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J Bacteriol. Feb 2007; 189(3): 683–690.
Published online Nov 10, 2006. doi:  10.1128/JB.01390-06
PMCID: PMC1797316

The Complete Genome Sequence of Roseobacter denitrificans Reveals a Mixotrophic Rather than Photosynthetic Metabolism[down-pointing small open triangle]

Abstract

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 CO2. 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 α-proteobacterial ancestor. We describe the potential importance of mixotrophic rather than autotrophic CO2 fixation pathways in these organisms and suggest that these pathways function to fix CO2 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 α-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 CO2, counter to the traditional “CO2 sink” of the upper ocean. However, light-stimulated CO2 uptake has been seen in some AAP species (22, 39), and several members of the Roseobacter clade were shown to oxidize CO to CO2 (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 photosynthesis genes in phototrophic purple bacteria.

MATERIALS AND METHODS

A single colony of Roseobacter denitrificans strain OCh 114 was grown heterotrophically as described previously (8), and total DNA was isolated using proteinase K treatment followed by phenol extraction. The DNA was fragmented by kinetic shearing, and three shotgun libraries were generated: small- and medium-insert libraries in pOTWI3 (using size fractions of 2 to 3 kb and 6 to 8 kb, respectively) and a large-insert fosmid library in pEpiFOS-5 (insert sizes ranging from 28 to 47 kb), which was used as a scaffold. The relative amounts of sequence coverage obtained from the small-, medium-, and large-insert libraries were 8×, 1×, and 1×, respectively. The whole genome sequence was established from 55,081 end sequences (giving 9.6× coverage) derived from these libraries using dye terminator chemistry on ABI 3730xl automated sequencers. The sequence was assembled and finished as described previously (37). Pseudogenes contained one or more mutations that would ablate expression; each inactivating mutation was subsequently checked against the original sequencing data.

Initial annotation data were built using the Annotation Engine at The Institute for Genomic Research (http://www.tigr.org/edutraining/training/annotation_engine.shtml), followed by comprehensive manual inspection and editing of each feature by using Manatee (http://manatee.sourceforge.net/). The circular genome map was created using the program CGView (35).

Phylogenetic comparisons were performed using clustalW and MEGA (http://www.megasoftware.net/). Jannaschia sp. strain CCS1 (http://genome.jgi-psf.org/draft_microbes/jan_c/jan_c.home.html), Roseobacter sp. strain MED193 (http://www.moore.org/), and other draft genomes were analyzed and compared to their current genomes found in NCBI genome databases (http://www.ncbi.nlm.nih.gov/).

RESULTS AND DISCUSSION

Genome properties.

R. denitrificans contains a circular chromosome of 4,133,097 bp and four plasmids, yielding a total of 4,007 predicted genes (Tables (Tables11 and and22 and Fig. Fig.1;1; see Fig. S1 in the supplemental material). ABC-type transport proteins account for roughly 6.5 to 7.0% of all open reading frames, while tripartite ATP-independent periplasmic-type transporters are 10-fold less common. Major metabolic pathways for the tricarboxylic acid (TCA) cycle, amino acid and nucleotide biosynthesis, glycolysis, nitrogen metabolism, etc., fit the described lifestyle of R. denitrificans and are, in fact, quite similar to its well-studied anaerobic photosynthetic relative Rhodobacter sphaeroides. No extensive metabolic losses or gains indicate a change to aerobic phototrophic metabolism in R. denitrificans.

FIG. 1.
Circular representation of the Roseobacter denitrificans OCh 114 chromosome (maps of plasmids pTB1, pTB2, pTB3, and pTB4 are found in Fig. S1 in the supplemental material). The different rings represent (from outer to inner) all genes and insertion elements, ...
TABLE 1.
General features of the Roseobacter denitrificans genome
TABLE 2.
Features of selected gene categories of the Roseobacter denitrificans genome

Nearly half of the genes in the largest plasmid (pTB1) share a high degree of similarity to genes in plasmid pSD25 from Ruegeria sp. isolate PR1b and the Ti plasmid from Agrobacterium tumefaciens strain C58 (16). Agrobacterium in particular is a well-studied plant pathogen known to transfer genetic elements into host genomes via plasmid-encoded integrases (41). The conservation of many DNA integration and transfer proteins, plasmid replication proteins, and inverted repeats imply that R. denitrificans plasmid pTB1 may also promote lateral gene transfer. This possibility is especially interesting considering the propensity of R. denitrificans to associate with higher organisms (39).

