Purple aerobic anoxygenic phototrophs (AAPs) are the only organisms known to capture light energy to enhance growth only in the presence of oxygen but do not produce oxygen. The highly adaptive AAPs compose more than 10% of the microbial community in some euphotic upper ocean waters and are potentially major contributors to the fixation of the greenhouse gas CO 2 . We present the complete genomic sequence and feature analysis of the AAP Roseobacter denitrificans, which reveal clues to its physiology. The genome lacks genes that code for known photosynthetic carbon fixation pathways, and most notably missing are genes for the Calvin cycle enzymes ribulose bisphosphate carboxylase (RuBisCO) and phosphoribulokinase. Phylogenetic evidence implies that this absence could be due to a gene loss from a RuBisCO-containing ␣-proteobacterial ancestor. We describe the potential importance of mixotrophic rather than autotrophic CO 2 fixation pathways in these organisms and suggest that these pathways function to fix CO 2 for the formation of cellular components but do not permit autotrophic growth. While some genes that code for the redox-dependent regulation of photosynthetic machinery are present, many light sensors and transcriptional regulatory motifs found in purple photosynthetic bacteria are absent.Among the five major phyla containing phototrophic prokaryotes, the purple proteobacteria are the most metabolically diverse. The anaerobic purple photosynthetic bacteria grow photoautotrophically only at low oxygen levels, while at higher oxygen levels, the photosynthetic apparatus is down-regulated, resulting in chemotrophic growth using organic carbon (3). In contrast, some related marine ␣-proteobacteria produce bacteriochlorophyll (BChl) a only in the presence of oxygen in the dark (39). These aerobic anoxygenic phototrophs (AAPs) (also known as AAnP or APB for aerobic phototrophic bacteria) have long been overlooked in oceanic studies, but recent data indicate that their contribution to the global carbon cycle could be significant (22).Typically, AAPs grow photoheterotrophically by respiration of organic substrates (39), resulting in the release of CO 2 , counter to the traditional "CO 2 sink" of the upper ocean. However, light-stimulated CO 2 uptake has been seen in some AAP species (22, 39), and several members of the Roseobacter clade were shown to oxidize CO to CO 2 (6).The marine AAP species Roseobacter denitrificans grows not only photoheterotrophically in the presence of oxygen and light but also anaerobically in the dark using nitrate or trimethylamine N-oxide as an electron acceptor (39). This adaptability has made R. denitrificans the most studied AAP and a model organism for this group.Our study of the R. denitrificans genome reveals a variety of metabolic options available to make this species successful in a competitive oligotrophic marine environment. We also investigated the complement of transcriptional regulators in R. denitrificans that are thought to be responsible for aerobic regulation of photosyn...

Photosynthesis was established on Earth more than 3 billion years ago. All available evidences suggest that the earliest photosynthetic organisms were anoxygenic and that oxygen-evolving photosynthesis is a more recent development. The reaction center complexes that form the heart of the energy storage process are integral membrane pigment proteins that span the membrane in vectorial fashion to carry out electron transfer. The origin and extent of distribution of these proteins has been perplexing from a phylogenetic point of view mostly because of extreme sequence divergence. A series of integral membrane proteins of known structure and varying degrees of sequence identity have been compared using combinatorial extension-Monte Carlo methods. The proteins include photosynthetic reaction centers from proteobacteria and cyanobacterial photosystems I and II, as well as cytochrome oxidase, bacteriorhodopsin, and cytochrome b. The reaction center complexes show a remarkable conservation of the core structure of 5 transmembrane helices, strongly implying common ancestry, even though the residual sequence identity is less than 10%, whereas the other proteins have structures that are unrelated. A relationship of sequence with structure was derived from the reaction center structures; with characteristic decay length of 1.6 A. Phylogenetic trees derived from the structural alignments give insights into the earliest photosynthetic reaction center, strongly suggesting that it was a homodimeric complex that did not evolve oxygen.

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