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The Calyptogena Magnifica Chemoautotrophic

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The Calyptogena Magnifica Chemoautotrophic REPORTS or cofactors, and all necessary biosynthetic The Calyptogena magnifica intermediates, supporting an essential role of symbiont metabolism in the nutrition of this Chemoautotrophic Symbiont Genome symbiosis. Two nitrogen assimilation pathways, essential to provisioning of amino acids in the I. L. G. Newton,1 T. Woyke,2 T. A. Auchtung,1 G. F. Dilly,1 R. J. Dutton,3 M. C. Fisher,1 symbiosis, occur in R. magnifica. Nitrate and K. M. Fontanez,1 E. Lau,1 F. J. Stewart,1 P. M. Richardson,2 K. W. Barry,2 E. Saunders,2 ammonia, which enter the cell via a nitrate or J. C. Detter,2 D. Wu,4 J. A. Eisen,5 C. M. Cavanaugh1* nitrite transporter and two ammonium per- meases, are reduced via nitrate and nitrite Chemoautotrophic endosymbionts are the metabolic cornerstone of hydrothermal vent reductase and assimilated via glutamine synthe- communities, providing invertebrate hosts with nearly all of their nutrition. The Calyptogena tase and glutamate synthase, respectively (fig. magnifica (Bivalvia: Vesicomyidae) symbiont, Candidatus Ruthia magnifica, is the first intracellular S1). Although nitrate is the dominant nitrogen sulfur-oxidizing endosymbiont to have its genome sequenced, revealing a suite of metabolic form at vents (13), the symbiont may also as- capabilities. The genome encodes major chemoautotrophic pathways as well as pathways for similate ammonia via recycling of the host’s biosynthesis of vitamins, cofactors, and all 20 amino acids required by the clam. amino acid waste. Unlike any other sequenced endosymbiont genome, R. magnifica encodes etazoans at deep-sea hydrothermal genome encodes enzymes specific to this cycle, complete pathways for the biosynthesis of 20 vents flourish with the support of including a form II ribulose 1,5-bisphosphate amino acids, including 9 essential amino acids Msymbiotic chemoautotrophic bacteria carboxylase-oxygenase (RuBisCO) and phos- or their precursors (fig. S3). R. magnifica also (1). Analogous to photosynthetic chloroplasts, phoribulokinase (6). Interestingly, however, it has complete biosynthetic pathways for the which evolved from cyanobacterial ancestors appears that R. magnifica lacks homologs of majority of vitamins and cofactors (SOM text). and use light energy to fix carbon for their plant sedoheptulose 1,7-bis phosphatase and fructose The genome encodes a complete glycolytic and algal hosts, chemoautotrophic endosym- 1,6-bis-phosphatase and may regenerate ribu- pathway and the nonoxidative branch of the bionts use the chemical energy of reduced sulfur lose 1,5-bisphosphate via an unconventional pentose phosphate pathway and, interestingly, emanating from vents to provide their hosts with route, one that was a reversible pyrophosphate- also encodes a tricarboxylic acid (TCA) cycle carbon and a large array of additional necessary dependent phosphofructokinase [supporting on- lacking a-ketoglutarate dehydrogenase. The nutrients. In return, host invertebrates bridge the line material (SOM) text]. lack of this enzyme has been suggested to oxic-anoxic interface to provide symbiotic bacte- Energy for carbon fixation in R. magnifica indicate obligate autotrophy in other bacteria ria with the inorganic substrates necessary for appears to result from sulfur oxidation via the (14). Carbon fixed via the Calvin cycle can enter chemoautotrophy. The giant clam, Calyptogena sox (sulfur oxidation) and dsr (dissimilatory the TCA cycle through phosphoenolpyruvate magnifica Boss and Turner (Bivalvia: Vesico- sulfite reductase) genes (fig. S1). The symbiont and here could follow biosynthetic routes either myidae), was one of the first organisms de- may oxidize its sulfur granules via dsr homo- to fumarate or to a-ketoglutarate. scribed after the discovery of hydrothermal logs when external sulfide is lacking, as oc- As with other intracellular species, genes not vents (2). It has a reduced gut and ciliary food curs in both Allochromatium vinosum and found in the R. magnifica genome reveal im- groove and is nutritionally dependent on its Chlorobium limicola (7, 8). Homologs en- portant details about the interaction between host g-proteobacterial symbionts (here named Can- coding both a sulfide:quinone oxidoreductase and symbiont. Few substrate-specific transporters didatus Ruthia magnifica)(3, 4). We present and rhodanese are also present, and, with the dsr were found, suggesting that the symbionts are the complete genome of Ruthia magnifica and sox proteins, these enzymes can oxidize leaky or that the host actively digests symbiont (Fig. 1). Despite having a relatively small ge- sulfide or thiosulfate to sulfite (fig. S1). Sulfite cells. Indeed, Ruthia’s closest known relatives, nome (1.2 Mb), R. magnifica is