Carbon fixation.

R. denitrificans lacks the key Calvin cycle enzymes ribulose bisphosphate carboxylase (RuBisCO), phosphoribulokinase, and other proteins typically encoded by Calvin cycle operons in closely related anaerobic purple bacteria. Two strains closely related to R. denitrificans, Jannaschia sp. strain CCS1 and Roseobacter sp. strain MED193, both encode a putative form-IV RuBisCO-like protein, an enzyme that has not been found to fix CO2 (25). These species also lack genes for phosphoribulokinase and other Calvin cycle-specific enzymes. As R. denitrificans is the first completely sequenced AAP, this is the first confirmation of the lack of these proteins. A full complement of Calvin cycle genes was found in the nonphotosynthetic plant symbiote Bradyrhizobium japonicum strain USDA110 (20), and our analyses also identified homologs in the genome assembly of the phototrophic plant symbiote Bradyrhizobium sp. strain BTAi1.

A phylogenetic tree of all α-proteobacteria with available genomic sequence data was constructed using the 16S small-subunit rRNA sequence (Fig. (Fig.2).2). Parasitic organisms were removed from the tree due to their loss of many metabolic pathways. The presence of RuBisCO across the represented α-proteobacterial lineages suggests that the ancestral species may have contained the enzyme (Fig. (Fig.2).2). Unfortunately, the gene tree for RuBisCO is riddled with lateral gene transfer, which leaves room for much debate (1). RuBisCO is not only missing in all AAPs, it is also missing from species that have a fermentative metabolism such as Gluconobacter oxydans and Zymomonas mobilis. These species and the AAPs are dependent on organic carbon compounds for growth. A combination of competitive RuBisCO inhibition by oxygen and the decreasing need for carbon assimilation could lead to a gene loss in these species. The ubiquity of AAPs worldwide suggests that the Calvin cycle is not an essential metabolic pathway for success in the open ocean.

FIG. 2.
16S ribosomal tree for the α-proteobacterial lineage using genomes available in the NCBI database. The tree was constructed using maximum likelihood methods. RuBisCO-containing taxa are indicated in red text, with putative RuBisCO-containing nodes ...

Because R. denitrificans lacks a RuBisCO gene, the central question is how it might fix CO2. Key genes involved in three anaerobic CO2 fixation pathways, the reductive TCA cycle, the hydroxypropionate pathway, and the reductive acetyl coenzyme pathway (31), are absent from the genome. However, putative genes for pyruvate-orthophosphate dikinase and phosphoenolpyruvate (PEP) carboxylase, two proteins related to plant C4 sequestration, crassulacean acid metabolism, and anaplerotic carbon fixation enzymes, are present in R. denitrificans (loci RD1_1948 and RD1_14248, respectively). In a mechanism first described by Wood et al. (38), PEP carboxylase attaches CO2 to PEP to form oxaloacetate (OAA) (Fig. (Fig.3).3). This two-step reaction can also be performed in a single step by pyruvate carboxylase. In C4 and crassulacean acid metabolism plants, a similar process provides high amounts of CO2 substrate to RuBisCO. In heterotrophic bacteria, this is primarily an anaplerotic reaction that feeds oxaloacetate into the TCA cycle (32). We suggest that this pathway, coupled with photoheterotrophic energy metabolism, is responsible for the observed mixotrophic CO2 assimilation in R. denitrificans and other AAPs (22, 39).

FIG. 3.
Proposed mixotrophic CO2 assimilation pathway in Roseobacter denitrificans. CO2 is taken up from the environment or supplied by the action of CO dehydrogenase. Carbonic anhydrase converts CO2 to HCO3, which is then used by PEP carboxylase and ...

Two key enzymes of the heterotrophic carbon fixation pathway, pyruvate-orthophosphate dikinase and pyruvate carboxylase, form monophyletic clusters distinct from closely related species (see Fig. S2 and S3, respectively, in the supplemental material). Their sequences may have diverged to accommodate a CO2 fixation role larger than purely anaplerotic assimilation. Other carboxylases within R. denitrificans could also have functionally diverged to further catalyze CO2 fixation, and these concerted carboxylase activities could account for the AAP CO2 assimilation seen previously (6, 39).

