Metabolic flexibility revealed in the genome of the cyst-forming α-1 proteobacterium Rhodospirillum centenum
© Lu et al; licensee BioMed Central Ltd. 2010
Received: 24 February 2010
Accepted: 25 May 2010
Published: 25 May 2010
Rhodospirillum centenum is a photosynthetic non-sulfur purple bacterium that favors growth in an anoxygenic, photosynthetic N2-fixing environment. It is emerging as a genetically amenable model organism for molecular genetic analysis of cyst formation, photosynthesis, phototaxis, and cellular development. Here, we present an analysis of the genome of this bacterium.
R. centenum contains a singular circular chromosome of 4,355,548 base pairs in size harboring 4,105 genes. It has an intact Calvin cycle with two forms of Rubisco, as well as a gene encoding phosphoenolpyruvate carboxylase (PEPC) for mixotrophic CO2 fixation. This dual carbon-fixation system may be required for regulating internal carbon flux to facilitate bacterial nitrogen assimilation. Enzymatic reactions associated with arsenate and mercuric detoxification are rare or unique compared to other purple bacteria. Among numerous newly identified signal transduction proteins, of particular interest is a putative bacteriophytochrome that is phylogenetically distinct from a previously characterized R. centenum phytochrome, Ppr. Genes encoding proteins involved in chemotaxis as well as a sophisticated dual flagellar system have also been mapped.
Remarkable metabolic versatility and a superior capability for photoautotrophic carbon assimilation is evident in R. centenum.
Rhodospirillum centenum (also known as Rhodocista centenaria) is a thermotolerant α-1 proteobacterium that is closely related to species of the Azospirillum genus [1–4]. R. centenum is one of the few known thermotolerant purple bacteria species. It has an optimal growth temperature of 44°C, and is capable of differentiating into metabolically dormant cysts that can survive at temperatures as high as 65°C [1–3, 5]. Consequently, R. centenum can often be cultivated from hot springs such as those found at Yellowstone National Park . R. centenum metabolizes a unique set of carbon sources, but is unable to utilize malate or other C4 dicarboxylic acids . Unlike Rhodobacter capsulatus and other known purple non-sulfur bacteria, R. centenum does not repress photosystem synthesis in the presence of molecular oxygen .
Members of the cyst forming Azospirillum genera have significant agricultural importance. Specifically, the aerobic nitrogen fixing species A. brasilense and A. lipoferum (both closely related to R. centenum) are known to associate with, and stimulate the growth of, numerous grasses and cereals . These bacteria may benefit such plants through their ability to aerobically fix nitrogen . Interestingly, mutations that affect swim cell to swarm cell differentiation [13, 14] and cyst-cell development  also affect plant root colonization. Thus, a better understanding of these cellular differentiation events is clearly warranted. A genome sequence advances the tools available for studies of these processes.
Results and Discussion
General genome characteristics
Average gene length
Number of CDS with a predicted function
Number of CDS similar to proteins of unknown function
Number of CDS without similarities
Number of insertion sequences
Functional categories of Rhodospirillum centenum genes
Gene functional category
No. of genes1
Energy and central intermediary metabolisms
Fatty acid and phospholipid metabolism
Purines, pyrimidines, nucleosides, and nucleotides
Regulatory function and Signal transduction
Protein synthesis and fate
Amino acid synthesis
Cellular processes and Envelope proteins
Unknown function and hypothetical proteins
Detailed metabolic pathway construction for R. centenum was generated from the annotated genome using the Pathway Tools suite of programs [16, 17]. The predicted metabolic networks were further validated and adjusted with information from the literature that contained experimental data from taxonomically related bacteria. Based on the constructed metabolic scheme, 1,295 known enzymatic reactions involved in 263 pathways are predicted. A total of 985 putative metabolic compounds are predicted to exist in the metabolism of R. centenum, which appears to possess many metabolic pathways typical of purple photosynthetic bacteria in the α-proteobacteria class. Despite the existence of multiple nutrient assimilation pathways, no sulfide metabolism was identified, which verifies an earlier observation that R. centenum is incapable of reducing sulfide [18, 19]. Nevertheless, genes required for anaerobic respiration involved in nitrate and fumarate reduction were identified.
