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Carbon Metabolic Pathways in Phototrophic Bacteria and Their Broader Evolutionary Implications

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Carbon Metabolic Pathways in Phototrophic Bacteria and Their Broader Evolutionary Implications REVIEW ARTICLE published: 01 August 2011 doi: 10.3389/fmicb.2011.00165 Carbon metabolic pathways in phototrophic bacteria and their broader evolutionary implications Kuo-HsiangTang1,2*†,Yinjie J.Tang3 and Robert Eugene Blankenship1,2* 1 Department of Biology, Washington University in St. Louis, St. Louis, MO, USA 2 Department of Chemistry, Washington University in St. Louis, St. Louis, MO, USA 3 Department of Energy, Environment, and Chemical Engineering, Washington University in St. Louis, St. Louis, MO, USA Edited by: Photosynthesis is the biological process that converts solar energy to biomass, bio- Thomas E. Hanson, University of products, and biofuel. It is the only major natural solar energy storage mechanism on Delaware, USA Earth. To satisfy the increased demand for sustainable energy sources and identify the Reviewed by: Thomas E. Hanson, University of mechanism of photosynthetic carbon assimilation, which is one of the bottlenecks in pho- Delaware, USA tosynthesis, it is essential to understand the process of solar energy storage and associated Ulrike Kappler, University of carbon metabolism in photosynthetic organisms. Researchers have employed physiological Queensland, Australia studies, microbiological chemistry, enzyme assays, genome sequencing, transcriptomics, *Correspondence: and 13C-based metabolomics/fluxomics to investigate central carbon metabolism and Kuo-Hsiang Tang, One Brookings Drive, Campus Box 1137, St. Louis, enzymes that operate in phototrophs. In this report, we review diverse CO2 assimilation MO, USA. pathways, acetate assimilation, carbohydrate catabolism, the tricarboxylic acid cycle and e-mail: [email protected]; some key, and/or unconventional enzymes in central carbon metabolism of phototrophic Robert Eugene Blankenship, One microorganisms. We also discuss the reducing equivalent flow during photoautotrophic Brookings Drive, Campus Box 1137, St. Louis, MO, USA. and photoheterotrophic growth, evolutionary links in the central carbon metabolic network, e-mail: [email protected] and correlations between photosynthetic and non-photosynthetic organisms. Considering †Current Address the metabolic versatility in these fascinating and diverse photosynthetic bacteria, many Kuo-Hsiang Tang, Carlson School of essential questions in their central carbon metabolism still remain to be addressed. Chemistry and Biochemistry, and 13 Department of Biology, Clark Keywords: acetate assimilation, autotrophic and anaplerotic CO2 assimilation, biomass and biofuel, C-based University, 950 Main Street, metabolomics, citrate metabolism, photosynthesis, unconventional pathways and enzymes Worcester, MA 01610, USA. INTRODUCTION plastoquinone oxidoreductase) through the cytochrome b6f com- Phototrophic bacteria use light as the energy source to produce plex to NADP+ in Photosystem I (plastocyanin: ferredoxin oxi- phosphate bond energy (ATP) and reductants [e.g., NAD(P)H and doreductase; Blankenship, 2002). This non-cyclic electron trans- reduced ferredoxin] through photosynthetic electron transport. port is represented in the Z-scheme of photosynthesis. A cyclic Oxygenic phototrophic bacteria, known as cyanobacteria, share electron transport pathway also operates in oxygenic phototrophs similar electron transport pathways with other oxygenic pho- during phototrophic growth and synthesizes ATP instead of totrophs (e.g., plants and algae). Photosynthetic electron trans- NADPH (Iwai et al., 2010). Photosynthetic electron transport port in cyanobacteria proceeds from oxidation of H2Oin pathways are different in anoxygenic (non-oxygen evolving) pho- the oxygen evolving complex of Photosystem II (or H2O: totrophs, all of which contain either a type II (quinone type) or a type I (Fe-S type) reaction center (RC). Five out of six phyla of photosynthetic bacteria are anoxygenic phototrophs: proteobac- teria [anaerobic anoxygenic phototrophic Proteobacteria (AnAPs) Abbreviations: Abbreviations of phototrophic bacteria. Three-letter abbrevia- tion for the generic name of phototrophic bacteria follows the information and aerobic anoxygenic phototrophic Proteobacteria (AAPs)], listed on LPSN (List of Prokaryotic names with Standing in Nomenclature) green sulfur bacteria (GSBs), filamentous anoxygenic phototrophs (http://www.bacterio.cict.fr/index.html). (FAPs; or green non-sulfur/gliding bacteria), heliobacteria, and Other abbreviations. AAPs, aerobic anoxygenic phototrophic Proteobacteria; ACL, the recently discovered chloroacidobacteria (Blankenship, 2002; ATP citrate lyase; AnAPs, anaerobic anoxygenic phototrophic Proteobacteria; CCL, Bryant and Frigaard, 2006; Bryant et al., 2007). AAPs, AnAPs, citryl-CoA