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Title: Genes essential for phototrophic growth by a purple alphaproteobacterium

Abstract

Summary Tn‐seq was used to identify genes essential for phototrophic growth by the purple bacterium Rhodopseudomonas palustris . About 167 genes required for anaerobic growth on acetate in light were identified, 35 of which are annotated as photosynthesis genes. The essentiality of many of these genes by analysing the phenotypes of independently generated mutants that had altered pigmentation was verified. Three genes were identified, two possibly involved in biogenesis of the membrane‐bound photosynthetic apparatus and one for phosphatidylcholine biosynthesis, that were not known to be essential for phototrophic growth. Site‐directed mutagenesis was used to show that the NADH:quinone oxidoreductase complex I E was essential for phototrophic growth under strictly anaerobic conditions and appeared to play a role in reverse electron transport to generate NADH. A homologous NADH:quinone oxidoreductase complex I A likely operates in the opposite direction to oxidize NADH. The operation of the two enzymes in opposition would allow R. palustris to maintain redox balance. As a complement to the genetic data, proteomics experiments were carried out in which it was found that 408 proteins were present in significantly higher amounts in cells grown anaerobically in light compared with aerobically. Among these were proteins encoded by subset of the phototrophicmore » growth‐essential genes.« less

Authors:
 [1];  [2];  [3];  [4];  [4];  [2];  [5];  [2]
  1. Key Lab of Applied Mycology, College of Life Sciences Qingdao Agricultural University Qingdao Shandong Province People's Republic of China, Department of Microbiology University of Washington Seattle WA USA
  2. Department of Microbiology University of Washington Seattle WA USA
  3. Department of Biological Sciences University of Arkansas Fayetteville AR USA
  4. Biological Sciences Division Pacific Northwest National Laboratory Richland WA USA
  5. Department of Genome Sciences University of Washington Seattle WA USA
Publication Date:
Sponsoring Org.:
USDOE
OSTI Identifier:
1390349
Resource Type:
Publisher's Accepted Manuscript
Journal Name:
Environmental Microbiology
Additional Journal Information:
Journal Name: Environmental Microbiology Journal Volume: 19 Journal Issue: 9; Journal ID: ISSN 1462-2912
Publisher:
Wiley-Blackwell
Country of Publication:
United Kingdom
Language:
English

Citation Formats

Yang, Jianming, Yin, Liang, Lessner, Faith H., Nakayasu, Ernesto S., Payne, Samuel H., Fixen, Kathryn R., Gallagher, Larry, and Harwood, Caroline S. Genes essential for phototrophic growth by a purple alphaproteobacterium. United Kingdom: N. p., 2017. Web. doi:10.1111/1462-2920.13852.
Yang, Jianming, Yin, Liang, Lessner, Faith H., Nakayasu, Ernesto S., Payne, Samuel H., Fixen, Kathryn R., Gallagher, Larry, & Harwood, Caroline S. Genes essential for phototrophic growth by a purple alphaproteobacterium. United Kingdom. https://doi.org/10.1111/1462-2920.13852
Yang, Jianming, Yin, Liang, Lessner, Faith H., Nakayasu, Ernesto S., Payne, Samuel H., Fixen, Kathryn R., Gallagher, Larry, and Harwood, Caroline S. Mon . "Genes essential for phototrophic growth by a purple alphaproteobacterium". United Kingdom. https://doi.org/10.1111/1462-2920.13852.
@article{osti_1390349,
title = {Genes essential for phototrophic growth by a purple alphaproteobacterium},
author = {Yang, Jianming and Yin, Liang and Lessner, Faith H. and Nakayasu, Ernesto S. and Payne, Samuel H. and Fixen, Kathryn R. and Gallagher, Larry and Harwood, Caroline S.},
abstractNote = {Summary Tn‐seq was used to identify genes essential for phototrophic growth by the purple bacterium Rhodopseudomonas palustris . About 167 genes required for anaerobic growth on acetate in light were identified, 35 of which are annotated as photosynthesis genes. The essentiality of many of these genes by analysing the phenotypes of independently generated mutants that had altered pigmentation was verified. Three genes were identified, two possibly involved in biogenesis of the membrane‐bound photosynthetic apparatus and one for phosphatidylcholine biosynthesis, that were not known to be essential for phototrophic growth. Site‐directed mutagenesis was used to show that the NADH:quinone oxidoreductase complex I E was essential for phototrophic growth under strictly anaerobic conditions and appeared to play a role in reverse electron transport to generate NADH. A homologous NADH:quinone oxidoreductase complex I A likely operates in the opposite direction to oxidize NADH. The operation of the two enzymes in opposition would allow R. palustris to maintain redox balance. As a complement to the genetic data, proteomics experiments were carried out in which it was found that 408 proteins were present in significantly higher amounts in cells grown anaerobically in light compared with aerobically. Among these were proteins encoded by subset of the phototrophic growth‐essential genes.},
doi = {10.1111/1462-2920.13852},
journal = {Environmental Microbiology},
number = 9,
volume = 19,
place = {United Kingdom},
year = {Mon Jul 24 00:00:00 EDT 2017},
month = {Mon Jul 24 00:00:00 EDT 2017}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1111/1462-2920.13852

