Insights into heliobacterial photosynthesis and physiology from the genome of Heliobacterium modesticaldum

Abstract

The complete annotated genome sequence of Heliobacterium modesticaldum strain Ice1 provides our first glimpse into the genetic potential of the Heliobacteriaceae, a unique family of anoxygenic phototrophic bacteria. H. modesticaldum str. Ice1 is the first completely sequenced phototrophic representative of the Firmicutes, and heliobacteria are the only phototrophic members of this large bacterial phylum. The H. modesticaldum genome consists of a single 3.1-Mb circular chromosome with no plasmids. Of special interest are genomic features that lend insight to the physiology and ecology of heliobacteria, including the genetic inventory of the photosynthesis gene cluster. Genes involved in transport, photosynthesis, and central intermediary metabolism are described and catalogued. The obligately heterotrophic metabolism of heliobacteria is a key feature of the physiology and evolution of these phototrophs. The conspicuous absence of recognizable genes encoding the enzyme ATP-citrate lyase prevents autotrophic growth via the reverse citric acid cycle in heliobacteria, thus being a distinguishing differential characteristic between heliobacteria and green sulfur bacteria. The identities of electron carriers that enable energy conservation by cyclic light-driven electron transfer remain in question.

Unique Central Carbon Metabolic Pathways and Novel Enzymes in Phototrophic Bacteria Revealed by Integrative Genomics, 13C-based Metabolomics and Fluxomics

“…Our studies showed that the anoxygenic heliobacterium Heliobacterium modesticaldum uses (Re)-citrate synthase ((Re)-CS), an alternative biosynthetic pathway, to produce citrate . Activity of (Si)-CS has not been detected and the gene encoding (Si)-CS has not been annotated in the H. modesticaldum genome (Sattley and Blankenship, 2009;Sattley et al, 2008). As indicated in Fig.…”

Energy metabolism of Heliobacterium modesticaldum during phototrophic and chemotrophic growth

“…Several features characterize the physiological and metabolic aspects of phototrophic heliobacteria [1-5]: (a) They are the only known phototrophs that belong to the gram-positive bacterial phylum Firmicutes , and as is typical of members of this group, which includes species of Bacillus and Clostridium , heliobacteria can form heat resistant endospores; (b) They produce the unique pigment bacteriochlorophyll g (BChl g ); (c) They produce 8 1 -hydroxy-chlorophyll a with a farnesol tail (8 1 -OH-Chl a F ), which serves as the primary electron acceptor from the reaction center (RC) special pair; (d) They contain a type I homodimeric RC bound to the cytoplasmic membrane; (e) They require organic carbon sources for both phototrophic growth and chemotrophic (fermentative) growth; and (f) they are active nitrogen-fixers and also produce hydrogen. Further, Heliobacterium modesticaldum , isolated from hot springs microbial mats and volcanic soils in Iceland [6], is one of only two known anoxygenic phototrophs that can fix nitrogen at temperatures higher than 50°C (the other is Chlorobaculum tepidum ) [7,8].…”

Purification and biochemical characterization of the ATP synthase from Heliobacterium modesticaldum

“…Therefore, the cytoplasmic membrane is the only membrane system found in Heliobacteria [48]. All membrane-bound complexes, including all photosynthetic complexes and a large number of various transporters for transporting essential substrates into the cells, are confined to this cytoplasmic membrane [2, 48]. According to the complete genome sequence analysis of H. modesticaldum [49], a gene cluster was identified for the ATP synthase that contains all eight subunits and it is assumed that the enzyme is present in the cytoplasmic membrane [2, 49].…”

“…Heliobacterium modesticaldum is a thermophilic anoxygenic phototrophic bacterium that grows either photoheterotrophically or chemotrophically in the dark by fermentation but does not grow photoautotrophically due to the lack of several genes encoding key enzymes required for the known autotrophic carbon fixation pathways [1, 2]. Heliobacterium modesticaldum may have played a key role in the evolution of phototrophic bacteria.…”

“…The energy metabolism of H. modesticaldum has been studied to a much lesser extend, and no isolation or biochemical studies have been reported thus far for the H. modesticaldum ATP synthase, which is one of the key enzymes involved in bioenergetic energy conversion. Based on the genomic information of H. modesticaldum , it is known that this organism contains a gene cluster for an F-type ATP synthase in which all eight subunits are encoded in a single conserved operon [2]. However, due to the lack of any biochemical data, the structure, function and regulation of the ATP synthase of H. modesticaldum are still poorly understood.…”