DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Oxygen-­dependent regulation of bacterial lipid production

Abstract

Understanding the mechanisms of lipid accumulation in microorganisms is important for several reasons. In addition to providing insight into assembly of biological membranes, lipid accumulation has important applications in the production of renewable fuels and chemicals. The photosynthetic bacterium Rhodobacter sphaeroides is an attractive organism to study lipid accumulation, as it has the somewhat unique ability to increase membrane production at low O₂ tensions. Under these conditions, R. sphaeroides develops invaginations of the cytoplasmic membrane to increase its membrane surface area for housing of the membrane-bound components of its photosynthetic apparatus. Here we use fatty acid levels as a reporter of membrane lipid content. We show that, under low-O₂ and anaerobic conditions, the total fatty acid content per cell increases 3-fold. We also find that the increases in the amount of fatty acid and photosynthetic pigment per cell are correlated as O₂ tensions or light intensity are changed. To ask if lipid and pigment accumulation were genetically separable, we analyzed strains with mutations in known photosynthetic regulatory pathways. While a strain lacking AppA failed to induce photosynthetic pigment-protein complex accumulation, it increased fatty acid content under low O2 conditions. We also found that an intact PrrBA pathway is required formore » low O2-induced fatty acid accumulation. In conclusion, our findings suggest a previously unknown role of R. sphaeroides transcriptional regulators in increasing fatty acid and phospholipid accumulation in response to decreased O₂ tension.« less

Authors:
 [1];  [2];  [1];  [1]
  1. Univ. of Wisconsin, Madison, WI (United States)
  2. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Publication Date:
Research Org.:
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States). Environmental Molecular Sciences Laboratory (EMSL)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1208744
Report Number(s):
PNNL-SA-106866
Journal ID: ISSN 0021-9193; 48544; 48815; KP1704020
Grant/Contract Number:  
AC05-76RL01830; FC02-07ER64494
Resource Type:
Accepted Manuscript
Journal Name:
Journal of Bacteriology
Additional Journal Information:
Journal Volume: 197; Journal Issue: 9; Journal ID: ISSN 0021-9193
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Environmental Molecular Sciences Laboratory

Citation Formats

Lemmer, Kimberly C., Dohnalkova, Alice C., Noguera, Daniel R., and Donohue, Timothy J. Oxygen-­dependent regulation of bacterial lipid production. United States: N. p., 2015. Web. doi:10.1128/JB.02510-14.
Lemmer, Kimberly C., Dohnalkova, Alice C., Noguera, Daniel R., & Donohue, Timothy J. Oxygen-­dependent regulation of bacterial lipid production. United States. https://doi.org/10.1128/JB.02510-14
Lemmer, Kimberly C., Dohnalkova, Alice C., Noguera, Daniel R., and Donohue, Timothy J. Sat . "Oxygen-­dependent regulation of bacterial lipid production". United States. https://doi.org/10.1128/JB.02510-14. https://www.osti.gov/servlets/purl/1208744.
@article{osti_1208744,
title = {Oxygen-­dependent regulation of bacterial lipid production},
author = {Lemmer, Kimberly C. and Dohnalkova, Alice C. and Noguera, Daniel R. and Donohue, Timothy J.},
abstractNote = {Understanding the mechanisms of lipid accumulation in microorganisms is important for several reasons. In addition to providing insight into assembly of biological membranes, lipid accumulation has important applications in the production of renewable fuels and chemicals. The photosynthetic bacterium Rhodobacter sphaeroides is an attractive organism to study lipid accumulation, as it has the somewhat unique ability to increase membrane production at low O₂ tensions. Under these conditions, R. sphaeroides develops invaginations of the cytoplasmic membrane to increase its membrane surface area for housing of the membrane-bound components of its photosynthetic apparatus. Here we use fatty acid levels as a reporter of membrane lipid content. We show that, under low-O₂ and anaerobic conditions, the total fatty acid content per cell increases 3-fold. We also find that the increases in the amount of fatty acid and photosynthetic pigment per cell are correlated as O₂ tensions or light intensity are changed. To ask if lipid and pigment accumulation were genetically separable, we analyzed strains with mutations in known photosynthetic regulatory pathways. While a strain lacking AppA failed to induce photosynthetic pigment-protein complex accumulation, it increased fatty acid content under low O2 conditions. We also found that an intact PrrBA pathway is required for low O2-induced fatty acid accumulation. In conclusion, our findings suggest a previously unknown role of R. sphaeroides transcriptional regulators in increasing fatty acid and phospholipid accumulation in response to decreased O₂ tension.},
doi = {10.1128/JB.02510-14},
journal = {Journal of Bacteriology},
number = 9,
volume = 197,
place = {United States},
year = {2015},
month = {5}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 10 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Biodiesel production from oleaginous microorganisms
journal, January 2009


