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Peptidoglycan Recycling in Gram-Positive Bacteria Is Crucial for Survival in Stationary Phase

Marina Borisova, Rosmarie Gaupp, Amanda Duckworth, Alexander Schneider, Désirée Dalügge, Maraike Mühleck, Denise Deubel, Sandra Unsleber, Wenqi Yu, Günther Muth, Markus Bischoff, Friedrich Götz (+1 others)
2016 mBio  
Peptidoglycan recycling is a metabolic process by which Gram-negative bacteria reutilize up to half of their cell wall within one generation during vegetative growth. Whether peptidoglycan recycling also occurs in Gram-positive bacteria has so far remained unclear. We show here that three Gram-positive model organisms, Staphylococcus aureus , Bacillus subtilis , and Streptomyces coelicolor , all recycle the sugar N -acetylmuramic acid (MurNAc) of their peptidoglycan during growth in rich
more » ... They possess MurNAc-6-phosphate (MurNAc-6P) etherase (MurQ in E. coli ) enzymes, which are responsible for the intracellular conversion of MurNAc-6P to N -acetylglucosamine-6-phosphate and d -lactate. By applying mass spectrometry, we observed accumulation of MurNAc-6P in MurNAc-6P etherase deletion mutants but not in either the isogenic parental strains or complemented strains, suggesting that MurQ orthologs are required for the recycling of cell wall-derived MurNAc in these bacteria. Quantification of MurNAc-6P in Δ murQ cells of S. aureus and B. subtilis revealed small amounts during exponential growth phase (0.19 nmol and 0.03 nmol, respectively, per ml of cells at an optical density at 600 nm [OD 600 ] of 1) but large amounts during transition (0.56 nmol and 0.52 nmol) and stationary (0.53 nmol and 1.36 nmol) phases. The addition of MurNAc to Δ murQ cultures greatly increased the levels of intracellular MurNAc-6P in all growth phases. The Δ murQ mutants of S. aureus and B. subtilis showed no growth deficiency in rich medium compared to the growth of the respective parental strains, but intriguingly, they had a severe survival disadvantage in late stationary phase. Thus, although peptidoglycan recycling is apparently not essential for the growth of Gram-positive bacteria, it provides a benefit for long-term survival. IMPORTANCE The peptidoglycan of the bacterial cell wall is turned over steadily during growth. As peptidoglycan fragments were found in large amounts in spent medium of exponentially growing Gram-positive bacteria, their ability to recycle these fragments has been questioned. We conclusively showed recycling of the peptidoglycan component MurNAc in different Gram-positive model organisms and revealed that a MurNAc-6P etherase (MurQ or MurQ ortholog) enzyme is required in this process. We further demonstrated that recycling occurs predominantly during the transition to stationary phase in S. aureus and B. subtilis , explaining why peptidoglycan fragments are found in the medium during exponential growth. We quantified the intracellular accumulation of recycling products in MurNAc-6P etherase gene mutants, revealing that about 5% and 10% of the MurNAc of the cell wall per generation is recycled in S. aureus and B. subtilis , respectively. Importantly, we showed that MurNAc recycling and salvaging does not sustain growth in these bacteria but is used to enhance survival during late stationary phase.
doi:10.1128/mbio.00923-16 pmid:27729505 pmcid:PMC5061867 fatcat:j37qwqvpdvbufdgueugku26q7e

StreptomeDB 2.0—an extended resource of natural products produced by streptomycetes