The global carbon cycle may also be influenced by members of the widespread Roseobacter lineage that were shown to metabolize CO (6). All other aerobic organisms that oxidize CO to CO2 for energy grow autotrophically using the Calvin cycle (21). Although R. denitrificans has not been shown to oxidize CO in culture, it contains the necessary genes (coxG and coxSML) (Table (Table3)3) and likely performs the reaction under proper conditions. Along with phototrophy and denitrification, this further mechanism for energy metabolism, as well as a full complement of genes for the transport and metabolism of inorganic sulfur (sox) and phosphonate (phn) (discussed below), indicates the great metabolic versatility of R. denitrificans and possibly other AAPs.

TABLE 3.
Genes involved in major metabolic pathways in Roseobacter denitrificans

Based on the genome sequence of R. denitrificans, we suggest that they fix CO2 mixotrophically by using a sequestration pathway supplemented with additional CO2 provided by CO oxidation and heterotrophic respiration. Further studies will show whether this metabolic activity is conserved within all AAPs. The diverse array of energy-yielding metabolic pathways in this organism likely helps provide additional energy, in the form of ATP, for the formation of OAA from CO2 and metabolic intermediates.

Metabolic versatility.

The ability of Roseobacter clade members to metabolize sulfur compounds has been well studied (15). Although R. denitrificans has not been studied in the same thorough manner, its genome codes for many of the same conserved sulfur metabolic pathways (Table (Table3).3). Inorganic sulfur oxidation, encoded by the large soxWXYZABCDEF cluster, is a likely source for extra energy production yielding sulfate as environmental output. The presence of dms and dmd genes indicates that dimethyl sulfoxide reduction and the breakdown of the biological by-product dimethyl sulfoniopropionate could be useful for assimilating additional sulfur into cellular material or providing sulfide for oxidation (15).

One of the major limiting growth factors in the open ocean is phosphorous availability (primarily as organic phosphates). R. denitrificans has the ability to process organic phosphates as well as degrade the chemically stable C-P bond-containing phosphonates (Table (Table3).3). While the concentration of natural phosphonates in seawater is likely low, it has been shown to be an important alternative phosphorous source during phosphate starvation (17, 36).

The reduction of oxidized nitrogen compounds is a significant aspect of the lifestyle of R. denitrificans, and it has a large complement of genes to account for this (Table (Table3).3). All nitrogen metabolism genes are located in three gene clusters, the largest of which codes for nitrite, nitrous oxide, and nitric oxide reduction pathways. Because R. denitrificans cannot fix dinitrogen, the presence of nirBD, coding for assimilatory nitrite reductase, shows that R. denitrificans can acquire nitrogen through means other than recycling.

Like the metabolically diverse anaerobic purple photosynthetic bacterium Rhodopseudomonas palustris (24), R. denitrificans dedicates nearly 15% of its genome to the construction of transport proteins (Table (Table2).2). Among these transporters are more than 120 genes coding for peptide and amino acid transporters (many branched chain), more than 110 genes coding for sugar and carbohydrate transporters, and more than 70 cation and iron transporters. The number of iron transport mechanisms, while not as high as that in R. palustris (24), should still be sufficient to supply R. denitrificans with iron. The high number of peptide and sugar transporters suggests that R. denitrificans and perhaps other non-Calvin-cycle AAPs rely on available sources of organic carbon compounds. However, the library of diverse channel proteins should allow R. denitrificans to adapt to the uptake of a variety of available carbon sources.

PGC.

Figure Figure44 shows the photosynthesis gene cluster (PGC) organization in R. denitrificans, spanning between loci RD1_0102 and RD1_0147. The organization of genes within purple bacterial PGCs was proposed to reflect regulatory mechanisms, evolutionary history, and relationships between species (18, 40).

FIG. 4.
Photosynthesis gene cluster arrangement in the purple bacteria Rubrivivax gelatinosus, Roseobacter denitrificans, and Rhodobacter capsulatus. Genes are presented as arrows indicating their direction of transcription. Genes are colored as listed: chlorophyll ...

