Lipogenesis and redox balance in nitrogen-fixing pea bacteroids

J.J. Terpolilli; S.K. Masakapalli; R. Karunakaran; I.U.C. Webb; R. Green; N.J. Watmough; N.J. Kruger; R.G. Ratcliffe; P.S. Poole; I.B. Zhulin

doi:10.1128/JB.00451-16

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Lipogenesis and redox balance in nitrogen-fixing pea bacteroids

Journal article

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Peer reviewed

Lipogenesis and redox balance in nitrogen-fixing pea bacteroids

J.J. Terpolilli, S.K. Masakapalli, R. Karunakaran, I.U.C. Webb, R. Green, N.J. Watmough, N.J. Kruger, R.G. Ratcliffe, P.S. Poole and I.B. Zhulin

Journal of Bacteriology, Vol.198(20), pp.2864-2875

2016

DOI: https://doi.org/10.1128/JB.00451-16

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Abstract

Within legume root nodules, rhizobia differentiate into bacteroids that oxidize host-derived dicarboxylic acids, which is assumed to occur via the tricarboxylic acid (TCA) cycle to generate NAD(P) H for reduction of N-2. Metabolic flux analysis of laboratory- grown Rhizobium leguminosarum showed that the flux from [C-13] succinate was consistent with respiration of an obligate aerobe growing on a TCA cycle intermediate as the sole carbon source. However, the instability of fragile pea bacteroids prevented their steady-state labeling under N-2-fixing conditions. Therefore, comparative metabolomic profiling was used to compare free-living R. leguminosarum with pea bacteroids. While the TCA cycle was shown to be essential for maximal rates of N-2 fixation, levels of pyruvate (5.5-fold reduced), acetyl coenzyme A (acetyl-CoA; 50-fold reduced), free coenzyme A (33-fold reduced), and citrate (4.5-fold reduced) were much lower in bacteroids. Instead of completely oxidizing acetyl-CoA, pea bacteroids channel it into both lipid and the lipid-like polymer poly-beta-hydroxybutyrate (PHB), the latter via a type III PHB synthase that is active only in bacteroids. Lipogenesis may be a fundamental requirement of the redox poise of electron donation to N-2 in all legume nodules. Direct reduction by NAD(P) H of the likely electron donors for nitrogenase, such as ferredoxin, is inconsistent with their redox potentials. Instead, bacteroids must balance the production of NAD(P) H from oxidation of acetyl-CoA in the TCA cycle with its storage in PHB and lipids.

Details

Title: Lipogenesis and redox balance in nitrogen-fixing pea bacteroids
Authors/Creators: J.J. Terpolilli (Author/Creator)
S.K. Masakapalli (Author/Creator)
R. Karunakaran (Author/Creator)
I.U.C. Webb (Author/Creator)
R. Green (Author/Creator)
N.J. Watmough (Author/Creator)
N.J. Kruger (Author/Creator)
R.G. Ratcliffe (Author/Creator)
P.S. Poole (Author/Creator)
I.B. Zhulin (Author/Creator)
Publication Details: Journal of Bacteriology, Vol.198(20), pp.2864-2875
Publisher: American Society for Microbiology
Identifiers: 991005544550907891
Copyright: © 2016, American Society for Microbiology.
Murdoch Affiliation: Centre for Rhizobium Studies
Language: English
Resource Type: Journal article

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Collaboration types: Domestic collaboration; International collaboration
Citation topics: 3 Agriculture, Environment & Ecology; 3.97 Plant Pathology; 3.97.892 Rhizobium-Legume Symbiosis
Web Of Science research areas: Microbiology
ESI research areas: Microbiology