Dennis Klementz, Kersten Döring, Xavier Lucas, Kiran K. Telukunta, Anika Erxleben, Denise Deubel, Astrid Erber, Irene Santillana, Oliver S. Thomas, Andreas Bechthold, Stefan Günther
2015 Nucleic Acids Research  
Over the last decades, the genus Streptomyces has stirred huge interest in the scientific community as a source of bioactive compounds. The majority of all known antibiotics is isolated from these bacterial strains, as well as a variety of other drugs such as antitumor agents, immunosuppressants and antifungals. To the best of our knowledge, Strep-tomeDB was the first database focusing on compounds produced by streptomycetes. The new version presented herein represents a major step forward: its
more » ... content has been increased to over 4000 compounds and more than 2500 host organisms. In addition, we have extended the background information and included hundreds of new manually curated references to literature. The latest update features a unique scaffold-based navigation system, which enables the exploration of the chemical diversity of StreptomeDB on a structural basis. We have included a phylogenetic tree, based on 16S rRNA sequences, which comprises more than two-thirds of the included host organisms. It enables visualizing the frequency, appearance, and persistence of compounds and scaffolds in an evolutionary context. Additionally, we have included predicted MS-and NMRspectra of thousands of compounds for assignment of experimental data. The database is freely accessible via http://www.pharmaceutical-bioinformatics. org/streptomedb.
doi:10.1093/nar/gkv1319 pmid:26615197 pmcid:PMC4702922 fatcat:u7svsg52wbcutnipkbzzzz6hom

Wide Distribution of Foxicin Biosynthetic Gene Clusters in Streptomyces Strains – An Unusual Secondary Metabolite with Various Properties

Anja Greule, Marija Marolt, Denise Deubel, Iris Peintner, Songya Zhang, Claudia Jessen-Trefzer, Christian De Ford, Sabrina Burschel, Shu-Ming Li, Thorsten Friedrich, Irmgard Merfort, Steffen Lüdeke (+4 others)
2017 Frontiers in Microbiology  
Streptomyces diastatochromogenes Tü6028 is known to produce the polyketide antibiotic polyketomycin. The deletion of the pokOIV oxygenase gene led to a nonpolyketomycin-producing mutant. Instead, novel compounds were produced by the mutant, which have not been detected before in the wild type strain. Four different compounds were identified and named foxicins A-D. Foxicin A was isolated and its structure was elucidated as an unusual nitrogen-containing quinone derivative using various
more » ... pic methods. Through genome mining, the foxicin biosynthetic gene cluster was identified in the draft genome sequence of S. diastatochromogenes. The cluster spans 57 kb and encodes three PKS type I modules, one NRPS module and 41 additional enzymes. A foxBII gene-inactivated mutant of S. diastatochromogenes Tü6028 pokOIV is unable to produce foxicins. Homologous fox biosynthetic gene clusters were found in more than 20 additional Streptomyces strains, overall in about 2.6% of all sequenced Streptomyces genomes. However, the production of foxicin-like compounds in these strains has never been described indicating that the clusters are expressed at a very low level or are silent under fermentation conditions. Foxicin A acts as a siderophore through interacting with ferric ions. Furthermore, it is a weak inhibitor of the Escherichia coli aerobic respiratory chain and shows moderate antibiotic activity. The wide distribution of the cluster and the various properties of the compound indicate a major role of foxicins in Streptomyces strains.
doi:10.3389/fmicb.2017.00221 pmid:28270798 pmcid:PMC5318452 fatcat:yfl6k2fxjvazzaljijecwrptbu

Frequency effects of knowledge of results in learning of a motor task with spatial control demands in visual impairment people

Suzete Chiviacowsky, Denise C. Insaurriaga, Igor De O. Silva, João A. Krüger
1969 Brazilian Journal of Motor Behavior  
aprendizagem de habilidades motoras (Chiviacowsky, 1994; Chiviacowsky & Tani, 1993 , 1997 Godinho, 1992; Salmoni, Schmidt, & Walter, 1984; Winstein & Schmidt, 1990; Wulf & Schmidt, 1989; Wulf, Schmidt & Deubel  ...  informações de CR, conforme estudos realizados com estes últimos (Chiviacowsky & Tani, 1997; Godinho, 1992; Salmoni, Schmidt, & Walter, 1984; Winstein & Schmidt, 1990; Wulf & Schmidt, 1989; Wulf, Schmidt & Deubel  ... 
doi:10.20338/bjmb.v4i1.21 fatcat:ujzf4dwx7ze5hky2wp5drbveri