Fatty acid synthesis in Escherichia coli and its applications towards the production of fatty acid based biofuels
journal, January 2014

  • Janßen, Helge; Steinbüchel, Alexander
  • Biotechnology for Biofuels, Vol. 7, Issue 1
  • DOI: 10.1186/1754-6834-7-7

A Requirement for Sodium in the Growth of Rhodopseudomonas spheroides
journal, June 1960


Lipids from heterotrophic microbes: advances in metabolism research
journal, February 2011


Purification and characterization of an N-acylphosphatidylserine from Rhodopseudomonas sphaeroides
journal, May 1982

  • Donohue, Timothy J.; Cain, Brian D.; Kaplan, Samuel
  • Biochemistry, Vol. 21, Issue 11
  • DOI: 10.1021/bi00540a029

Aerobic and anaerobic regulation in Rhodobacter sphaeroides 2.4.1: the role of the fnrL gene.
journal, November 1995


Control of Photosystem Formation inRhodobacter sphaeroides
journal, June 1998


The architecture and function of the light-harvesting apparatus of purple bacteria: from single molecules to in vivo membranes
journal, August 2006

  • Cogdell, Richard J.; Gall, Andrew; Köhler, Jürgen
  • Quarterly Reviews of Biophysics, Vol. 39, Issue 3
  • DOI: 10.1017/S0033583506004434

Convergence of the Transcriptional Responses to Heat Shock and Singlet Oxygen Stresses
journal, September 2012


Adaptation of intracytoplasmic membranes to altered light intensity in Rhodobacter sphaeroides
journal, September 2012

  • Adams, Peter G.; Hunter, C. Neil
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1817, Issue 9
  • DOI: 10.1016/j.bbabio.2012.05.013

Development of the bacterial photosynthetic apparatus
journal, December 2006


PpsR: a multifaceted regulator of photosynthesis gene expression in purple bacteria: Photosynthesis regulation by PpsR
journal, April 2005


Perspectives of microbial oils for biodiesel production
journal, August 2008

  • Li, Qiang; Du, Wei; Liu, Dehua
  • Applied Microbiology and Biotechnology, Vol. 80, Issue 5, p. 749-756
  • DOI: 10.1007/s00253-008-1625-9

Activation of the cycA P2 promoter for the Rhodobacter sphaeroides cytochrome c2 gene by the photosynthesis response regulator
journal, November 1999


Engineering fatty acid biosynthesis in microalgae for sustainable biodiesel
journal, June 2013

  • Blatti, Jillian L.; Michaud, Jennifer; Burkart, Michael D.
  • Current Opinion in Chemical Biology, Vol. 17, Issue 3
  • DOI: 10.1016/j.cbpa.2013.04.007

Enhancing fatty acid production by the expression of the regulatory transcription factor FadR
journal, November 2012


Rhodopseudomonas sphaeroides membranes: alterations in phospholipid composition in aerobically and phototrophically grown cells.
journal, January 1982


iRsp1095: A genome-scale reconstruction of the Rhodobacter sphaeroides metabolic network
journal, January 2011


