A novel route for ethanol oxidation in the acetogenic bacterium <i>Acetobacterium woodii</i>: the acetaldehyde/ethanol dehydrogenase pathway

Bertsch, Johannes; Siemund, Anna Lena; Kremp, Florian; Müller, Volker

doi:10.1111/1462-2920.13082

Cited by 74 publications

(95 citation statements)

References 47 publications

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“…A. woodii is able to grow by the conversion of ethanol to acetate according to the equation 2 ethanol ϩ 2 CO 2 → 3 acetate ϩ 2 H 2 O (5) (13,26,27). We therefore conclude that ethylene glycol utilization starts by the disproportionation to acetate and ethanol as seen here.…”

Section: Growth Of a Woodii On Ethylene Glycolsupporting

confidence: 61%

“…The ethanol metabolism in A. woodii was recently characterized (27). Ethanol is first oxidized to acetate, and the reducing equivalents are used to reduce 2 molecules of CO 2 to 1 molecule of acetate via the WLP.…”

Section: Discussionmentioning

confidence: 99%

“…In A. woodii, the bacterial microcompartment might be a more general mechanism for protection from toxic aldehydes, as is obvious from the dual function of the microcompartments for 1,2-PD and ethylene glycol degradation. In addition, synthesis of a microcompartment shell protein has been observed in A. woodii cells grown on ethanol, 2,3-butanediol, and, to a lesser extent, fructose and H 2 and CO 2 , all of which, except for H 2 and CO 2 , are substrates that lead to small amounts of ethanol or aldehyde intermediates (16,26,27).…”

Section: Discussionmentioning

confidence: 99%

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Ethylene Glycol Metabolism in the Acetogen Acetobacterium woodii

2016

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The acetogenic bacterium Acetobacterium woodii is able to grow by the oxidation of diols, such as 1,2-propanediol, 2,3-butanediol, or ethylene glycol. Recent analyses demonstrated fundamentally different ways for oxidation of 1,2-propanediol and 2,3-butanediol. Here, we analyzed the metabolism of ethylene glycol. Our data demonstrate that ethylene glycol is dehydrated to acetaldehyde, which is then disproportionated to ethanol and acetyl coenzyme A (acetyl-CoA). The latter is further converted to acetate, and this pathway is coupled to ATP formation by substrate-level phosphorylation. Apparently, the product ethanol is in part further oxidized and the reducing equivalents are recycled by reduction of CO 2 to acetate in the Wood-Ljungdahl pathway. Biochemical data as well as the results of protein synthesis analysis are consistent with the hypothesis that the propane diol dehydratase (PduCDE) and CoA-dependent propionaldehyde dehydrogenase (PduP) proteins, encoded by the pdu gene cluster, also catalyze ethylene glycol dehydration to acetaldehyde and its CoA-dependent oxidation to acetyl-CoA. Moreover, genes encoding bacterial microcompartments as part of the pdu gene cluster are also expressed during growth on ethylene glycol, arguing for a dual function of the Pdu microcompartment system. IMPORTANCEAcetogenic bacteria are characterized by their ability to use CO 2 as a terminal electron acceptor by a specific pathway, the WoodLjungdahl pathway, enabling in most acetogens chemolithoautotrophic growth with H 2 and CO 2 . However, acetogens are very versatile and can use a wide variety of different substrates for growth. Here we report on the elucidation of the pathway for utilization of ethylene glycol by the model acetogen Acetobacterium woodii. This diol is degraded by dehydration to acetaldehyde followed by a disproportionation to acetate and ethanol. We present evidence that this pathway is catalyzed by the same enzyme system recently described for the utilization of 1,2-propanediol. The enzymes for ethylene glycol utilization seem to be encapsulated in protein compartments, known as bacterial microcompartments. In the absence of other energetically more favorable electron acceptors, CO 2 is the only electron acceptor used for energy conservation in anoxic ecosystems. Only two groups of organisms are able to utilize CO 2 as a terminal electron acceptor, namely, methanogenic archaea and acetogenic bacteria. Acetogenic bacteria are a specialized group of strictly anaerobic bacteria that, in most cases, can use molecular hydrogen as an electron donor for CO 2 reduction and can thus grow autotrophically with H 2 and CO 2 . Therefore, they reduce two molecules of CO 2 to acetyl coenzyme A (acetyl-CoA) via the reductive acetyl-CoA pathway (the WoodLjungdahl pathway [WLP]) (1-3). This pathway of CO 2 fixation also provides energy for growth by a chemiosmotic mechanism: an electrochemical ion gradient is established in the course of CO 2 reduction (4-6) and can be used by an ATP synthase to drive the phosphory...

