Sulfur Metabolism in Phototrophic Sulfur Bacteria

https://doi.org/10.1016/S0065-2911(08)00002-7Get rights and content

ABSTRACT

Phototrophic sulfur bacteria are characterized by oxidizing various inorganic sulfur compounds for use as electron donors in carbon dioxide fixation during anoxygenic photosynthetic growth. These bacteria are divided into the purple sulfur bacteria (PSB) and the green sulfur bacteria (GSB). They utilize various combinations of sulfide, elemental sulfur, and thiosulfate and sometimes also ferrous iron and hydrogen as electron donors. This review focuses on the dissimilatory and assimilatory metabolism of inorganic sulfur compounds in these bacteria and also briefly discusses these metabolisms in other types of anoxygenic phototrophic bacteria. The biochemistry and genetics of sulfur compound oxidation in PSB and GSB are described in detail. A variety of enzymes catalyzing sulfur oxidation reactions have been isolated from GSB and PSB (especially Allochromatium vinosum, a representative of the Chromatiaceae), and many are well characterized also on a molecular genetic level. Complete genome sequence data are currently available for 10 strains of GSB and for one strain of PSB. We present here a genome-based survey of the distribution and phylogenies of genes involved in oxidation of sulfur compounds in these strains. It is evident from biochemical and genetic analyses that the dissimilatory sulfur metabolism of these organisms is very complex and incompletely understood. This metabolism is modular in the sense that individual steps in the metabolism may be performed by different enzymes in different organisms. Despite the distant evolutionary relationship between GSB and PSB, their photosynthetic nature and their dependency on oxidation of sulfur compounds resulted in similar ecological roles in the sulfur cycle as important anaerobic oxidizers of sulfur compounds.

Section snippets

INTRODUCTION

The most important common property of phototrophic prokaryotes is the possession of tetrapyrrole pigments and a photosynthetic apparatus enabling light-dependent electron transfer and energy conservation processes. Only a few groups, all within the domain of Bacteria, possess these properties. Fundamental physiological differences exist between these groups: (a) the oxygenic phototrophic bacteria (cyanobacteria) that use water as photosynthetic electron donor and thus produce molecular oxygen

ANOXYGENIC PHOTOTROPHIC BACTERIA: PHYSIOLOGY AND TAXONOMY

The major groups of phototrophic bacteria are well-distinguished on the basis of fundamental structural, molecular, ecological, and physiological properties (Table 1). While the oxygenic cyanobacteria represent a separate large phylogenetic lineage not discussed further here, the anoxygenic phototrophic bacteria are found in only five different major phylogenetic lineages: (1) the FAP bacteria (Chloroflexus and relatives), (2) the GSB (comprising the family Chlorobiaceae), (3) the heliobacteria

ANOXYGENIC PHOTOTROPHIC SULFUR BACTERIA: ECOLOGY

The various photosynthetic tetrapyrrole and carotenoid pigments in phototrophic bacteria lead to a distinct coloration of the cells ranging from green, brown, and red to purple. Older reports about colored waters or sediments occurring in various natural environments (Bavendamm, 1924; Engelmann, (1882), Engelmann, (1888); van Niel, 1931; Winogradsky, 1887) can nowadays be explained by massive blooms of anoxygenic phototrophic sulfur bacteria forming in the water column or in aquatic sediments

TRANSFORMATIONS OF SULFUR COMPOUNDS

In the following section the sulfur oxidation capabilities of the various groups of anoxygenic phototrophic bacteria will be briefly described. PSB and GSB preferentially use reduced sulfur compounds as electron donors during photolithoautotrophic growth. Their sulfur-metabolizing capabilities are summarized in Table 2. Sulfur oxidation capabilities in the ABC bacteria, the FAP bacteria, and the heliobacteria are rather limited. Information about the enzymes involved in the bacteria is in most

OXIDATIVE SULFUR METABOLISM: ENZYMES AND GENES

Here, we attempt to describe the enzymes or multienzyme systems involved in sulfur compound oxidation in phototrophic sulfur bacteria and summarize information on their occurrence. On a molecular genetic and biochemical level, sulfur oxidation is best characterized in the PSB Alc. vinosum and in the GSB Cba. tepidum. However, our knowledge of these processes is still rather incomplete. An overview of the currently proposed metabolic network is shown in Fig. 2. This figure is based on a

EVOLUTION OF SULFUR METABOLISM

The dissimilatory oxidation of sulfur compounds as a means to supply phototrophic sulfur bacteria with electrons for thiotrophic growth clearly is a complex metabolism. Nevertheless, increasing biochemical and genetic information reveal that many similarities exist in the enzyme systems that transform sulfur compounds in thiotrophic organisms and that these similarities in many cases clearly are due to lateral gene transfer events. However, it is also apparent that the exact genetic composition

SULFATE ASSIMILATION IN ANOXYGENIC PHOTOTROPHIC BACTERIA

Assimilatory metabolism of sulfate in anoxygenic phototrophic bacteria has not been covered in the reviews by Brune, (1989), Brune, 1995b). We therefore take this opportunity to summarize the currently available information for all groups of these organisms and include not only GSB and PSB but also purple non-sulfur bacteria, FAP bacteria, aerobic anoxygenic bacteria, and one representative of the Heliobacteria.

CONCLUSIONS

The combination of available biochemical information and the survey of genome sequence data presented here allows some general conclusions to be made about the sulfur compound oxidation enzymes in GSB and PSB. Sulfide:quinone oxidoreductase (encoded by sqr) appears to be especially important for the oxidation of sulfide. Flavocytochrome c is less widespread. Sox genes (SoxXABYZ) occur in both GSB and PSB and are responsible for the oxidation of thiosulfate. In many cases, elemental sulfur

ACKNOWLEDGEMENTS

Support by the Deutsche Forschungsgemeinschaft to C.D. is gratefully acknowledged. Birgitt Hüttig provided excellent technical assistance. N.-U.F. gratefully acknowledges support from the Danish Natural Science Research Council (grant 21-04-0463). We thank Hans G. Trüper for the light and electron micrographs presented in Fig. 1.

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