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Cited by: 15 works
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Works referenced in this record:

The bacterial cytochrome cbb3 oxidases
journal, April 2004

  • Pitcher, Robert S.; Watmough, Nicholas J.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1655
  • DOI: 10.1016/j.bbabio.2003.09.017

Genotypic and Phenotypic Diversity within Species of Purple Nonsulfur Bacteria Isolated from Aquatic Sediments
journal, July 2002


Phenotypic and genetic characterization of cytochrome c2-deficient mutants of Rhodobacter sphaeroides
journal, March 1988

  • Donohue, Timothy J.; McEwan, Alastair G.; Van Doren, Steven
  • Biochemistry, Vol. 27, Issue 6
  • DOI: 10.1021/bi00406a018

Phylogenomic Analysis and Predicted Physiological Role of the Proton-Translocating NADH:Quinone Oxidoreductase (Complex I) Across Bacteria
journal, April 2015

  • Spero, Melanie A.; Aylward, Frank O.; Currie, Cameron R.
  • mBio, Vol. 6, Issue 2
  • DOI: 10.1128/mBio.00389-15

Identification of essential genes of the periodontal pathogen Porphyromonas gingivalis
journal, January 2012

  • Klein, Brian A.; Tenorio, Elizabeth L.; Lazinski, David W.
  • BMC Genomics, Vol. 13, Issue 1
  • DOI: 10.1186/1471-2164-13-578

Integration of energy and electron transfer processes in the photosynthetic membrane of Rhodobacter sphaeroides
journal, October 2014

  • Cartron, Michaël L.; Olsen, John D.; Sener, Melih
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1837, Issue 10
  • DOI: 10.1016/j.bbabio.2014.02.003

Cytochrome cbb3 oxidase and bacterial microaerobic metabolism
journal, August 2002

  • Pitcher, R. S.; Brittain, T.; Watmugh, N. J.
  • Biochemical Society Transactions, Vol. 30, Issue 4
  • DOI: 10.1042/bst0300653

A polymorphism in the oxygen-responsive repressor PpsR2 confers a growth advantage to Rhodopseudomonas palustris under low light
journal, June 2016


Production of Hydrogen Gas from Light and the Inorganic Electron Donor Thiosulfate by Rhodopseudomonas palustris
journal, October 2010

  • Huang, J. J.; Heiniger, E. K.; McKinlay, J. B.
  • Applied and Environmental Microbiology, Vol. 76, Issue 23
  • DOI: 10.1128/AEM.01143-10

Data, information, knowledge and principle: back to metabolism in KEGG
journal, November 2013

  • Kanehisa, Minoru; Goto, Susumu; Sato, Yoko
  • Nucleic Acids Research, Vol. 42, Issue D1
  • DOI: 10.1093/nar/gkt1076

Organization and expression of photosynthesis genes and operons in anoxygenic photosynthetic proteobacteria
journal, September 2008


RegB/RegA, a Highly Conserved Redox-Responding Global Two-Component Regulatory System
journal, June 2004


Multicopy Single-Stranded DNA Directs Intestinal Colonization of Enteric Pathogens
journal, September 2015


Genome-Scale Identification of Resistance Functions in Pseudomonas aeruginosa Using Tn-seq
journal, January 2011


Amplifying DNA with arbitrary oligonucleotide primers.
journal, October 1993


Quantitative proteomic analysis of intracytoplasmic membrane development in Rhodobacter sphaeroides: Proteomics of membrane assembly in Rba. sphaeroides
journal, May 2012


Atomic Force Microscopy Studies of Native Photosynthetic Membranes
journal, May 2009