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Section: Growth Of a Woodii On Ethylene Glycolsupporting

confidence: 61%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Ethylene Glycol Metabolism in the Acetogen Acetobacterium woodii

2016

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“…2 ethanol ϩ 2 CO 2 → 3 acetate (12) Just recently, ethanol metabolism was elucidated in detail for the first time for an acetogenic bacterium (75). The oxidative module has a thermodynamic barrier comparable to lactate oxidation.…”

Section: Alcohol Metabolismmentioning

confidence: 99%

“…Whereas flavin-based electron bi-furcation is used to energize the unfavorable oxidation of lactate, ethanol oxidation does not utilize electron bifurcation. Instead, a bifunctional acetaldehyde/alcohol dehydrogenase, AdhE, is used that catalyzes two consecutive oxidation steps (75). First, AdhE oxidizes ethanol to acetaldehyde.…”

Section: Alcohol Metabolismmentioning

confidence: 99%

Energetics and Application of Heterotrophy in Acetogenic Bacteria

Schuchmann

Müller

2016

Appl Environ Microbiol

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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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Impact of different trace elements on metabolic routes during heterotrophic growth of C. ljungdahlii investigated through online measurement of the carbon dioxide transfer rate

Mann

Darina

Patrick

et al. 2022

Biotechnology Progress

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Synthesis gas fermentation using acetogenic clostridia is a rapidly increasing research area. It offers the possibility to produce platform chemicals from sustainable C1 carbon sources. The Wood-Ljungdahl pathway (WLP), which allows acetogens to grow autotrophically, is also active during heterotrophic growth. It acts as an electron sink and allows for the utilization of a wide variety of soluble substrates and increases ATP yields during heterotrophic growth. While glycolysis leads to CO 2 evolution, WLP activity results in CO 2 fixation. Thus, a reduction of net CO 2 emissions during growth with sugars is an indicator of WLP activity. To study the effect of trace elements and ventilation rates on the interaction between glycolysis and the WLP, the model acetogen Clostridium ljungdahlii was cultivated in YTF medium, a complex medium generally employed for heterotrophic growth, with fructose as growth substrate. The recently reported anaRAMOS device was used for online measurement of metabolic activity, in form of CO 2 evolution. The addition of multiple trace elements (iron, cobalt, manganese, zinc, nickel, copper, selenium, and tungsten) was tested, to study the interaction between glycolysis and the Wood ljungdahl pathway. While the addition of iron(II) increased growth rates and ethanol production, added nickel(II) increased WLP activity and acetate formation, reducing net CO 2 production by 28%. Also, higher CO 2 availability through reduced volumetric gas flow resulted in 25% reduction of CO 2 evolution. These online metabolic data demonstrate that the anaRAMOS is a valuable tool in the investigation of metabolic responses i.e. to determine nutrient requirements that results in reduced CO 2 production. Thereby the media composition can be optimized depending on the specific goal.

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A novel route for ethanol oxidation in the acetogenic bacterium Acetobacterium woodii: the acetaldehyde/ethanol dehydrogenase pathway

Cited by 74 publications

References 47 publications

Ethylene Glycol Metabolism in the Acetogen Acetobacterium woodii

Ethylene Glycol Metabolism in the Acetogen Acetobacterium woodii

Energetics and Application of Heterotrophy in Acetogenic Bacteria

Impact of different trace elements on metabolic routes during heterotrophic growth of C. ljungdahlii investigated through online measurement of the carbon dioxide transfer rate

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