they contained a full complement of membrane glycerophospholipids, including PE, PG, and phosphatidylcholine (PC) (3). Thus, PA production must be carried out by an unknown enzyme distinct from OlsA.…”

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Rhodobacter capsulatus OlsA Is a Bifunctional Enyzme Active in both Ornithine Lipid and Phosphatidic Acid Biosynthesis

et al. 2007

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The Rhodobacter capsulatus genome contains three genes (olsA [plsC138], plsC316, and plsC3498) that are annotated as lysophosphatidic acid (1-acyl-sn-glycerol-3-phosphate) acyltransferase (AGPAT). Of these genes, olsA was previously shown to be an O-acyltransferase in the second step of ornithine lipid biosynthesis, which is important for optimal steady-state levels of c-type cytochromes (S. Aygun-Sunar, S. Mandaci, H.-G. Koch, I. V. J. Murray, H. Goldfine, and F. Daldal. Mol. Microbiol. 61:418-435, 2006). The roles of the remaining plsC316 and plsC3498 genes remained unknown. In this work, these genes were cloned, and chromosomal insertion-deletion mutations inactivating them were obtained to define their function. Characterization of these mutants indicated that, unlike the Escherichia coli plsC, neither plsC316 nor plsC3498 was essential in R. capsulatus. In contrast, no plsC316 olsA double mutant could be isolated, indicating that an intact copy of either olsA or plsC316 was required for R. capsulatus growth under the conditions tested. Compared to OlsA null mutants, PlsC316 null mutants contained ornithine lipid and had no c-type cytochrome-related phenotype. However, they exhibited slight growth impairment and highly altered total fatty acid and phospholipid profiles. Heterologous expression in an E. coli plsC(Ts) mutant of either R. capsulatus plsC316 or olsA gene products supported growth at a nonpermissive temperature, exhibited AGPAT activity in vitro, and restored phosphatidic acid biosynthesis. The more vigorous AGPAT activity displayed by PlsC316 suggested that plsC316 encodes the main AGPAT required for glycerophospholipid synthesis in R. capsulatus, while olsA acts as an alternative AGPAT that is specific for ornithine lipid synthesis. This study therefore revealed for the first time that some OlsA enzymes, like the enzyme of R. capsulatus, are bifunctional and involved in both membrane ornithine lipid and glycerophospholipid biosynthesis.

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Ornithine lipid is required for optimal steady‐state amounts of c‐type cytochromes in Rhodobacter capsulatus

Cited by 40 publications

References 54 publications

SAR11 lipid renovation in response to phosphate starvation

SAR11 lipid renovation in response to phosphate starvation

Missense Mutations in Cytochrome c Maturation Genes Provide New Insights into Rhodobacter capsulatus cbb ₃ -Type Cytochrome c Oxidase Biogenesis

Rhodobacter capsulatus OlsA Is a Bifunctional Enyzme Active in both Ornithine Lipid and Phosphatidic Acid Biosynthesis

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Ornithine lipid is required for optimal steady‐state amounts of c‐type cytochromes in Rhodobacter capsulatus

Cited by 40 publications

References 54 publications

SAR11 lipid renovation in response to phosphate starvation

SAR11 lipid renovation in response to phosphate starvation

Missense Mutations in Cytochrome c Maturation Genes Provide New Insights into Rhodobacter capsulatus cbb 3 -Type Cytochrome c Oxidase Biogenesis

Rhodobacter capsulatus OlsA Is a Bifunctional Enyzme Active in both Ornithine Lipid and Phosphatidic Acid Biosynthesis

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Missense Mutations in Cytochrome c Maturation Genes Provide New Insights into Rhodobacter capsulatus cbb ₃ -Type Cytochrome c Oxidase Biogenesis