Physiology of the thermophilic acetogen Moorella thermoacetica

Drake, Harold L.; Daniel, Steven L.

doi:10.1016/j.resmic.2004.10.002

Cited by 135 publications

(69 citation statements)

References 105 publications

(7 reference statements)

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“…thermoacetica is able to catalyze the near-stoichiometric conversion of glucose to 3 mol of acetate using PFOR, which couples the glycolytic pathway to the WoodLjungdahl pathway (1,47). In contrast, C. maritimus KKC1 cannot grow on glucose (and other organic compounds) without electron acceptors, but it can grow with electron acceptors such as thiosulfate, resulting in a small amount of acetate (23).…”

Section: Discussionmentioning

confidence: 99%

“…Genomic analysis of C. maritimus KKC1 revealed that it lacks genes encoding authentic PFOR, which is conserved across Moorella species. From a thermodynamic perspective, acetogenesis from glucose is less effective in supporting growth than anaerobic respiration using electron acceptors except for CO 2 (1). Therefore, it is assumed that the lack of authentic PFOR in C. maritimus KKC1 might result in a survival strategy different from that of M. thermoacetica, which can thrive where no electron acceptors (except for CO 2 ) are available.…”

Section: Discussionmentioning

confidence: 99%

“…Although Moorella stamsii and Moorella thermoacetica strain AMP are reported to be hydrogenogenic carboxydotrophs like C. maritimus KKC1 (24,25), most Moorella strains are known homoacetogens. M. thermoacetica is the type species for the genus and is a well-known model of acetogenic bacteria that can grow autotrophically using H 2 plus CO 2 or CO to produce acetate via the Wood-Ljungdahl pathway (1,26). We compared the overall genomic features of C. maritimus KKC1 (a hydrogenogenic carboxydotroph) to those of acetogenic M. thermoacetica ATCC 39073 and Moorella perchloratireducens An10 and analyzed CODH gene clusters to gain insight into the physiological and phylogenetic differences between C. maritimus KKC1 and Moorella groups.…”

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confidence: 99%

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Genomic Analysis of Calderihabitans maritimus KKC1, a Thermophilic, Hydrogenogenic, Carboxydotrophic Bacterium Isolated from Marine Sediment

Omae

Yoneda

Fukuyama

et al. 2017

Appl Environ Microbiol

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Calderihabitans maritimus KKC1 is a thermophilic, hydrogenogenic carboxydotroph isolated from a submerged marine caldera. Here, we describe the de novo sequencing and feature analysis of the C. maritimus KKC1 genome. Genomebased phylogenetic analysis confirmed that C. maritimus KKC1 was most closely related to the genus Moorella, which includes well-studied acetogenic members. Comparative genomic analysis revealed that, like Moorella, C. maritimus KKC1 retained both the CO 2 -reducing Wood-Ljungdahl pathway and energy-converting hydrogenase-based module activated by reduced ferredoxin, but it lacked the HydABC and NfnAB electron-bifurcating enzymes and pyruvate:ferredoxin oxidoreductase required for ferredoxin reduction for acetogenic growth. Furthermore, C. maritimus KKC1 harbored six genes encoding CooS, a catalytic subunit of the anaerobic CO dehydrogenase that can reduce ferredoxin via CO oxidation, whereas Moorella possessed only two CooS genes. Our analysis revealed that three cooS genes formed known gene clusters in other microorganisms, i.e., cooS-acetyl coenzyme A (acetylCoA) synthase (which contained a frameshift mutation), cooS-energy-converting hydrogenase, and cooF-cooS-FAD-NAD oxidoreductase, while the other three had novel genomic contexts. Sequence composition analysis indicated that these cooS genes likely evolved from a common ancestor. Collectively, these data suggest that C. maritimus KKC1 may be highly dependent on CO as a low-potential electron donor to directly reduce ferredoxin and may be more suited to carboxydotrophic growth compared to the acetogenic growth observed in Moorella, which show adaptation at a thermodynamic limit.IMPORTANCE Calderihabitans maritimus KKC1 and members of the genus Moorella are phylogenetically related but physiologically distinct. The former is a hydrogenogenic carboxydotroph that can grow on carbon monoxide (CO) with H 2 production, whereas the latter include acetogenic bacteria that grow on H 2 plus CO 2 with acetate production. Both species may require reduced ferredoxin as an actual "energy equivalent," but ferredoxin is a low-potential electron carrier and requires a highenergy substrate as an electron donor for reduction. Comparative genomic analysis revealed that C. maritimus KKC1 lacked specific electron-bifurcating enzymes and possessed six CO dehydrogenases, unlike Moorella species. This suggests that C. maritimus KKC1 may be more dependent on CO, a strong electron donor that can directly reduce ferredoxin via CO dehydrogenase, and may exhibit a survival strategy different from that of acetogenic Moorella, which solves the energetic barrier associated with endergonic reduction of ferredoxin with hydrogen.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

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Genomic Analysis of Calderihabitans maritimus KKC1, a Thermophilic, Hydrogenogenic, Carboxydotrophic Bacterium Isolated from Marine Sediment

Omae

Yoneda

Fukuyama

et al. 2017

Appl Environ Microbiol

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“…Constitutive parts of the WLP have been elucidated in the Echcontaining acetogen M. thermoacetica (12,28). Now, available data indicate that the basic principles can be transferred to all acetogens, including those in the Rnf-containing subclass.…”