Different kinetic properties reported for these various Rubisco forms have led to speculation that each is adapted for use in specific environmental CO2 concentrations, and that possession of multiple Rubisco forms may be advantageous . For instance, Form IC Rubisco has a slightly lower reaction rate (k cat ~2-3.2 s-1) than IAq (k cat ~3.7 s-1), suggesting that they are adapted to medium-to-high and medium-to-low [CO2] environments, respectively . The need for such extreme metabolic flexibility is reflected by the wide range of environments that non-sulfur purple bacteria inhabit. The mechanism of switching between two Rubisco forms and the roles of the dedicated regulatory proteins CbbR1 and CbbR2 are unclear in these bacteria.
Phosphoenolpyruvate carboxylase (PEPC, RC1_2446) and pyruvate orthophosphate dikinase (Pdk, RC1_1667) are present in the R. centenum genome. These enzymes are widespread in plants and bacteria. PEPC and Pdk (with malic enzyme) are thought to be responsible for heterotrophic carbon dioxide assimilation in Roseobacter denitrificans since this bacteria does not contain Rubisco . However, PEPC and Pdk are also found in species that primarily use Rubisco for carbon fixation, such as R. palustris. Thus, the function that PEPC and Pdk perform in R. centenum, as well as in related Rubisco-containing purple bacteria, is unclear. An R. palustris PEPC-deficient strain does exhibit a slower doubling time compared with the wild-type strain grown anaerobically in the light and aerobically in the dark when pyruvate is used as a carbon source . Thus, autotrophic bacteria like R. centenum that cannot acquire C4 dicarboxylic acids heterotrophically may have evolved an anaplerotic assimilation to ensure a continuous replenishment of C4-dicarboxylic acids needed for amino acid biosynthesis.
An analysis of the α-proteobacteria class shows that only four anoxygenic photosynthetic species are known to possess Pk, Pdk, and PEPS (phosphoenolpyruvate synthase) together (Additional File 1, Figure S1). These include two members of the Bradyrhizobium family, Hoeflea phototropica, and R. centenum. The others contain only Pk and Pdk, or just Pdk (e.g., the mutualistic parasites of Rickettsiales). The four containing Pk, Pdk, and PEPS are reported to grow poorly with pyruvate, malate, and various other dicarboxylic acids, indicating a strong dependence on carbon source such as we observe with R. centenum [2, 24, 25].
R. centenum is an active nitrogen fixer. The nif genes of R. centenum are located in two distant regions: the first region consists of 22 genes that essentially include nifIXENKDHTZBAVW for nitrogenase biosynthesis, modBC for molybdenum transport, and fixABCX for electron transport. Phylogenetic analysis using a concatenated alignment of the nitrogenase structural genes nifHDK shows that R. centenum falls within a clade containing R. sphaeroides, R. rubrum and several Rhizobiales (not shown). This result suggests that this group of nitrogenases originated from a common ancestor.
Neither iron nor vanadium nitrogenases, coded by anf and vnfVHDK, respectively, were identified in the R. centenum genome. In R. rubrum the regulatory enzymes dinitrogenase reductase ADP-ribosyl transferase (DRAT) and dinitrogenase reductase-activating glycohydrolase (DRAG) regulate nitrogenase activity by reversible ADP-ribosylation of NifH [28, 29]. An absence of these genes in R. centenum suggests that these organisms have different environmental requirements for nitrogen fixation. While R. centenum possesses a nitrogenase for nitrogen fixation, utilization of inorganic nitrogen compounds as an alternative nitrogen source is restricted. Unlike R. denitrificans, which has a large complement of genes for nitrogen metabolism (but not nitrogenase), the R. centenum genome does not contain genes which encode an assimilatory nitrite reductase (nirSCFDGHJN) for the denitrification pathway. Yet, the nitrate reduction by periplasmic nitrate reductase (napABCDEF) seems to be intact.
We identified the presence of two cytosolic detoxifying enzymes, arsenate and mercuric reductase. To our knowledge, the latter has never been reported in a purple bacterium. Two copies of arsenate reductase, encoded by arsC1 and arsC2, are present (RC1_2995 and RC1_3700). One copy is associated with genes encoding an arsenate efflux pump (arc3) and an arsenic resistance repressor (arsR). In both ArsC proteins, the cysteine residues that presumably bind arsenate are conserved, but the protein sequences share less than 20% overall identity. The presence of arc3 and arsR implies that arsenate reductase is an inducible enzyme when arsenate is present. There is one copy of mercuric reductase encoding merA (RC1_2279). Generally, these two detoxifying systems are energy dependent, with arsenate reductase using either thioredoxin or glutaredoxin while mercuric reductase uses NADPH .