  • Sturgis, James N.; Tucker, Jaimey D.; Olsen, John D.
  • Biochemistry, Vol. 48, Issue 17
  • DOI: 10.1021/bi900045x

Directed Mutational Analysis of Bacteriochlorophyll a Biosynthesis in Rhodobacter capsulatus
journal, April 1994

  • Bollivar, David W.; Suzuki, Jori Y.; Beatty, J. Thomas
  • Journal of Molecular Biology, Vol. 237, Issue 5
  • DOI: 10.1006/jmbi.1994.1260

Multiple genome sequences reveal adaptations of a phototrophic bacterium to sediment microenvironments
journal, November 2008

  • Oda, Y.; Larimer, F. W.; Chain, P. S. G.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 47
  • DOI: 10.1073/pnas.0809160105

Progress toward a biomimetic leaf: 4,000 h of hydrogen production by coating-stabilized nongrowing photosynthetic Rhodopseudomonas palustris
journal, January 2010

  • Gosse, Jimmy L.; Engel, Brian J.; Hui, Jeremy C. -H.
  • Biotechnology Progress
  • DOI: 10.1002/btpr.406

Isolation and characterization of enhanced fluorescence mutants of Rhodopseudomonas capsulata
journal, May 1983


Localized transposon Tn5 mutagenesis of the photosynthetic gene cluster of Rhodobacter sphaeroides
journal, June 1990


Adaptation to Oxygen: ROLE OF TERMINAL OXIDASES IN PHOTOSYNTHESIS INITIATION IN THE PURPLE PHOTOSYNTHETIC BACTERIUM, RUBRIVIVAX GELATINOSUS
journal, March 2010

  • Hassani, Bahia Khalfaoui; Steunou, Anne-Soisig; Liotenberg, Sylviane
  • Journal of Biological Chemistry, Vol. 285, Issue 26
  • DOI: 10.1074/jbc.M109.086066

The essential gene set of a photosynthetic organism
journal, October 2015

  • Rubin, Benjamin E.; Wetmore, Kelly M.; Price, Morgan N.
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 48
  • DOI: 10.1073/pnas.1519220112

Essential Genome of the Metabolically Versatile Alphaproteobacterium Rhodopseudomonas palustris
journal, December 2015

  • Pechter, Kieran B.; Gallagher, Larry; Pyles, Harley
  • Journal of Bacteriology, Vol. 198, Issue 5
  • DOI: 10.1128/JB.00771-15

On the mechanism of respiratory complex I
journal, July 2014


Controlling the delicate balance of tetrapyrrole biosynthesis
journal, July 2013

  • Yin, Liang; Bauer, Carl E.
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 368, Issue 1622
  • DOI: 10.1098/rstb.2012.0262

Bacterial NADH-quinone oxidoreductases
journal, April 1991

  • Yagi, Takao
  • Journal of Bioenergetics and Biomembranes, Vol. 23, Issue 2
  • DOI: 10.1007/BF00762218

Genetic and physical mapping of the Rhodobacter sphaeroides photosynthetic gene cluster from R-prime pWS2
journal, May 1991


Carotenoids in Photosynthesis
journal, March 1996


Molecular genetics of photosynthetic membrane biosynthesis in Rhodobacter sphaeroides.
journal, January 1988


Investigation of photosynthetic membrane structure using atomic force microscopy
journal, May 2013


Non-growing Rhodopseudomonas palustris Increases the Hydrogen Gas Yield from Acetate by Shifting from the Glyoxylate Shunt to the Tricarboxylic Acid Cycle
journal, December 2013

  • McKinlay, James B.; Oda, Yasuhiro; Rühl, Martin
  • Journal of Biological Chemistry, Vol. 289, Issue 4
  • DOI: 10.1074/jbc.M113.527515

2016 update of the PRIDE database and its related tools
journal, November 2015

  • Vizcaíno, Juan Antonio; Csordas, Attila; del-Toro, Noemi
  • Nucleic Acids Research, Vol. 44, Issue D1
  • DOI: 10.1093/nar/gkv1145

Carbon dioxide fixation as a central redox cofactor recycling mechanism in bacteria
journal, June 2010

  • McKinlay, J. B.; Harwood, C. S.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 26
  • DOI: 10.1073/pnas.1006175107

Regulation of Uptake Hydrogenase and Effects of Hydrogen Utilization on Gene Expression in Rhodopseudomonas palustris
journal, August 2006