Oxygen intervention in the regulation of gene expression: the photosynthetic bacterial paradigm
journal, February 2004

  • Zeilstra-Ryalls, J. H.; Kaplan, S.
  • Cellular and Molecular Life Sciences (CMLS), Vol. 61, Issue 4
  • DOI: 10.1007/s00018-003-3242-1

The Use of Chromatin Immunoprecipitation to Define PpsR Binding Activity in Rhodobacter sphaeroides 2.4.1
journal, August 2008

  • Bruscella, P.; Eraso, J. M.; Roh, J. H.
  • Journal of Bacteriology, Vol. 190, Issue 20
  • DOI: 10.1128/JB.00719-08

Reconstruction of the Core and Extended Regulons of Global Transcription Factors
journal, July 2010


Cell-cycle-specific biosynthesis of the photosynthetic membrane of Rhodopseudomonas sphaeroides Structural implications
journal, October 1984

  • Yen, Grace S. L.; Cain, Brian D.; Kaplan, Samuel
  • Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 777, Issue 1
  • DOI: 10.1016/0005-2736(84)90495-4

Analysis of the fnrL gene and its function in Rhodobacter capsulatus.
journal, January 1997


An overview of lipid metabolism in yeasts and its impact on biotechnological processes
journal, March 2011

  • Beopoulos, Athanasios; Nicaud, Jean-Marc; Gaillardin, Claude
  • Applied Microbiology and Biotechnology, Vol. 90, Issue 4, p. 1193-1206
  • DOI: 10.1007/s00253-011-3212-8

THE USE OF LEAD CITRATE AT HIGH pH AS AN ELECTRON-OPAQUE STAIN IN ELECTRON MICROSCOPY
journal, April 1963


Expression, Purification and Characterisation of Full-length Histidine Protein Kinase RegB from Rhodobacter sphaeroides
journal, July 2002


Photosynthetic and respiratory electron flow in the dual functional membrane of facultative photosynthetic bacteria
journal, August 1978

  • Melandri, A. Baccarini; Zannoni, D.
  • Journal of Bioenergetics and Biomembranes, Vol. 10, Issue 3-4
  • DOI: 10.1007/BF00743056

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


Triacylglycerols in prokaryotic microorganisms
journal, December 2002


Changes in the acyl lipid composition of photosynthetic bacteria grown under photosynthetic and non-photosynthetic conditions
journal, August 1979

  • Russell, Nicholas J.; Harwood, John L.
  • Biochemical Journal, Vol. 181, Issue 2
  • DOI: 10.1042/bj1810339

Construction, characterization, and complementation of a Puf- mutant of Rhodobacter sphaeroides.
journal, January 1988


Phospholipid Synthesis by Rhodopseudomonas spheroides in Relation to the Formation of Photosynthetic Pigments
journal, January 1965


Revised Sequence and Annotation of the Rhodobacter sphaeroides 2.4.1 Genome
journal, December 2012

  • Kontur, W. S.; Schackwitz, W. S.; Ivanova, N.
  • Journal of Bacteriology, Vol. 194, Issue 24
  • DOI: 10.1128/JB.01214-12

Advancing oleaginous microorganisms to produce lipid via metabolic engineering technology
journal, October 2013


Spectroscopic Analysis of Bacteriochlorophylls in Vitro and in vivo
journal, August 1966


Induction of the photosynthetic membranes of Rhodopseudomonas sphaeroides: biochemical and morphological studies.
journal, January 1984


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


Alterations in the phospholipid composition of Rhodopseudomonas sphaeroides and other bacteria induced by Tris
journal, November 1982


Overproduction of fumarate reductase in Escherichia coli induces a novel intracellular lipid-protein organelle.
journal, January 1984


Crystalline arrays of the Escherichia coli sn-glycerol-3-phosphate acyltransferase, an integral membrane protein.
journal, July 1986


Works referencing / citing this record: