Abstract
SummaryFacultative phototrophs such as Rhodobacter sphaeroides can switch between heterotrophic and photosynthetic growth. This transition is governed by oxygen tension and involves the large‐scale production of bacteriochlorophyll, which shares a biosynthetic pathway with haem up to protoporphyrin IX. Here, the pathways diverge with the insertion of Fe2+ or Mg2+ into protoporphyrin by ferrochelatase or magnesium chelatase, respectively. Tight regulation of this branchpoint is essential, but the mechanisms for switching between respiratory and photosynthetic growth are poorly understood. We show that PufQ governs the haem/bacteriochlorophyll switch; pufQ is found within the oxygen‐regulated pufQBALMX operon encoding the reaction centre–light‐harvesting photosystem complex. A pufQ deletion strain synthesises low levels of bacteriochlorophyll and accumulates the biosynthetic precursor coproporphyrinogen III; a suppressor mutant of this strain harbours a mutation in the hemH gene encoding ferrochelatase, substantially reducing ferrochelatase activity and increasing cellular bacteriochlorophyll levels. FLAG‐immunoprecipitation experiments retrieve a ferrochelatase‐PufQ‐carotenoid complex, proposed to regulate the haem/bacteriochlorophyll branchpoint by directing porphyrin flux toward bacteriochlorophyll production under oxygen‐limiting conditions. The co‐location of pufQ and the photosystem genes in the same operon ensures that switching of tetrapyrrole metabolism toward bacteriochlorophyll is coordinated with the production of reaction centre and light‐harvesting polypeptides.
Highlights
The purple photosynthetic bacterium Rhodobacter (Rba.) sphaeroides is capable of both aerobic chemoheterotrophy and anaerobic phototrophy (Mackenzie et al, 2007)
The reaction centre (RC) is a membrane-intrinsic complex composed of L, M and H subunits that sits within a ring of LH1 and polypeptides with associated bacteriochlorophyll a (BChl a) and carotenoid pigments
The deleted region is indicated in Figure 1A. pufQ mutant cells are orange in colour, as are many others harbouring mutations that abolish BChl biosynthesis
Summary
The purple photosynthetic bacterium Rhodobacter (Rba.) sphaeroides is capable of both aerobic chemoheterotrophy and anaerobic phototrophy (Mackenzie et al, 2007). The assembly of RC-LH1-PufX and LH2 complexes depends on the availability of BChl, which shares a common biosynthetic pathway with haem up to protoporphyrin IX (Proto), at which point the pathway branches with the insertion of either Mg2+ or Fe2+ into the Proto macrocycle Chelation of these metal ions, catalysed by magnesium chelatase (MgCH) and ferrochelatase (FeCH) respectively, commits tetrapyrrole biosynthesis to BChl and haem (Bollivar et al, 1994; Yaronskaya and Grimm, 2006). We conclude that pufQ PSvar strain, the reduced activity of the mutant FeCH serves to increase the availability of Proto to MgCH This allows BChl biosynthesis to proceed at levels sufficient for normal photosystem assembly and thereby rescuing the low BChl pufQ mutant
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