To date, the only concerted effort at finding regulators of encystment (Figure 1B) in any bacterial species has been undertaken in R. centenum, where a screen for Tn5 mutants displaying de-repressed encystment on nutrient-rich media uncovered several such components . A subset of identified elements lay within an operon of chemotaxis-like genes (che3), individual in-frame deletions of which exhibit opposing premature 'hyper-cyst' or delayed 'hypo-cyst' phenotypes . Predicted signaling components of note in this cluster include a small receiver domain protein (CheY3; RC1_2133), a hybrid sensor kinase-receiver CheA homolog (CheA3; RC1_2127) and a similarly hybridized kinase-receiver protein (CstS3; RC1_2124) that also contains a PAS sensory domain. As ultimate control over cyst cell development no doubt occurs at the transcriptional level, the immediate output of this system is unclear, as none of the aforementioned components has an obvious DNA binding domain. Whether or not Che3 signaling ultimately regulates timing of encystment directly, through the phosphorylation of a classic response regulator, or does so by means of a more indirect mechanism remains to be elucidated. This screen also identified two genomically orphaned, cytoplasmic sensor kinases (CstS1, RC1_2847 and CstS2, RC1_2047), both predicted to contain PAS and PAC sensory motifs with CstS1 also containing a GAF and a receiver domain . Deletion of cstS1 and cstS2 have contrasting respective hypo-cyst and hyper-cyst phenotypes, and epistatic analyses of these genes and che 3 components indicate a complex signaling hierarchy into which contributions are undoubtedly made by hitherto unknown regulatory elements (Berleman and Bauer, Unpublished Data). In fact further screens in our lab have uncovered several such regulators, including two sensor kinases, RC1_0896 and RC1_3465 (Marden and Bauer, Unpublished Data). These genes were independently identified by a similar screen in a separate lab where they are currently the subject of genetic characterization (Bird, Manuscript in preparation).
Photosynthetic and chlorophyll biosynthetic proteins
The R. centenum ppr gene represents the first bacteriophytochrome identified in purple bacteria . Distinctive characteristics of Ppr, with respect to other bacteriophytochromes, have been discussed in detail elsewhere [reviewed in ]. In addition to ppr, a second gene (RC1_3803) is predicted to encode an additional bacteriophytochrome. RC1_3803 does not possess a photoactive yellow protein (PYP) domain, and has 45% and 55% similarity to both the photosensory core domain (PCD) and histidine kinase domain (HKD) of Ppr, respectively (not shown). A search of public protein databases identified a number of bacteriophytochromes that show homology to RC1_3803 (not shown). Based on characteristics of other bacteriophytochromes, we hypothesize that RC1_3803 may absorb near far-red light, as that wavelength of light is reported to promote negative phototaxis of R. centenum and is in the region of the spectrum where other bacteriophytochromes exhibit spectral absorbance , reviewed in .
Finally, there are two genes coding for flavin-binding photoreceptors. One gene (RC1_2193) putatively codes for a small blue light photoreceptor utilizing a flavin (BLUF) and a second protein (RC1_0351) putatively encodes a histidine kinase containing a light-oxygen-voltage (LOV) domain. Both of these putative photoreceptors likely utilize FAD or FMN as a chromophore to absorb blue light to promote a conformational change to elicit an output response. Neither protein has been genetically disrupted, but they may play a role in controlling light regulated physiology or behavior in R. centenum.
We have obtained several mutations in the transcription factor FlbD that disrupt synthesis of the polar, but not lateral flagella (D. Rollo and C. Bauer, unpublished results). These results indicate that expression of the polar and lateral flagella genes are distinct. Also, several insertion mutations that affect synthesis of both the lateral and polar flagellum map to components of the type III export system comprised of FliI, FlhA, FlhB and FliL, indicating that this export apparatus is used by both flagella systems.
There are 13 additional genes that include three functionally identified, four functionally predicted, and six of unknown function distributed among the fla clusters. These include genes encoding a CheY-like receiver protein (RC1_0209), lytic muramyl transglycoylase (RC1_0192), DNA polymerase III (RC1_0787), PPE-repeat proteins (RC1_0178), tetratricopeptide TPR_2 (RC1_0215), DNA binding protein (RC1_0222), and an ATPase involved in DNA repair (RC1_0187).