predicted to can then be oxidized to sulfate by adenosine 5′- the bathymodiolid mussel symbionts, are di- encode all the metabolic pathways typical of phosphosulfate (APS) reductase and adenosine gested intracellularly by their host (15). Although free-living chemoautotrophs, including carbon triphosphate (ATP) sulfurylase before being the vesicomyids and the bathymodiolids are fixation, sulfur oxidation, nitrogen assimilation, exported from the cell via a sulfate transporter. distantly related, putative degradative stages of and amino acid and cofactor/vitamin bio- Genomic evidence of the Calvin cycle and the symbionts also are observed within C. magnifica synthesis (fig. S1 and table S1). sulfur oxidation pathways confirms the chemo- bacteriocytes (fig. S2b). The symbiont is also The following sections outline the recon- autoautotrophic nature of this symbiosis. These lacking the key cell division protein ftsZ sug- struction of R. magnifica’s chemoautotrophic data support prior reports showing RuBisCO gesting that, like Chlamydia spp., intracellular metabolism and what this might mean for the and ATP sulfurylase activity in C. magnifica gill division may not proceed through usual path- biology of its host. Our analysis provides direct tissue (4, 9), carbon dioxide uptake by the clam ways (SOM text). evidence that this symbiont fixes carbon via the in response to sulfide or thiosulfate (10), and Intracellular endosymbionts often follow dis- Calvin cycle, the dominant form of carbon fixa- sulfide-binding, zinc-containing lipoprotein in tinctive evolutionary routes, including genome tion in vent symbioses (5), by using energy the host blood stream (11). reduction, skewed base compositions, and elevated derived from sulfur oxidation. The R. magnifica Energy conservation via the creation of mutation rates (16). Given the apparent defects in a charge across a membrane proceeds in DNA repair in R. magnifica (SOM text) and the 1Harvard University, 16 Divinity Avenue, Biolabs 4080, R. magnifica through a nicotinamide adenine likely evolutionary forces pushing this genome Cambridge, MA 02138, USA. 2Department of Energy Joint dinucleotide (NADH) dehydrogenase, a sulfide: toward degradation, it is particularly informative Genome Institute, 2800 Mitchell Drive, Walnut Creek, CA quinone oxidoreductase, and an rnf complex that Ruthia retains genes encoding a full suite of 94598, USA. 3Harvard Medical School, Department of Microbiology and Molecular Genetics, 200 Longwood (12). The genome encodes a straightforward chemoautotrophic processes. Indeed, R. magnifica Avenue, Boston, MA 02115, USA. 4Institute for Genomic electron transport chain; thus, the reduced has the largest genome of any intracellular sym- Research, 9712 Medical Center Drive, Rockville, MD quinone in the symbiont membrane may transfer biont sequenced to date and may represent an early 5 20850, USA. University of California, Davis Genome electrons to cytochrome c via a bc complex, intermediate in the evolution toward a plastid-like Center, Genome and Biomedical Sciences Facility, Room 1 5311, 451 East Health Sciences Drive, Davis, CA 95616– and a terminal cytochrome c oxidase could then chemoautotrophic organelle. The broad array of 8816, USA transfer these electrons to oxygen (fig. S1). metabolic pathways revealed through sequencing *To whom correspondence should be addressed. E-mail: Our analysis shows that R. magnifica has the of the R. magnifica genome confirms and extends [email protected] potential to produce 20 amino acids, 10 vitamins prior knowledge of host nutritional dependency. 998 16 FEBRUARY 2007 VOL 315 SCIENCE www.sciencemag.org REPORTS Fig. 1. A circular representation of the R. magnifica genome. The innermost circle highlights genes of special interest: cbb (Calvin-Benson-Bassham cycle, red), sox (sulfur oxidation, green), dsr (dissimilatory sulfite reductase, blue), and rnf (NADH de- hydrogenase). The second and third circles show GC skew and %G+C, respectively. The distribution of genes is depicted on the two outer rings (fourth and fifth, forward and re- verse, respectively) colored by role category. References and Notes 3. C. M. Cavanaugh, Nature 302, 58 (1983). Academic, Dordrecht, Netherlands, 1996), pp. 285–292. 1. C. M. Cavanaugh, Z. P. McKiness, I. L. G. Newton, 4. J. J. Robinson, thesis, Harvard University, Cambridge, MA 6. J. M. Shively, G. Van Keulen, W. G. Meijer, Annu. Rev. F. J. Stewart, in The Prokaryotes (Springer-Verlag, Berlin, (1997). Microbiol. 52, 191 (1998). 2004). 5. C. M. Cavanaugh, J. J. Robinson, in Microbial Growth on 7. C. Dahl et al., J. Bacteriol. 187, 1392 (2005). 2. K. J. Boss, R. D. Turner, Malacologia 20, 161 (1980). C1 Compounds, M. E. Lidstrom, F. R. Tabita, Eds. (Kluwer 8. F. Verte et al., Biochemistry 41, 2932 (2002). www.sciencemag.org SCIENCE VOL 315 16 FEBRUARY 2007
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