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The Hydroxypropionate Pathway of CO2 Fixation: Fait Accompli

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The Hydroxypropionate Pathway of CO2 Fixation: Fait Accompli COMMENTARY The hydroxypropionate pathway of CO2 fixation: Fait accompli F. Robert Tabita1 Department of Microbiology and Plant Molecular Biology/Biotechnology Program, Ohio State University, Columbus, OH 43210-1292 t has long been appreciated that plants, algae, phototrophic and chemoautotrophic bacteria, and archaea are able to grow by using Icarbon dioxide (or bicarbonate) as their sole source of carbon. This feat enables such organisms to function as the ulti- mate synthetic machines as they are able to synthesize all of the needed building blocks of life via the bioconversion of the most oxidized form of carbon found in the biosphere to the reduced organic carbon compounds required for cell metabolism. Studies over the years, pri- marily with various microbes, have indicated that some organisms may ac- complish this autotrophic existence by means distinct from the usual and well- studied paradigms. In this issue of Fig. 1. Abridged outline of the completed 3-hydroxypropionate pathway of CO2 assimilation in C. PNAS (1), the finishing touches for the aurantiacus showing two distinct stages. In the first part of this scheme, CO2 fixation leads to the formation of glyoxylate and acetyl-CoA. The second part of the pathway involves the assimilation of glyoxylate, with completion of a previously proposed propionyl-CoA, to eventually form a dicarboxylic CoA ester, which is then cleaved to generate pyruvate novel route of carbon assimilation are and acetyl CoA. The acetyl-CoA formed in the second stage allows closure of the cycle with the first stage, presented for the model organism Chlo- while the pyruvate produced is used as a precursor metabolite for all subsequent metabolism. roflexus aurantiacus. This pathway en- ables synthesis of necessary metabolic Ϫ intermediates from CO2/HCO3 and potential intermediate of CO2 and ace- study is the elucidation of the enzymatic involves unique enzymatic steps (1). tate metabolism (7). Studies over the steps by which glyoxylate and propionyl- There is an interesting history relative years basically confirmed that this or- CoA may be further assimilated to pyru- to the discovery of metabolic schemes ganism, and certain relatives, use a dis- vate, with acetyl-CoA as an additional by which organisms may reduce and tinct and fourth CO2 fixation pathway product. The regeneration of acetyl-CoA then grow at the expense of oxidized (8), but until the study by Zarzycki et al. connects the second half of the pathway inorganic carbon. Elegant studies, per- (1) was performed, many key details to the first, to allow a complete and en- formed some 50–60 years ago, first elu- were not apparent, especially how the closed cyclic pathway for net assimila- cidated the metabolic pathway by which organism might assimilate key interme- tion of all potential intermediates, with CO2 could be reduced to the level of diates formed by previously known pyruvate serving as the key precursor organic carbon in plants, algae, and bac- steps. It should also be noted that two compound for all other biosynthetic pro- teria (2, 3). This scheme, the Calvin– additional CO2 fixation pathways are cesses (Fig. 1). Bassham–Benson (CBB) pathway, for now known to occur in various archaea, Zarzycki et al. (1) demonstrated that many years was thought to be the only with a total of six known autotrophic the second part of the hydroxypropi- route by which CO2 could serve as sole CO2 fixation pathways now documented onate pathway involves the condensation carbon source. Then, in the mid-1960s, (9, 10). of two-carbon and three-carbon inter- Arnon and colleagues (4) showed that Previous studies had indicated that mediates (glyoxylate and propionyl-CoA, there was another way, the reductive the first part of the hydroxypropionate respectively). This process results in the tricarboxylic acid (RTCA) cycle, which pathway involved the bicarbonate- formation of methylmalyl-CoA, which is enabled certain anaerobic phototrophic dependent formation of malyl-CoA, in- then converted to mesaconyl-C1-CoA. bacteria to accomplish an autotrophic volving several steps, including the use The next step is particularly noteworthy existence without using the CBB path- of two carboxylating enzymes, acetyl- as the CoA moiety is subsequently way. Indeed, the RTCA pathway was CoA and propionyl-CoA carboxylase shifted within the molecule from the shown to be less energetically expensive (11). Malyl-CoA is then cleaved into C1-carboxyl group to the C4-carboxyl to than the CBB route (4). Later, a third two carbon units, resulting in the forma- form mesaconyl-C4-CoA. This then CO2 reduction pathway, the Wood– tion of glyoxylate and the regeneration leads to the formation of the C5- Ljungdahl pathway, was described and of acetyl-CoA. This last step basically dicarboxylic acid CoA ester citramalyl- shown to be used by acetogenic bacteria completes the first part of the hy- CoA, which subsequently