Energy metabolism of Heliobacterium modesticaldum during phototrophic and chemotrophic growth

Kuo-Hsiang Tang,Hai Yue,Robert E Blankenship

doi:10.1186/1471-2180-10-150

Abstract

BackgroundHeliobacterium modesticaldum is a gram-positive nitrogen-fixing phototrophic bacterium that can grow either photoheterotrophically or chemotrophically but not photoautotrophically. Surprisingly, this organism is lacking only one gene for the complete reverse tricarboxylic acid (rTCA) cycle required for autotrophic carbon fixation. Along with the genomic information reported recently, we use multiple experimental approaches in this report to address questions regarding energy metabolic pathways in darkness, CO2 fixation, sugar assimilation and acetate metabolism.ResultsWe present the first experimental evidence that D-ribose, D-fructose and D-glucose can be photoassimilated by H. modesticaldum as sole carbon sources in newly developed defined growth medium. Also, we confirm two non-autotrophic CO2-fixation pathways utilized by H. modesticaldum: reactions catalyzed by pyruvate:ferredoxin oxidoreductase and phosphoenolpyruvate carboxykinase, and report acetate excretion during phototrophic and chemotrophic growth. Further, genes responsible for pyruvate fermentation, which provides reducing power for nitrogen assimilation, carbon metabolism and hydrogen production, are either active or up-regulated during chemotrophic growth. The discovery of ferredoxin-NADP+ oxidoreductase (FNR) activity in cell extracts provides the reducing power required for carbon and nitrogen metabolisms. Moreover, we show that photosynthetic pigments are produced by H. modesticaldum during the chemotrophic growth, and demonstrate that H. modesticaldum performs nitrogen fixation during both phototrophic and chemotrophic growth.ConclusionCollectively, this report represents the first comprehensive studies for energy metabolism in heliobacteria, which have the simplest known photosynthetic machinery among the entire photosynthetic organisms. Additionally, our studies provide new and essential insights, as well as broaden current knowledge, on the energy metabolism of the thermophilic phototrophic bacterium H. modesticaldum during phototrophic and chemotrophic growth.

Highlights

Heliobacterium modesticaldum is a gram-positive nitrogen-fixing phototrophic bacterium that can grow either photoheterotrophically or chemotrophically but not photoautotrophically
Glucose or fructose are reported to support the growth of Heliobacterium gestii but not H. modesticaldum [2], whereas a complete EMP pathway has been annotated in the genome of H. modesticaldum [1]
In the yeast extract (YE) growth medium with 0.4% yeast extract included, significant cell growth can be detected with 40 mM D-glucose or D-fructose supplied, and cell growth is glucose concentration -dependent (Additional file 1: Figure S1)

Summary

Introduction

Heliobacterium modesticaldum is a gram-positive nitrogen-fixing phototrophic bacterium that can grow either photoheterotrophically or chemotrophically but not photoautotrophically. This organism is lacking only one gene for the complete reverse tricarboxylic acid (rTCA) cycle required for autotrophic carbon fixation. Along with the genomic information reported recently, we use multiple experimental approaches in this report to address questions regarding energy metabolic pathways in darkness, CO2 fixation, sugar assimilation and acetate metabolism. Genomic sequence data of H. modesticaldum suggests that several genes required for the known autotrophic. In the absence of known CO2-fixation mechanisms, it is unknown whether alternative pathways may be adapted by H. modesticaldum for CO2 assimilation. We recently identified the non-autotrophic, anaplerotic CO2 assimilation mechanism in the photoheterotrophic α-proteobacterium Roseobacter denitrificans [9]. Whether a similar anaplerotic pathway and/or other pathways are employed for CO2 incorporation in H. modesticaldum has not been verified

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