Energetics and Application of Heterotrophy in Acetogenic Bacteria

Abstract

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...

The Wood–Ljungdahl pathway as a key component of metabolic versatility in candidate phylum Bipolaricaulota (Acetothermia, OP1)

“…As previously noted (Ljungdahl, ; Schuchmann and Müller, ; Buckel and Thauer, ), the genomic context within which the WL exists can provide important clues regarding its functionality in a specific organism. Below, we provide a detailed evaluation of the potential role of the WL pathway in various Bipolaricaulota modes of metabolism.…”

“…The possession of heterotrophic capabilities argues for the use of WL in homoacetogenic growth in all analysed Bipolaricaulota orders; as previously observed in model bacterial acetogens, e.g., Moorella thermoacetica and Acetobacterium woodii (Schuchmann and Müller, ). Under heterotrophic growth scenarios, WL would function to recycle CO 2 and reduced electron carriers (NADH, reduced ferredoxin) generated during substrate degradation to acetyl CoA, with the production of one acetate molecule from two CO 2 molecules.…”

Fermentation and chemical composition of high‐moisture lucerne leaf and stem silages harvested at different stages of development using a leaf stripper

“…Heterofermentative bacteria such as Lactobacillus buchneri, as well as acetogenic bacteria, may be responsible for the anaerobic conversion of lactic acid to acetic acid (Oude Elferink et al, 2001;Schuchmann & Müller, 2016 Although fermentation was variable for high-moisture leaf and stem silages, butyric acid was not present in significant amounts except for cut 1's 10%-20% bloom leaf silages, which did not achieve a pH <5. Heterofermentative bacteria such as Lactobacillus buchneri, as well as acetogenic bacteria, may be responsible for the anaerobic conversion of lactic acid to acetic acid (Oude Elferink et al, 2001;Schuchmann & Müller, 2016 Although fermentation was variable for high-moisture leaf and stem silages, butyric acid was not present in significant amounts except for cut 1's 10%-20% bloom leaf silages, which did not achieve a pH <5.…”

Energy Metabolism during Anaerobic Methane Oxidation in ANME Archaea

“…A diversity of enzyme compliments are found within methanogens and acetogens, which accomplish what at first glance looks like the same overall metabolisms respectively— making methane (100, 111), or making acetate (73, 90, 91). Yet the differences in specific enzyme compliments are significant because they influence basic energy metabolism and its yield.…”