  • Rey, F. E.; Oda, Y.; Harwood, C. S.
  • Journal of Bacteriology, Vol. 188, Issue 17
  • DOI: 10.1128/JB.00381-06

Regulation of benzoate-CoA ligase in Rhodopseudomonas palustris
journal, October 1991


Phylogenetic and evolutionary relationships of RubisCO and the RubisCO-like proteins and the functional lessons provided by diverse molecular forms
journal, May 2008

  • Tabita, F. Robert; Hanson, Thomas E.; Satagopan, Sriram
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 363, Issue 1504
  • DOI: 10.1098/rstb.2008.0023

Mini-Tn5 transposon derivatives for insertion mutagenesis, promoter probing, and chromosomal insertion of cloned DNA in gram-negative eubacteria.
journal, November 1990


CbbR, the Master Regulator for Microbial Carbon Dioxide Fixation
journal, August 2015

  • Dangel, Andrew W.; Tabita, F. Robert
  • Journal of Bacteriology, Vol. 197, Issue 22
  • DOI: 10.1128/JB.00442-15

The Photosynthetic Apparatus of Rhodopseudomonas palustris: Structures and Organization
journal, April 2006

  • Scheuring, Simon; Gonçalves, Rui Pedro; Prima, Valérie
  • Journal of Molecular Biology, Vol. 358, Issue 1
  • DOI: 10.1016/j.jmb.2006.01.085

Combining Genome-Scale Experimental and Computational Methods To Identify Essential Genes in Rhodobacter sphaeroides
journal, June 2017


Resources for Genetic and Genomic Analysis of Emerging Pathogen Acinetobacter baumannii
journal, April 2015

  • Gallagher, Larry A.; Ramage, Elizabeth; Weiss, Eli J.
  • Journal of Bacteriology, Vol. 197, Issue 12
  • DOI: 10.1128/JB.00131-15

PucC and LhaA direct efficient assembly of the light-harvesting complexes in Rhodobacter sphaeroides : Photosystem assembly in
journal, November 2015

  • Mothersole, David J.; Jackson, Philip J.; Vasilev, Cvetelin
  • Molecular Microbiology, Vol. 99, Issue 2
  • DOI: 10.1111/mmi.13235

Descriptions of Rhodopseudomonas parapalustris sp. nov., Rhodopseudomonas harwoodiae sp. nov. and Rhodopseudomonas pseudopalustris sp. nov., and emended description of Rhodopseudomonas palustris
journal, October 2011

  • Ramana, V. V.; Chakravarthy, S. K.; Raj, P. S.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 62, Issue Pt 8
  • DOI: 10.1099/ijs.0.026815-0

FixK, a global regulator of microaerobic growth, controls photosynthesis in Rhodopseudomonas palustris
journal, February 2010


Biosynthesis of phosphatidylcholine in bacteria
journal, March 2003


Tn-seq: high-throughput parallel sequencing for fitness and genetic interaction studies in microorganisms
journal, September 2009

  • van Opijnen, Tim; Bodi, Kip L.; Camilli, Andrew
  • Nature Methods, Vol. 6, Issue 10
  • DOI: 10.1038/nmeth.1377

Determination and Comparison of the Baseline Proteomes of the Versatile Microbe Rhodopseudomonas p alustris under Its Major Metabolic States
journal, February 2006

  • VerBerkmoes, Nathan C.; Shah, Manesh B.; Lankford, Patricia K.
  • Journal of Proteome Research, Vol. 5, Issue 2
  • DOI: 10.1021/pr0503230

Complete genome sequence of the metabolically versatile photosynthetic bacterium Rhodopseudomonas palustris
journal, December 2003

  • Larimer, Frank W; Chain, Patrick; Hauser, Loren
  • Nature Biotechnology, Vol. 22, Issue 1, p. 55-61
  • DOI: 10.1038/nbt923

A giant molecular proton pump: structure and mechanism of respiratory complex I
journal, May 2015

  • Sazanov, Leonid A.
  • Nature Reviews Molecular Cell Biology, Vol. 16, Issue 6
  • DOI: 10.1038/nrm3997

EcoCyc: fusing model organism databases with systems biology
journal, November 2012

  • Keseler, Ingrid M.; Mackie, Amanda; Peralta-Gil, Martin
  • Nucleic Acids Research, Vol. 41, Issue D1
  • DOI: 10.1093/nar/gks1027