Neural and Temporal Dynamics Underlying Visual Selection for Action

M. van Elk, H. T. van Schie, S.F.W. Neggers, H. Bekkering
2010 Journal of Neurophysiology  
Andersson F, Etard O, Denise P, Petit L. Early visual evoked potentials are modulated by eye position in humans induced by whole body rotations. BMC Neurosci 5: 35, 2004.  ...  Preparing a finger-lifting response, for instance, was found to facilitate the processing of tactile stimuli presented at the effector of the prepared movement (Juravle and Deubel 2009 ).  ...  addition, it has been shown that manual response preparation is accompanied by attentional shifts as well, resulting in enhanced recognition of targets at intended reaching and grasp-ing locations (Deubel  ... 
doi:10.1152/jn.01079.2009 pmid:20538783 fatcat:6vsltnh2xvfvlhaqop7yrgcliq

Page 101 of Psychological Abstracts Vol. 89, Issue Author Index [page]

Psychological Abstracts  
., 10100 DeLong, Mahlon R DelPorto-Bedoya, Denise, 34929 Delporto-Bedoya, Denise, 36824 Deltenre, P., 35172 Deltenre, Paul, 6726 Deluca, Alexander, 11386 DeLuca, John, 1834, 1838, 18088 DeLuca, Lara, 2449  ...  ., 2722, 36711 Dette, Dorothea E., 22621 Detterman, Douglas K., 26070 Dettling, Andrea C., 32597 Dettling, M., 15235 Dettmar, P., 32249 Detweiler-Bedell, Brian, 10774 Detwiler-Breidenbach, Ann, 21845 Deubel  ... 

Comparison of dengue infection in human mononuclear leukocytes with mosquito C6/36 and mammalian Vero cells using flow cytometry to detect virus antigen

Farid FO von Sydow, Marta A Santiago, Patricia C Neves-Souza, Denise IS Cerqueira, Adriana S Gouvea, Maryrose FH Lavatori, Álvaro L Bertho, Claire F Kubelka
2000 Memórias do Instituto Oswaldo Cruz  
Quantification of viral RNA by hybridization or quantitative RT-PCR (Vordam & Kuno 1997 , Deubel 1997 , Gubler 1998 ) are very sensitive methodologies but still very laborious, time consuming and costly  ... 
doi:10.1590/s0074-02762000000400007 fatcat:p3k2qdgjbjcv3p64uzzmjdzx5q

In vitro enzyme activity and in vivo healing activity of the protein extract from pineapple peel

Denise Alvarenga Rocha, Estela De Rezende Queiroz, Lucimara Nazaré Silva Botelho, Rodrigo Martins Fráguas, Cláudia Mendes dos Santos, Celeste Maria Patto Abreu, Raimundo Vicente de Sousa
2019 Acta Scientiarum : Biological Sciences  
Aichele, Bubel, Deubel, Pohlemann, and Oberringer (2013) studied the effect of bromelain on tissue regeneration at the cellular level through in vitro wound healing assay.  ... 
doi:10.4025/actascibiolsci.v41i1.41466 fatcat:crr25ilz5fftrao24646hth6nu

Page 255 of Psychological Abstracts Vol. 77, Issue Author Index 1-2 [page]

Psychological Abstracts  
Mark A.— See Goldhaber, Gerald M. 22211, 4111 Deubel, Heiner. Sensory and motor aspects of saccade con- trol.  ...  Marital Therapy, 1989, Vol 4(2), 195-204. 17548 de Silva, Padmal— See Channon, Shelley 8139, 31298 DeSilva, Padmal— See Fahy, Thomas A. 17556 de Simone, Roberta— See Maestripieri, Dario 16500 Desio, Denise  ... 

Page 81 of Psychological Abstracts Vol. 85, Issue Author Index [page]

Psychological Abstracts  
-J., 31209 Detre, Thomas, 12133 Detterman, Douglas K.., Dettling, Andrea, 26417 deTurck, Mark A., 32673 Detweiler, Michael F., 18240 Detzner, U., 8230 Deubel, Heiner, 22888, 35916 Deuel, Lois-Lynn Stoyko  ...  ., DeRaad, Agnes, $387" DeRafael, Denise A., 10320 Derakshan, Nazanin, 1245, 17353, 36060 Deransart, C., 16667 Derby, K. Mark, 5387, 34206, 37984 Derby, Susan, 21928 Derbyshire, S. W.  ... 

A metanalysis of the effect of the Müller-Lyer illusion on saccadic eye movements: No general support for a dissociation of perception and oculomotor action

Nicola Bruno, Paul C. Knox, Denise D.J. de Grave
2010 Vision Research  
However, Walker, Deubel, Schneider, and Findlay (1997) demonstrated that this only happens when distractors are relatively close to the target.  ... 
doi:10.1016/j.visres.2010.09.016 pmid:20858510 fatcat:2ie3k4udwjcoxlvlwbmbecmg3i

Voluntary and involuntary contributions to perceptually guided saccadic choices resolved with millisecond precision

Emilio Salinas, Benjamin R Steinberg, Lauren A Sussman, Sophia M Fry, Christopher K Hauser, Denise D Anderson, Terrence R Stanford
2019 eLife  
., 1995; Deubel and Schneider, 1996; Moore and Fallah, 2001; Godijn and Theeuwes, 2003; Moore and Armstrong, 2003; Cavanaugh and Wurtz, 2004; Steinmetz and Moore, 2014; Klapetek et al., 2016) .  ... 
doi:10.7554/elife.46359 pmid:31225794 pmcid:PMC6645714 fatcat:gi6sorhqy5avrceurr2pw6se3u

Idea and realization: Christian Valuch

Ulrich Ansorge, Thomas Ditye, Arnd Florack, Helmut Leder
2015 unpublished
Children's Cognitive Processes and Learning Strategies for Reading Illustrated Biol-ogy Texts: Eye Movement Measurements Yu-Cin Jian Mon-35 Exploring Attentional Mechanisms in Express Saccade Makers Felicity Denise  ...  blinks Mark Wexler, Marianne Duyck, Thérèse Collins 9.10 am A common spatial map for Auditory and Visual Targets revealed by Landmark-induced positional shifts David Aagten-Murphy, Martin Szinte, Heiner Deubel  ... 

Revisión teórica y empírica desde la psicología sobre representaciones sociales del envejecimiento y la vejez en Latinoamérica y España (2009-2013)

María Del Pilar López Gómez
2016 Revista Científica General José María Córdova  
cual es coordinado por la socióloga argentina Liliana Gastrón, una de las pioneras en América Latina en investigar las representaciones sociales de la vejez, el libro cuenta con prólogo de la doctora Denise  ...  que funcionan como "el lazo entre el Estado y la sociedad, el instrumento de concretización de sus objetivos […] ofrecen un marco de acción y eventualmente recursos para la transformación social" (Roth Deubel  ... 
doi:10.21830/19006586.8 fatcat:nvcgvmxcsfaazaxktdktsrpdhe


Beatriz Silva Matos, Luana Ferreira Botelho, Preciliana Barreto de Morais, Rosendo Freitas de Amorim, Amanda Sousa Felix, Breno Igor Medeiros Freitas, Bruna Maria Costa Gomes, Luany de Queiroz da Silva, Antônio Fábio Macedo de Sousa, Clara da Silva Soares
2021 Epistemologia e Metodologia da Pesquisa Interdisciplinar em Ciências Humanas 2  
(DEUBEL, 2002).  ...  FRADE, Ana Cristina Morado Nascimento; NASCIMENTO, Denise Morado; TOMAÉL, Maria Inês; ALVARENGA NETO, Rivadávia Corre Drummond de.  ... 
doi:10.22533/at.ed.52621080311 fatcat:nayofi2bzzddpgxpkq27hctmaa
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