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The Complete Genome Sequence of Moorella Thermoacetica (F Environmental Microbiology (2008) 10(10), 2550–2573 doi:10.1111/j.1462-2920.2008.01679.x The complete genome sequence of Moorella thermoacetica (f. Clostridium thermoaceticum) Elizabeth Pierce,1 Gary Xie,2,3 Ravi D. Barabote,2,3 functions, 665 (25.43%) matched genes of unknown Elizabeth Saunders,2,3 Cliff S. Han,2,3 function, and the remaining 24 (0.92%) had no data- John C. Detter,2,3 Paul Richardson,2,4 base match. A total of 2384 (91.17%) of the ORFs in Thomas S. Brettin,2,3 Amaresh Das,5 the M. thermoacetica genome can be grouped in Lars G. Ljungdahl5 and Stephen W. Ragsdale1* orthologue clusters. This first genome sequence of 1Department of Biological Chemistry, University of an acetogenic bacterium provides important informa- Michigan, Ann Arbor, MI, USA. tion related to how acetogens engage their extreme 2Los Alamos National Laboratory, Bioscience Division, metabolic diversity by switching among different Los Alamos, NM, USA. carbon substrates and electron donors/acceptors and 3Department of Energy Joint Genome Institute, how they conserve energy by anaerobic respiration. Walnut Creek, CA, USA. Our genome analysis indicates that the key genetic 4Lawrence Berkeley National Laboratory, Berkeley, CA, trait for homoacetogenesis is the core acs gene USA. cluster of the Wood–Ljungdahl pathway. 5Department of Biochemistry and Molecular Biology, University of Georgia, Athens, GA, USA. Introduction Here we report the first complete genome sequence of an Summary acetogenic bacterium. Acetogens are obligately anaero- This paper describes the genome sequence of bic bacteria that use a mechanism of anaerobic CO and Moorella thermoacetica (f. Clostridium thermoaceti- CO2 fixation, called the reductive acetyl-CoA or the cum), which is the model acetogenic bacterium Wood–Ljungdahl pathway as their main mechanism for that has been widely used for elucidating the energy conservation and for synthesis of acetyl-CoA and Wood–Ljungdahl pathway of CO and CO2 fixation. cell carbon from CO2 (Drake et al., 1994). Other terms to This pathway, which is also known as the reductive describe an organism using this type of metabolism are acetyl-CoA pathway, allows acetogenic (often called ‘homoacetogen’ and ‘CO2-reducing acetogen’. We deter- homoacetogenic) bacteria to convert glucose sto- mined the genome sequence of Moorella thermoacetica, ichiometrically into 3 mol of acetate and to grow originally named Clostridium thermoaceticum, which has autotrophically using H2 and CO as electron donors been the model acetogen since its isolation in 1942 and CO2 as an electron acceptor. Methanogenic (Fontaine et al., 1942) for elucidating the Wood– archaea use this pathway in reverse to grow by con- Ljungdahl pathway. As discussed below, this pathway is verting acetate into methane and CO2. Acetogenic found in a broad range of phylogenetic classes, and is bacteria also couple the Wood–Ljungdahl pathway to used in both the oxidative and reductive directions. a variety of other pathways to allow the metabolism of Besides being used for energy production and autotrophic a wide variety of carbon sources and electron donors carbon assimilation in acetogens (Ljungdahl, 1994; (sugars, carboxylic acids, alcohols and aromatic Ragsdale, 1997; Drake et al., 2002), the Wood–Ljungdahl compounds) and electron acceptors (CO2, nitrate, pathway is used for acetate catabolism by sulfate- nitrite, thiosulfate, dimethylsulfoxide and aromatic reducing bacteria (Schauder et al., 1988; Spormann and carboxyl groups). The genome consists of a single Thauer, 1988) and aceticlastic methanogens (Ferry, 1999) circular 2 628 784 bp chromosome encoding 2615 and for CO2 fixation by hydrogenotrophic methanogens open reading frames (ORFs), which includes 2523 (Stupperich et al., 1983; Ladapo and Whitman, 1990). predicted protein-encoding genes. Of these, 1834 As early as 1932, organisms were discovered that genes (70.13%) have been assigned tentative could convert H2 and CO2 into acetic acid (Fischer et al., 1932). In 1936, Wieringa reported the first acetogenic bacterium, Clostridium aceticum (Wieringa, 1936; 1940), Received 20 December, 2007; accepted 1 May, 2008. *For correspondence. E-mail [email protected]; Tel. (+1) 734 615 which was reisolated in 1981 (Braun et al., 1981). 