Chemotaxis and Signal Transduction
The three previously identified operons (Che1, Che2 and Che3) encoding chemotaxis-like proteins were confirmed to represent the entirety of such 'Che-like' clusters in R. centenum [32, 37, 38]. Each contains homologs of the E. coli chemotactic proteins CheA, CheY, CheW, CheB and CheR, with an additional CheW in the Che3 cluster (CheW3a and CheW3b) and a tripartate CheW in the Che2 cluster composed of three distinct CheW domains. Atypical CheA sensor kinases are also present in the Che1 and Che2 clusters, as each is hybridized to a receiver domain. Also of note are genes encoding non-canonical chemotactic components, two small proteins of unknown function in the Che2 cluster (RC1_0336 and RC1_0341) and an additional sensor kinase receiver domain hybrid (CstS3; RC1_2124) in the Che3 cluster.
The functions of all three chemotaxis operons have been elucidated. Both chemotactic and phototactic behavior in R. centenum are under Che1 control, as strains with Che1 component disruptions have motility phenotypes similar to those of E. coli chemotactic mutants . The Che2 cluster is involved in lateral flagella biosynthesis, as strains deleted of Che2 components are either hyper-flagellated or lack flagella completely, but remain chemotactic . Lastly, the Che3 cluster directs timing of encystment, as deletions of Che3 components produce strains that are either early or delayed in cyst cell development . The molecular mechanisms by which the latter two clusters achieve such altered functions are yet to be elucidated.
Whereas CheA, CheW, CheB and CheR homologs were only identified within these chemotaxis clusters (a CheB-CheR hybrid, RC1_3878, was discovered), 19 genes encode for small, stand-alone CheY-like receiver domain proteins. Besides the three Che cluster-associated CheY encoding homologs, two of these cheY-like genes are associated with neighboring genes encoding chemosensory proteins. The first (RC1_0955) is adjacent to one of two putative CheZ phosphatases (RC1_0954 and RC1_0882). The second (RC1_0353) is part of a potential operon with genes encoding a small hypothetical protein (RC1_0352), a methyl accepting chemotaxis domain protein (MCP; RC1_0354) and a homolog of the response regulator fixJ (RC1_0355). Whether these stand-alone receiver domains play a part in chemotactic signal transduction will require significant genetic and biochemical characterization.
A total of 33 genes encoding MCP domains were identified in our analysis, only three of which have been previously genetically characterized. The first identified, Ptr, was shown to be responsible for photosensory perception in R. centenum . MCP2 and MCP3, which are respectively and functionally associated with the aforementioned Che2 and Che3 clusters, have functions independent of taxis, since gene deletion strains are chemotactic but instead are either hyper-flagellated (Δmcp2) or delayed in encystment (Δmcp3) [32, 37]. As discussed above, a methyl-accepting sensory transducer is also tightly linked with a homolog of fixJ, which is known to be a transcription activator for nitrogen fixation in microaerobic conditions . We speculate that this MCP may thus have a role in altering bacterial swimming to approach the microaerobic conditions that are optimal for nitrogen fixation. The relatively large number of new and uncharacterized MCP domain-containing proteins suggests a capacity to sense and respond to a wide variety of extracellular signals, either with a tactic response, or with the alternate functions controlled by the Che2 and Che3 pathways.
In our analysis of two-component signal transduction, 55 identified genes are predicted to encode sensor kinases, 16 of which are hybridized to receiver domains. Excluding the latter group, 54 proteins are predicted to contain receiver domains. Of these 19 are stand-alone receiver domains with the remainder fused to assorted sensory and/or output domains. Lastly, 8 predicted proteins contain a histidine-containing phosphotransfer domain; three Class II histidine kinases (all R. centenum CheA proteins), two within hybrid Class I histidine kinases (RC1_0633 and RC1_2262), two stand-alone domains (RC1_2126 and RC1_3033) and one associated with a receiver domain (RC1_1779).
Analysis of the R. centenum genome demonstrates that both Rubisco- and PEPC- derived carbon assimilation can compensate for the inability to utilize malate or other C4 dicarboxylic acids in the R. centenum environment. Many newly identified genes that are discussed in this report have advanced our knowledge of the structure and origin of the R. centenum PGC, the complex life cycle involving differentiation from swim to swarm cells, and the differentiation into heat and desiccation resistant resting cysts. R. centenum also contains many sensory proteins such as bacteriophytochromes that control gene expression in response to complex environmental stimuli.