Section: Wood-ljungdahl Pathway and Redox Balancingmentioning

confidence: 99%

“…These donors include hexoses like glucose or fructose, which most acetogens can use, but also pentoses like xylose (44). Alcohols, including ethanol, propanol, and butanol, can be utilized, for example, by M. thermoacetica, whereas diols such as 1,2-propanediol, ethylene glycol, or 2,3-butanediol can be utilized, for example, by some Acetobacterium species, including A. woodii (28,45,46). The potential substrates of acetogens extend to carboxylic acids, such as pyruvate, lactate, citrate, or the C 2 acids oxalate, glyoxylate, or glycolate.…”

Section: Metabolic Flexibility Of Acetogensmentioning

confidence: 99%

Energetics and Application of Heterotrophy in Acetogenic Bacteria

Schuchmann

Müller

2016

Appl Environ Microbiol

208

214

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Acetogenic bacteria are a diverse group of strictly anaerobic bacteria that utilize the Wood-Ljungdahl pathway for CO 2 fixation and energy conservation. These microorganisms play an important part in the global carbon cycle and are a key component of the anaerobic food web. Their most prominent metabolic feature is autotrophic growth with molecular hydrogen and carbon dioxide as the substrates. However, most members also show an outstanding metabolic flexibility for utilizing a vast variety of different substrates. In contrast to autotrophic growth, which is hardly competitive, metabolic flexibility is seen as a key ability of acetogens to compete in ecosystems and might explain the almost-ubiquitous distribution of acetogenic bacteria in anoxic environments. This review covers the latest findings with respect to the heterotrophic metabolism of acetogenic bacteria, including utilization of carbohydrates, lactate, and different alcohols, especially in the model acetogen Acetobacterium woodii. Modularity of metabolism, a key concept of pathway design in synthetic biology, together with electron bifurcation, to overcome energetic barriers, appears to be the basis for the amazing substrate spectrum. At the same time, acetogens depend on only a relatively small number of enzymes to expand the substrate spectrum. We will discuss the energetic advantages of coupling CO 2 reduction to fermentations that exploit otherwise-inaccessible substrates and the ecological advantages, as well as the biotechnological applications of the heterotrophic metabolism of acetogens. Synthesis of acetate from molecular hydrogen (H 2 ) and carbon dioxide (CO 2 ) by microorganisms was discovered in 1932 by F. Fischer (1). Only 4 years later, the first acetogenic bacterium was isolated in pure culture (2). However, understanding the metabolism of acetogenesis turned out to be a challenging task and continues to be so today. Nevertheless, the road toward this goal is paved with landmark discoveries in the field of microbiology. The most characteristic feature of acetogens is their ability to produce acetate from H 2 plus CO 2 . This reaction provides only very little energy (⌬G 0= ϭ Ϫ95 kJ/mol [3]); still, acetogens evolved special adaptations to "make a living" from this conversion (4, 5). We refer to this as "autotrophic acetogenesis." Ironically, major parts to our understanding of this trait came from studies on an organism that was not known to perform autotrophic acetogenesis: Moorella thermoacetica (formerly Clostridium thermoaceticum). This organism, isolated by F. E. Fontaine in 1942 (6), attracted interest for its ability to convert glucose stoichiometrically to 3 moles of acetate, a conversion named "homoacetogenesis." Elucidation of this pathway led to the discovery of an entirely new pathway of CO 2 fixation, the reductive acetyl coenzyme A (CoA) pathway, or the Wood-Ljungdahl pathway (WLP; named after Harland G. Wood and Lars G. Ljungdahl, who made major contributions to the elucidation of this pathway) (7-9). This pathway has t...

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CODehydrogenase/Acetyl‐CoASynthase

Volbeda

2004

Handbook of Metalloproteins

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The bifunctional tetrameric (α 2 β 2 ) enzyme carbon monoxide dehydrogenase (CODH)/acetyl‐CoA synthase (ACS) is a central component of the Wood‐Ljungdahl pathway of acetogenic bacteria. In this pathway, two CO 2 molecules are reduced to a methyl group by folate‐containing enzymes and to CO by CODH, respectively. These two substrates are subsequently combined in ACS to form an Ni‐bound acetyl group that is reductively eliminated as acetyl‐CoA. The CODH and ACS active sites are about 70 Å apart and are connected by a network of hydrophobic tunnels. Thus, CO produced at the former enzyme migrates inside the bifunctional protein to the ACS site. Site‐directed mutagenesis has confirmed the functional role of the tunnels. The ACS subunit undergoes a conformational change that blocks the tunnel near the active site, preventing the escape of the toxic CO from within the enzyme upon methyl binding to nickel.

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Physiology of the thermophilic acetogen Moorella thermoacetica

Cited by 135 publications

References 105 publications

Genomic Analysis of Calderihabitans maritimus KKC1, a Thermophilic, Hydrogenogenic, Carboxydotrophic Bacterium Isolated from Marine Sediment

Genomic Analysis of Calderihabitans maritimus KKC1, a Thermophilic, Hydrogenogenic, Carboxydotrophic Bacterium Isolated from Marine Sediment

Energetics and Application of Heterotrophy in Acetogenic Bacteria

CODehydrogenase/Acetyl‐CoASynthase

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