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Hybrid respiration

A new method of energy harvest by L. plantarum (and maybe other LAB) 

In early 2021, The International Scientific Association for Probiotics and Prebiotics (ISAPP) defined food that are ‘fermented’ as  “foods made through desired microbial growth and enzymatic conversions of food components” (Marco et al. 2021).

There was good reason to establish this new definition. In biochemistry, fermentation  is “the extraction of energy from carbohydrates in the absence of oxygen”. In food fermentation, this definition would exclude foods produced using fungi like A. oryzae and R. oryzae used in koji and tempeh production, as well vinegar and kombucha.

Transformation of food into fermented food occurs when microbes use nutrients like carbohydrates as a source of energy and store this energy in the form of ATP (adenine triphosphate). Generation of ATP is dependent on a shuffling of electrons through various chemical pathways, before reaching a terminal electron acceptor. This shuffling of electrons, where one molecule loses an electron and the terminal electron acceptor gains an electron is called a redox reaction. Simply put: the better a microbe is at moving electrons through a metabolic pathway (e.g. managing its redox reaction), the greater its ecological fitness.

managing redox homeostasis = greater ecological fitness

Since food is a rich source of organic nutrients, food fermenting microbes can use these organic nutrients to produce energy. They can generate energy using three types of metabolism: fermentation, aerobic respiration,  anaerobic respiration. Depending on which nutrients are available and the amount of oxugen present at the various stages of fermentation, some microbes (like S. cerevisiae) can also switch which type of metabolism they use to produce energy. This can result in changes in the rate of microbial growth and nutrient consumption, which translates to changes in food fermentation rate and flavor production. 

What are the key metabolic pathways in food fermentation?



Description: “Extraction of energy from carbohydrates in the absence of oxygen.” Fermentation does not use an electrochemical gradient to drive ATP generation.

Final Electon Acceptor:
pyruvate (usually)

Metabolic products: lactic acid, acetic acid, formic acid , succinic acid, butanol, or ethanol among others, and ATP

ATP generated: 2 (least efficient)

Example organism involved: Lactobacillus spp.

Aerobic Respiration

Description: “Extraction of energy from carbohydrates in the presence of oxygen.” Aerobic respiration uses an electrochemical gradient to drive ATP generation.

Final Electon Acceptor:

Metabolic products: carbon dioxyde, water, ATP

ATP generated: 38 (most efficient)

Example organism involved: Rhizopus oryzae

Anaerobic Respiration

Description: “Respiration using electron acceptors other than oxygen.” Anaerobic respiration uses an electrochemical gradient to drive ATP generation.

Final Electon Acceptor:
nitrate, sulfate,ferric ion, carbon dioxide, and other inorganics

Metabolic products: lactic acid, ethanol, ATP

ATP generated: 5-36 (medium-high efficiency)

Example organism involved:Saccharomyces cerevisiae

Recently, Dr. Tejedor-Sanz in Maria Marco’s lab at UC Davis described a novel type of metabolism occuring in food fermentation, called hybrid respiration. This novel microbial metabolic pathway uses both features of fermentation (where pyruvate acts as an electron acceptor) and also makes use of an extracellular electron transfer (EET), an electrochemical gradient comparable to the intracellular electron transport chain (ETC) that drives aerobic and anaerobic respiration. This process results in a ~1.75x-more efficient process (i.e. ATP generation) compared to fermentation alone.

Hybrid Respiration

Description: “Extraction of energy from carbohydrates in the absence of oxygen that uses features of respiration to generate ATP”

Final Electon Acceptor: pyruvate and extracellular iron
ATP generated: 3-8

Example organism involved: Lactobacillus plantatum

How does this relate to food fermentation?

  • Tejedor-Sanz et al. identified a novel way in which L. plantarum generates energy called hybrid respiration

  • Hybrid respiration is dependent on the presence of quinones and extracellular electron acceptors like iron, both typically present in dairy and plant foods

  • To test if hybrid respiration happens in food fermentation, the group fermented kale juice, and reported hybrid respiration allows L. plantarum to make more ATP, grow faster, and produce more lactic acid and acetic acid

  • This increase the acidification rate, allowing L. plantarum to outcompete other microbes present, increasing the food safety profile, and changing the final taste profile
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