The completion of the R. centenum genome impacts the study of cyst cell development in particular, already allowing the identification of an A. brasilense flcA homolog. FlcA is a transcriptional regulator of A. brasilense encystment, and appears to have a role in R. centenum encystment (Marden and Bauer, Unpublished Data). The sequenced genome has also allowed for the discovery of an additional sensor kinase involved in encystment, RC1_2747. This gene was originally disrupted and identified in a hyper-cyst screen, however the transposition occurred in a region with low sequence similarity and was placed in a class of unknown genes .
R. centenum is emerging as a model organism for molecular genetic analysis of cyst formation, photosynthesis, phototaxis, and cellular development. This species is genetically amenable, with a variety of genetic tools already developed to explore these processes. The generation of a complete and annotated genome sequence establishes the genetic infrastructure for such studies, provides a framework to organize all the genetic information about the organism, and catalyzes future 'omics' research.
R. centenum strain SW (ATCC 51521) originated from hot spring mud in Wyoming, United States. A single colony was grown anaerobically 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 the plasmid pOTWI3 (using size fractions of 2-3 kb and 6-8 kb, respectively), and a large insert fosmid library in pEpiFOS-5 (insert sizes ranging from 28-47 kb), which was used as a scaffold. The relative amount of sequence coverage obtained from the small, medium, and large insert libraries was approximately 8×, 1×, and 1×, respectively. The whole genome sequence was established from 55,014 end sequences (giving 9.7× coverage) derived from these libraries using dye terminator chemistry on ABI 3730xl automated sequencers. The sequence was assembled with the program Arachne  and finished as described previously . The complete and annotated genome sequence of R. centenum has been deposited at DDBJ/EMBL/GenBank under the accession number CP000613.
Initial automated annotation of the genome was performed with the TIGR/JCVI Annotation Engine http://www.tigr.org/AnnotationEngine, where it was processed by TIGR's prokaryotic annotation pipeline. Included in the pipeline is gene finding with Glimmer, Blast-extend-repraze (BER) searches, HMM searches, TMHMM searches, SignalP predictions, and automatic annotations from AutoAnnotate. The manual annotation tool Manatee (manatee.sourceforge.net) was used to carefully review and confirm the annotation of every gene. Pseudogenes contained one or more mutations that would ablate expression; each inactivating mutation was subsequently checked against the original sequencing data. The circular genome map was created using the program CGView .
Mulitple amino acid sequence alignment and phylogenetic trees for this study were built using Muscle , Gblocks , PhyML , and MEGA 4.0  as previously described . Some of the sequences used in our analysis were collected from the JGI Integrated Microbial Genomes browser http://img.jgi.doe.gov/cgi-bin/pub/main.cgi. The Pathway-Tools software was employed for predicting and comparing metabolic pathways of R. centenum [16, 17]. The initial process of metabolic construction for R. centenum was automatic and involved building each pathway based on genome annotation results and the presence of each pathway in the MetaCyc database . A further step to validate the accuracy of the constructed metabolic network was carried out based on supporting information from the scientific literature.
R. centenum cultures were harvested and washed three times in phosphate buffer and then pipetted onto CENBA plates in 5 μl aliquots. After 1, 2 and 3 days incubation, the cell spots were harvested, fixed in 5% glutaraldehyde/100 mM HEPES/2 mM MgCl2 and analyzed by transmission electron microscopy as described previously . Mature R. centenum colonies were analyzed by scanning electron microscopy, performed as described previously .
We would like to dedicate this study to the memory of Jeffrey Favinger who, along with Howard Gest, was the first to isolate R. centenum. We'd like to thank The Institute for Genomics Research and the J. C. Venter Institute for providing the Annotation Engine Service that provided us with first-pass automated annotation data and the manual annotation tool Manatee free of charge. Amber L. Conrad, Liza C. Dejesa, and Heather L. Taylor provided excellent technical assistance with genome sequencing and finishing.
This work was supported by the U.S. National Science Foundation Phototrophic Prokaryotes Sequencing Project, grant number 0412824, by a Grant-in-Aid for Creative Scientific Research (No. 17GS0314) from the Japanese Society for Promotion of Science, and a Indiana University MetaCyt grant. W.D.S. is funded by the Japanese Society for Promotion of Science Postdoctoral Fellowship for Foreign Researchers (No. P07141).
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