Trends in Microbiology
Volume 14, Issue 11, November 2006, Pages 488-496
Journal home page for Trends in Microbiology

Review
Prokaryotic photosynthesis and phototrophy illuminated

https://doi.org/10.1016/j.tim.2006.09.001Get rights and content

Genome sequencing projects are revealing new information about the distribution and evolution of photosynthesis and phototrophy. Although coverage of the five phyla containing photosynthetic prokaryotes (Chlorobi, Chloroflexi, Cyanobacteria, Proteobacteria and Firmicutes) is limited and uneven, genome sequences are (or soon will be) available for >100 strains from these phyla. Present knowledge of photosynthesis is almost exclusively based on data derived from cultivated species but metagenomic studies can reveal new organisms with novel combinations of photosynthetic and phototrophic components that have not yet been described. Metagenomics has already shown how the relatively simple phototrophy based upon rhodopsins has spread laterally throughout Archaea, Bacteria and eukaryotes. In this review, we present examples that reflect recent advances in phototroph biology as a result of insights from genome and metagenome sequencing.

Section snippets

Photosynthesis and phototrophy

Photosynthesis is arguably the most important biological process on Earth, and only two mechanisms for collecting light energy and converting it into chemical energy have been described (Box 1). The first mechanism, which is dependent upon photochemical reaction centers (RCs; see Glossary) that contain (bacterio)-chlorophyll [(B)Chl], is found in five bacterial phyla: Cyanobacteria, Proteobacteria, Chlorobi, Chloroflexi and Firmicutes. All currently described Chlorobi and Cyanobacteria strains

Genome sequencing projects for photosynthetic prokaryotes

Synechocystis sp. PCC6803, a unicellular cyanobacterium, was the third prokaryote and the first photosynthetic organism to have its chromosome completely sequenced [3]. Over the past decade, there has been explosive growth in the genome sequencing of photosynthetic prokaryotes, and the Genomes On-Line Database (http://www.genomesonline.org/) and other sources currently indicate that 55 Cyanobacteria, 12 Chlorobi, nine Chloroflexi, 24 Proteobacteria and two Firmicutes (heliobacteria) are or soon

Cyanobacteria: the oxyphototrophs

Cyanobacteria are such an ancient and remarkably diverse group of Bacteria that even data for 55 organisms provide an extremely limited view of their complexity. There are >475 pure strains in the Pasteur Culture Collection of Cyanobacteria, and yet this collection includes only a small number of the several thousand described species. To illustrate the magnitude of this problem, the smallest genomes for photosynthetic bacteria are ∼1.7 Mb and are found in the marine, unicellular Prochlorococcus

Chlorobi: green sulfur bacteria

In contrast to the extraordinary richness of cyanobacterial diversity, the phylum Chlorobi (comprising the green sulfur bacteria) is a metabolically limited, physiologically well-defined and genetically closely related bacterial group, which shares a common root with the Bacteroidetes. Comparative genomic analyses have enabled the elucidation of their unique BChl and carotenoid biosynthetic pathways. Chlorobi are obligately anaerobic photoautotrophs that (i) oxidize sulfur compounds, H2 or

Chloroflexi: filamentous anoxygenic phototrophs

Because of their diverse metabolic and physiological properties, genomic analyses of diverse strains of Chloroflexi are likely to produce novel insights into the evolution of photosynthesis. The phylum Chloroflexi is one of the earliest diverging lineages of the Bacteria, and it contains several genera of filamentous, gliding bacteria that perform anoxygenic photosynthesis (FAPs) [32]. The phylum contains two orders, the ‘Chloroflexales’ and ‘Herpetosiphonales’. Herpetosiphon aurantiacus, the

Proteobacteria: purple non-sulfur and purple sulfur bacteria

Photosynthesis is a trait that is widespread but not universal among members of the Proteobacteria and is found in morphologically and metabolically diverse species. Genome sequence information has largely confirmed the physiological versatility and corresponding large genome sizes of these organisms. Some of the photosynthetic proteobacteria are well suited for studies of global gene regulation because many members are facultatively phototrophic or photosynthetic under anoxic conditions.

Heliobacteria

Heliobacteria, first described by Gest and Favinger in 1983 [39], are the most recently discovered group of bacteria containing RCs and they remain the most poorly characterized overall. Heliobacteria are members of the phylum Firmicutes and are closely related to clostridia. Like Bacillus or Clostridium sp., heliobacteria produce heat-resistant endospores and, to date, no characterized member of this group is known to grow photoautotrophically. Studies with Heliobacillus mobilis have shown

Bacteriorhodopsin-based phototrophy in halophilic prokaryotes

Comparative analyses of sequenced genomes and metagenomic data from the ocean have shown the great diversity in the structure and function of rhodopsins and have demonstrated how easily lateral gene transfer can occur among unrelated organisms. Bacteriorhodopsin (BR) in the so-called ‘purple membrane’ of halophilic archaea has been studied for three decades and the structure and function of BR is known in great detail [1] (Figure 2). The halophilic archaea grow well in the dark as aerobic

Proteorhodopsin in marine prokaryotes

Other than those in haloarchaea, the first example of a prokaryotic rhodopsin was one found in a marine proteobacterium and, thus, it was named proteorhodopsin (PR) 47, 48. This identification was based on a metagenomics approach in which large fragments of genomic DNA isolated from marine picoplankton were cloned and sequenced. Like BR, PR has been shown by heterologous expression to function as a light-driven, transmembrane proton pump in E. coli [47] and, thus, it could contribute

The ‘cosmopolitan’ rhodopsins versus the ‘refined’ reaction centers

Shotgun sequencing of DNA from the Sargasso Sea illustrated how PRs are widespread in oceanic microorganisms [13]. Although the exact functions of the rhodopsins are often not known, genome sequencing projects of organisms in pure culture have also confirmed that rhodopsins are much more widely distributed among different organismal lineages than first anticipated. For example, rhodopsins of unknown function have been found in the genomes of organisms as diverse as halophilic archaea and

Concluding remarks and future perspectives

Genome sequencing of cultured organisms and metagenome sequencing of DNA from uncultured organisms of photic environments has already greatly accelerated the pace of new discoveries for the Cyanobacteria and Chlorobi. As more genomic sequence data become available for other phototrophic organisms, comparative bioinformatics will certainly catalyze advances in knowledge of the metabolism, gene regulation and physiology of these groups and might answer many outstanding questions about these

Acknowledgements

The authors would like to thank Julia A. Maresca for critical reading of the manuscript and many helpful comments. We also thank Joachim Weber (Texas Tech University) for use of the ATP synthase image in Figure 2 and Jörg Overmann (Ludwig Maximilians Universität, München) for providing Figure 3 parts (a) and (e), and for use of parts (b), (c) and (d). D.A.B. gratefully acknowledges support for genomics studies from the National Science Foundation (MCB-MCB-0519743 and MCB-0523100) and from the

Glossary

Anoxygenic photosynthesis
photosynthesis performed by organisms that do not evolve oxygen; it uses electron donors other than water for carbon dioxide reduction.
Bacteriorhodopsin (BR)
a rhodopsin first identified in haloarchaea; translocates protons to the periplasm after light-induced isomerization of retinal.
Chlorobi
bacterial phylum that includes the green-colored and brown-colored green sulfur bacteria; these bacteria have type 1 reaction centers (containing BChl a and Chl a) and chlorosomes

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