Igarashi et al. (18) previously described large-scale gene rearrangements in PGCs between the α-proteobacteria Rhodobacter capsulatus and R. sphaeroides and the β-proteobacterium Rubrivivax gelatinosus. The PGC organization in R. denitrificans, although unique, is similar to both PGCs (Fig. (Fig.4).4). The gene arrangement of idi-bchFNBHLM-lhaA-puhA in R. denitrificans matches that seen in R. gelatinosus (18), including the segregation of bchE and bchJ to distant parts of the chromosome. However, the crtEF-bchCXYZ-puf cluster resembles Rhodobacter rather than Rubrivivax organization, including the transposition of crtI and crtA. The central region of the PGC in R. denitrificans also includes the additional BChl/heme biosynthesis genes acsF and puhE (as in R. gelatinosus), hemA, and the gene encoding cytochrome c2, cycA.

The phylogenetic position of R. denitrificans, nested within the Rhodobacteraceae (Fig. (Fig.2),2), invites speculation on the relationship of its PGC to that of R. gelatinosus. Previous work proposed a lateral transfer of the PGC from an R. palustris ancestor into R. gelatinosus (18) due to the high BLAST similarity between PGC proteins in these species. However, the R. denitrificans cluster also shares a large degree of synteny with that of R. gelatinosus (as described above). Given only these few species, these two lines of conflicting evidence might imply a lateral genetic relationship between R. denitrificans, R. palustris, and R. gelatinosus clusters. However, our further analysis of purple bacterial PGCs revealed far more synteny between the Roseobacter cluster and the Rhodopseudomonas/Rubrivivax PGC than that from Rhodobacter species (the presence of acsF and the translocation of bchE and bchJ). It seems likely that evolutionary differentiation in the Rhodobacter species after the divergence of Roseobacter has led to its current PGC organization.

Our investigation of PGCs from all phototrophic α-proteobacteria with sequence data available at the time of submission of this paper revealed numerous gene arrangements with very few exact matches (data not shown). However, the two major superoperons found in Rhodobacter species, bchFNBHLM-lhaA-puh and crtEF-bchCXYZ-puf (4), were not disrupted in any species. A similar PGC operon structure in aerobic and anaerobic species suggests that PGC organization has no clear relationship to aerobic regulation of photosynthesis genes in R. denitrificans.

Regulation of gene transcription.

All phototrophic organisms contain mechanisms to sense environmental changes and appropriately regulate the transcription of genes encoding vital metabolic pathways. In photosynthetic purple bacteria, oxygen and light levels are known to regulate photosynthesis (2, 3). Characterizing these sensory pathways in R. denitrificans and other AAPs is key to understanding their unique pattern of gene regulation.

The primary cellular redox sensors RegA and RegB from R. denitrificans share a high degree of similarity with those in other purple bacteria (27). These proteins have been characterized as key activators of anaerobic photosynthesis gene expression as well as other cellular processes (3).

The global anaerobic activator FnrL in R. denitrificans (RD1_1268) is also quite similar to that studied in Rhodobacter species. FnrL not only is responsible for primary oxygen sensing but is also a DNA-binding transcription factor (33). Consensus recognition motifs for this protein have been identified in the promoter regions of Rhodobacter heme biosynthesis (hem) genes (33). This may regulate BChl levels via the shared biosynthesis pathway with heme. Of all hem promoters thought to be regulated by FnrL, only one of three hemN promoters in R. denitrificans (RD1_1267) contained a clear consensus binding motif.

Although both photosynthetic purple bacteria and AAPs repress photosynthetic apparatus production in high light, AAPs respond much more sensitively (39). One major feature implicated in light sensing in anaerobic purple bacteria is the BLUF (blue-light-using flavin adenine dinucleotide) domain (14), which has been studied in the R. sphaeroides AppA protein (5, 26). While the BLUF domain proteins found in other organisms and R. denitrificans (RD1_1653) are likely light sensors, they bear very little similarity to R. sphaeroides AppA. No genes coding for homologs to other major light-sensing proteins in purple bacteria, bacteriophytochromes (10, 11), photoactive yellow proteins (23), and HvrA/Spb (7) are found in the genome of R. denitrificans. This suggests the presence of a novel sensory mechanism that is responsible for the sensitive light response in R. denitrificans and other AAPs.