is cleaved to and many archaea (5). The discovery of droxypropionate pathway. Although it filamentous bacteria that inhabit and had been presumed that glyoxylate give an orange tinge to various hot springs might then be further assimilated (12), Author contributions: F.R.T. wrote the paper. (6) then led to the finding that one such presumably to pyruvate, the means by The author declares no conflict of interest. organism, C. aurantiacus, secretes a novel which this occurred was not readily ap- See companion article on page 21317. metabolite, 3-hydoxypropionate, as a parent. The major finding of the present 1E-mail: [email protected]. www.pnas.org͞cgi͞doi͞10.1073͞pnas.0912486107 PNAS ͉ December 15, 2009 ͉ vol. 106 ͉ no. 50 ͉ 21015–21016 Downloaded by guest on October 2, 2021 form pyruvate and acetyl-CoA, thus grown C. aurantiacus compared with pression under autotrophic growth con- completing and cyclizing the pathway. extracts from heterotrophically grown ditions, organisms that use the CBB All of the requisite enzymes that cata- cells (1). Are these levels of activity re- pathway have a real need for this lyze the newly identified steps of the flective of different amounts of synthe- pathway when growing photohetero- second stage that serve to complete the sized enzymes? There is also some trophically, because excess reducing overall pathway have been identified, equivalents from the oxidation of or- purified, and partially characterized. ganic carbon are preferentially shunted Clearly, these proteins present the op- Glyoxylate and to CO2 via the low basal levels of CBB portunity for some very interesting and enzymes. Thus, in this instance CO2 challenging mechanistic enzymology, propionyl-CoA may be serves as a necessary electron acceptor especially the CoA transferase that cata- to balance the redox potential of the cell lyzes the intramolecular CoA transfer further assimilated to (13). Does the hydroxypropionate path- between the two carboxyl groups (Fig. way play a similar role in C. aurantiacus 1). Moreover, in many cases, multifunc- pyruvate, with under photoheterotrophic growth condi- tional enzymes are involved that cata- tions or are the high levels of activity lyze more than one step of this pathway, acetyl-CoA as an seen under heterotrophic conditions thus providing some economy in the suggestive of another function? Because level of protein synthesis required to additional product. many of the enzymes of this pathway actuate this pathway. resemble other proteins, it is not beyond In addition to interesting fundamental the realm of possibility that the hy- issues relative to the structure and func- suggestion that the genes that encode droxypropionate pathway enzymes are tion of newly described enzymes, the the enzymes of this pathway might be used for other purposes in the cell. complete elucidation of this fourth CO2 regulated, yet the above enzyme activity Many of these questions, and other in- fixation scheme or hydoxypropionate levels may not be congruent with this teresting issues that arise relative to pathway raises many other interesting idea. Certainly it is not clear at this time photosynthesis in these organisms (14) questions. Not the least of which is the what might be the purpose for regulat- could be answered by developing a ge- reason this metabolic route seems, at ing these genes, especially because the netic system for C. aurantiacus. Perhaps least at this time, to be distributed in data thus far available indicate that the the studies reported here will stimulate such a limited suite of organisms. Is enzymes and the genes of this pathway such studies. there thus any real selective advantage are ‘‘on’’ all of the time. Indeed, what of this pathway for the organisms that purpose is there to basically having a ACKNOWLEDGMENTS. Work on CO2 fixation reg- use it? Moreover, the reported levels of functional hydroxypropionate pathway ulation and biochemistry in my laboratory is sup- ported by Department of Energy Grant DE-FG02– activity for key enzymatic steps are re- under photoherotrophic growth condi- 08ER15976 from the Chemical Sciences, ported to be only Ϸ2.5- to 3.5-fold tions? One is reminded that despite Geosciences, and Biosciences Division of the Of- higher from extracts of autotrophically highly regulated CO2 fixation gene ex- fice of Basic Energy Biosciences. 1. Zarzycki J, Brecht V, Muller M, Fuchs G (2009) Identify- 4:2771–2780. perthermophilic Archaeum Ignococcus hospitalis. Proc ing the missing steps of the autotrophic 3-hydroxypro- 6. Pierson BK, Castenholz RW (1974) A phototrophic glid- Natl Acad Sci USA 105:7851–7856. pionate CO2 fixation cycle in Chloroflexus aurantiacus. ing filamentous bacterium of hot springs, Chloroflexus 11. Herter S, Fuchs G, Bacher A, Eisenreich W (2002) A Proc Natl Acad Sci USA 106:21317–21322. aurantiacus, gen and sp nov. Arch Microbiol 100:5–24. bicyclic autotrophic CO2 fixation pathway in Chlo- 2. Bassham JA, Calvin M (1957) The Path of Carbon in 7. Holo H, Grace D (1989) Chloroflexus aurantiacus se- roflexus aurantiacus. J Biol Chem 277:20277–20283.
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