Propionibacterium freudenreichii thrives in microaerobic conditions by complete oxidation of lactate to CO2.

Alexander Dank,Oscar Van Mastrigt,Søren K Lillevang,Sjef Boeren,Eddy J Smid,Tjakko Abee

doi:10.1111/1462-2920.15532

Alexander Dank, Oscar Van Mastrigt + Show 4 more

Open Access

https://doi.org/10.1111/1462-2920.15532

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Abstract

SummaryIn this study we show increased biomass formation for four species of food‐grade propionic acid bacteria (Acidipropionibacterium acidipropionici, Acidipropionibacterium jensenii, Acidipropionibacterium thoenii and Propionibacterium freudenreichii) when exposed to oxygen, implicating functional respiratory systems. Using an optimal microaerobic condition, P. freudenreichii DSM 20271 consumed lactate to produce propionate and acetate initially. When lactate was depleted propionate was oxidized to acetate. We propose to name the switch from propionate production to consumption in microaerobic conditions the ‘propionate switch’. When propionate was depleted the ‘acetate switch’ occurred, resulting in complete consumption of acetate. Both growth rate on lactate (0.100 versus 0.078 h−1) and biomass yield (20.5 versus 8.6 g* mol−1 lactate) increased compared to anaerobic conditions. Proteome analysis revealed that the abundance of proteins involved in the aerobic and anaerobic electron transport chains and major metabolic pathways did not significantly differ between anaerobic and microaerobic conditions. This implicates that P. freudenreichii is prepared for utilizing O2 when it comes available in anaerobic conditions. The ecological niche of propionic acid bacteria can conceivably be extended to environments with oxygen gradients from oxic to anoxic, so‐called microoxic environments, as found in the rumen, gut and soils, where they can thrive by utilizing low concentrations of oxygen.

Highlights

Propionic acid bacteria (PAB) are Gram-positive, nonspore-forming bacteria belonging to the group of actinobacteria with a high GC content (53%–68%) (Poonam et al, 2012)
In aerobic shaken conditions the increased oxygen levels resulted in lower biomass production of the selected P. freudenreichii subsp. freudenreichii and P. freudenreichii subsp. shermanii strains compared to anaerobic conditions
Several A. acidipropionici, A. thoenii and A. jensenii strains were able to produce similar or higher biomass compared to anaerobic conditions and are more tolerant to higher oxygen levels

Summary

Introduction

Propionic acid bacteria (PAB) are Gram-positive, nonspore-forming bacteria belonging to the group of actinobacteria with a high GC content (53%–68%) (Poonam et al, 2012). PAB can be found in a large variety of environments, ranging from the deepest cave of the world (Kieraite-Aleksandrova et al, 2015), soil (Hayashi and Furusaka, 1979), silage (Merry and Davies, 1999), human skin (Perry and Lambert, 2006) and other tissue (Perry and Lambert, 2011), cheese (Britz and Riedel, 1994) and the rumen of animals (Bryant, 1959) This variety of environments points to versatility in metabolic traits of which the repertoire can be extended by the capacity to use a range of terminal electron acceptors. The relationship of various species of PAB with oxygen is complex and requires further study

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