In anaerobic purple bacteria, several global transcription factors are involved in oxygen and light regulation. The most studied of these proteins is PpsR (CrtJ in R. capsulatus), a DNA-binding protein that attaches to (usually) two tandem TGTN12ACA motifs upstream from promoters to block RNA polymerase sigma-subunit binding and repress transcription (9, 29). Although R. denitrificans encodes a homolog of PpsR (RD1_0143), aerobic gene repression would be counterproductive to the observed aerobic photosynthetic expression. Interestingly, PpsR in R. gelatinosus and PpsR1 in Bradyrhizobium strain ORS278 have been proposed to activate photosynthesis gene transcription under aerobiosis (19, 34).

The R. denitrificans PGC contains at least 22 putative PpsR-binding sites, compared to 13 in R. sphaeroides, 12 in R. capsulatus, and 9 in R. gelatinosus. This surprisingly large number of PpsR motifs implies that this protein is a transcriptional modulator in this species. It has also been shown that the spacing between tandem PpsR-binding motifs can drastically affect transcriptional regulation (30). In R. denitrificans, only crtE, crtI, and bchG have PpsR-binding motifs that would fit the previously described functional profile, overlapping the −10 or −35 promoter regions with the tandem motifs separated by 6 to 11 bases. The tandem PpsR-binding motifs at the major control sites of bchF and bchC (13, 30) are spaced too far apart and may be too far upstream in R. denitrificans, 39 and 57 bp, respectively, to properly regulate RNA polymerase activity. Many of the PpsR-binding motifs in R. denitrificans are also downstream of the promoter-binding site, which may also decrease their interaction with RNA polymerase (9). Future analyses of PpsR regulation in both aerobic and anaerobic species will clarify the importance of the conservation of the binding motif in the transcriptional regulation of photosynthesis.

The role of the transcriptional regulator PpaA is also unclear. PpaA overexpression in R. sphaeroides has been shown to activate the transcription of photosynthetic proteins only under aerobic conditions (12). This is contrary to the fact that this organism maximally produces these protein products under low oxygen tension. PpsR-binding sites in the R. sphaeroides ppaA promoter region are likely to repress transcription aerobically, negating its activation role. Since ppaA promoter regions in both R. denitrificans and R. sphaeroides contain similar PpsR consensus-binding motifs, ppaA transcription in R. denitrificans is likely to be activated by PpsR in the presence of oxygen.

The complement of sensory and regulatory proteins in R. denitrificans does not give a clear indication of its aerobic lifestyle. The roles of PpsR and PpaA have not been clearly defined (9, 12, 19, 34), and biochemical studies of R. denitrificans and other AAPs are needed to clarify their function. Furthermore, AAP genome sequences may reveal patterns in regulatory proteins that could lead to a better understanding of aerobic phototrophy. Of special interest is the genome of the “crossover” species Rhodocista centenaria, which photosynthesizes anaerobically but still produces pigments aerobically (http://genomes.tgen.org).

Conclusions.

The genome analysis of R. denitrificans, the first AAP sequenced, has opened the door to understanding their physiological capacity to fill a broad niche in the ocean ecosystem. The numerous mechanisms that members of the Roseobacter clade have evolved for chemotrophic and phototrophic energy metabolism may explain their wide dispersal and high abundance in the biosphere, by allowing them to adapt to changing conditions and outcompete organisms with more conventional lifestyles (6, 28). Because of this “jack-of-all-trades” approach, their contribution to the global carbon cycle is likely to be complex. Analyses of additional AAP genomes in combination with biochemical studies should clarify the information that we have presented regarding the role of the transcriptional regulators PpsR and PpaA, the photosynthesis gene cluster, and the details of the CO2 fixation pathway.

Supplementary Material

[Supplemental material]

Acknowledgments

We thank Paul Stothard and Jason Touchman for assistance with the generation of the circular genome and plasmid maps and Carl Bauer, Gerald Edwards, and Shinji Masuda for thoughtful discussion.

This work was supported by the U.S. National Science Foundation Phototrophic Prokaryotes Sequencing Project, grant number 0412824, and a grant to J.T.B. from the Natural Sciences and Engineering Research Council, Canada.

Footnotes

[down-pointing small open triangle]Published ahead of print on 10 November 2006.

Supplemental material for this article may be found at http://jb.asm.org/.

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