lyase; CCS, citryl-CoA synthetase; (Re)/(Si)-CS, (Re)/(Si)-citrate syn- thase; ED, Entner–Doudoroff; EMP, Emden–Meyerhof–Parnas; FAPs, filamen- and FAPs contain a type II RC, and GSBs, heliobacteria and tous anoxygenic phototrophs; FBP, fructose 1,6-bisphosphate; Fd, ferredoxin; chloroacidobacteriahaveatypeIRC.BacteriawithatypeIIRC GAP, d-glyceraldehyde-3-phosphate; Glc, glucose; GSBs, green sulfur bacteria; operate cyclic electron transport to generate ATP and reverse elec- 3HOP, 3-hydroxypropionate; KDPG, 2-keto-3-deoxy-6-phosphogluconate; α-KG, tron transport to produce NAD(P)H. GSBs operate both cyclic α-ketoglutarate; OAA, oxaloacetate; OPP pathway, oxidative pentose phosphate pathway; OTCA/RTCA cycle, oxidative/reductive tricarboxylic acid cycle; PGM, and non-cyclic electron transport to make NAD(P)H and ATP, phosphoglycerate mutase; RC, reaction center; R5P, ribose-5-phosphate; RuBisCO, and heliobacteria have been suggested to employ cyclic electron ribulose 1,5-bisphosphate carboxylase/oxygenase. transport (Kramer et al., 1997). www.frontiersin.org August 2011 | Volume 2 | Article 165 | 1 Tang et al. Central carbon metabolism and evolution in photosynthesis The energy and reducing equivalents generated from light- induced electron transport drive diverse carbon metabolic path- ways for producing cellular material, bioactive products and biofuel. Additionally, numerous photosynthetic bacteria play essential roles in global carbon, nitrogen, and sulfur cycles, as many of them are known to assimilate nitrogen and/or oxi- dize sulfide in conjunction with their central carbon and energy metabolisms. Inorganic and organic carbon sources are used for building cellular building blocks of photoautotrophic and photoheterotrophic bacteria, respectively. Cyanobacteria, AnAPs, FAPs, and GSBs can grow autotrophically via a variety of autotrophic CO2 assimilation pathways, while AAPs and heliobac- teria are obligate photoheterotrophs. AAPs have been discov- ered in some ocean surface waters (Kolber et al., 2001) and certain (extreme) ecosystems (Yurkov and Csotonyi, 2009), and may play important roles in global carbon regulation (Kol- ber et al., 2001). Heliobacteria are the most recently discov- ered anaerobic anoxygenic phototrophs. Compared to other phototrophic bacteria, heliobacteria have the simplest photo- system (Heinnickel and Golbeck, 2007; Sattley and Blanken- ship, 2010) and some unique features: they are the only Gram- positive phototrophic bacteria in the bacterial phylum Firmi- cutes (and form heat resistant endospores), and are the only obligate anaerobic photoheterotrophs. All known heliobacteria are active nitrogen fixers and hydrogen producers (Madigan, 2006). The evolution of eukaryotes has been suggested to have occurred through endosymbiosis (Margulis, 1968; Doolittle, 1998). It has been proposed that the ancestral eukaryotes were anaerobes, and that aerobic α-Proteobacteria, which include FIGURE1|Schematic representation of central carbon metabolism in many AAPs, were the origins of mitochondria of eukaryotes and phototrophic bacteria. The metabolic pathways of autotrophic CO2 fixation (red lines), anaplerotic CO2 assimilation (green lines), carbohydrate cyanobacteria were the forerunners of the chloroplast of higher metabolism (blue lines), acetate assimilation (brown lines), and the TCA plant cells (Margulis, 1968; Hohmann-Marriott and Blankenship, cycle (black lines) in phototrophic bacteria are shown. Some metabolic 2011). pathways are employed only in phototrophic bacteria, and others are While photosynthetic bacteria have simplified, and some- distributed in phototrophic and non-phototrophic microbes. times unique, photosystems compared to higher plants and green algae (Blankenship, 2002), their carbon metabolism pathways are rather complex (Figure 1). Previous studies on central car- RESULTS AND DISCUSSIONS bon metabolism of photosynthetic organisms have suggested OVERVIEW: THE LIGHT AND DARK REACTIONS IN PHOTOTROPHIC that some phototrophic and non-phototrophic organisms use BACTERIA some distinct carbon assimilation and carbon metabolic path- No two phyla of phototrophic bacteria have the same metabolic ways (Hugler et al., 2011). In this report, we review the stud- pathways, while some ecological and metabolic features of pho- ies of key central carbon metabolic pathways, including CO2 totrophic bacteria are correlated with the type of RC employed. and acetate assimilations, carbohydrate catabolism and the tri- Only the five most characterized phyla of phototrophic bacteria are carboxylic acid (TCA) cycle, and also highlight several essen- discussed here. Bacteria with a type II (quinone type) RC (e.g.,Pro- tial and/or unconventional enzymes contributing to the critical teobacteria and FAPs) are facultative phototrophs (can grow with metabolic pathways in phototrophic bacteria. Some related meta- or
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