4621; Fax (+1) 734 763 4581. Moorella thermoacetica (Collins et al., 1994), a © 2008 The Authors Journal compilation © 2008 Society for Applied Microbiology and Blackwell Publishing Ltd M. thermoacetica genome sequence 2551 clostridium in the Thermoanaerobacteriaceae family, community that has been enriched for bioremediation attracted wide interest when it was isolated because of its (Macbeth et al., 2004). unusual ability to convert glucose almost stoichiometri- For organisms that house acetogens in their digestive cally to 3 mol of acetic acid (Fontaine et al., 1942). It took systems, like humans, termites and ruminants (Greening many years to uncover the biochemical reactions respon- and Leedle, 1989; Tholen and Brune, 1999; Chassard sible for this homoacetogenic pathway. The novelty of this and Bernalier-Donadille, 2006), the acetate generated by pathway was recognized with the discovery that growth of microbial metabolism is a beneficial nutrient for the host M. thermoacetica on glucose involves incorporation of and for other microbes within the community. In these two molecules of CO2 directly into acetic acid (Barker and ecosystems, acetogens can compete directly with hydro- Kamen, 1945; Wood, 1952). The isolation of Acetobacte- genotrophic methanogenic archaea, or interact syntrophi- rium woodii in 1977 and the description of methods to cally with acetotrophic methanogens that use H2 and CO2 isolate organisms that can grow on H2 and CO2 (Balch to produce methane (Chassard and Bernalier-Donadille, et al., 1977) led to the isolation of many acetogens that 2006). Organisms containing the acs gene cluster are can grow autotrophically, and in 1983 M. thermoacetica also enriched in the marine and terrestrial vertebrate and was shown to grow on H2/CO2 (Kerby and Zeikus, 1983). invertebrate gut biomes (Gill et al., 2006; Warnecke et al., The identification of a hydrogenase in 1982 provided a 2007). In the termite gut, acetogens are the dominant biochemical basis for autotrophic growth of acetogens on hydrogen sinks (Pester and Brune, 2007), and it has been hydrogen (Drake, 1982). Subsequently, acetogens have proposed that acetate is the major energy source for the been shown to use a wide variety of carbon sources and termite (Odelson and Breznak, 1983). However, metha- electron donors and acceptors. Moorella thermoacetica is nogens are the dominant hydrogenotrophs in many envi- a versatile heterotroph, growing on sugars, two-carbon ronments as methanogens have a lower threshold for H2 compounds (glyoxylate, glycolate and oxalate), lactate, than acetogens (Le Van et al., 1998) and as the energy pyruvate, short-chain fatty acids and methoxylated yield from the conversion of CO2 and H2 to methane is aromatic compounds. Besides CO2, electron acceptors greater than that for conversion to acetate (Schink, 1997). include nitrate, nitrite, thiosulfate and dimethylsulfoxide. Under such conditions, acetogens must often resort to Acetogenic bacteria play an important role in the global other metabolic pathways for growth and, thus, have a carbon cycle, producing over 1012 kg (10 billion US tons) highly diverse metabolic menu that comprises the biodeg- of acetic acid on a huge scale annually (Wood and radation products of most natural polymers like cellulose Ljungdahl, 1991; Drake et al., 1994), which dwarfs the and lignin, including sugars, alcohols, organic acids and total output of acetate (an important chemical feedstock) aldehydes, aromatic compounds and inorganic gases like 10 -1 by the world’s chemical industry (~10 kg year ). While CO, H2 and CO2. They also can use a variety of electron most acetogens like M. thermoacetica are in the phylum acceptors, e.g. CO2, nitrate, dimethylsulfoxide, fumarate Firmicutes, acetogens include Spirochaetes (Leadbetter and protons. The M. thermoacetica genome sequence et al., 1999; Salmassi and Leadbetter, 2003), Deltapro- described here provides important information related to teobacteria like Desulfotignum phosphitoxidans (Schink how acetogens engage this extreme metabolic diversity et al., 2002), and Acidobacteria like Holophaga foetida and how they switch with such facility among different (Liesack et al., 1994). Important in the biology of the soil, carbon substrates and electron donors and acceptors. lakes and oceans, acetogens have been isolated from diverse environments, including the GI tracts of animals and termites (Breznak, 1994; Mackie and Bryant, 1994), Results rice paddy soils (Rosencrantz et al., 1999), hypersaline General genome features waters (Ollivier et al., 1994), surface soils (Peters and Conrad, 1995; Kusel et al., 1999) and deep subsurface The major features of the M. thermoacetica genome are sediments (Liu and Suflita, 1993). Like methanogens, listed in Table 1 and shown in Fig. S1. The genome con- acetogens act as a H2 sink, depleting H2 that is generated sists of a single circular 2 628 784 bp chromosome that in anaerobic environments during the natural biodegrada- has a GC content of 56% (Fig. S1). Base pair one of the tion of organic compounds. As the build-up of H2 inhibits chromosome was assigned within the putative origin of biodegradation by creating an unfavourable thermody- replication. The genome contains 51 tRNAs, three rRNAs namic equilibrium, acetogens
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