Aerobic metabolism in the genusLactobacillus: impact on stress response and potential applications in the food industry

Abstract

SummaryThis review outlines the recent advances in the knowledge on aerobic and respiratory growth of lactic acid bacteria, focusing on the features of respiration-competent lactobacilli. The species of the genus Lactobacillus have been traditionally classified as oxygen-tolerant anaerobes, but it has been demonstrated that several strains are able to use oxygen as a substrate in reactions mediated by flavin oxidases and, in some cases, to synthesize a minimal respiratory chain. The occurrence of genes related to aerobic and respiratory metabolism and to oxidative stress response apparently correlates with the taxonomic position of lactobacilli. Members of the ecologically versatile Lactobacillus casei, L. plantarum and L. sakei groups are apparently best equipped to deal with aerobic/respiratory growth. The shift from anaerobic growth to aerobic (oxygen) and/or respiratory promoting (oxygen, exogenous haem and menaquinone) conditions offers physiological advantages and affects the pattern of metabolite production in several species. Even if this does not result in dramatic increases in biomass production and growth rate, cells grown in these conditions have improved tolerance to heat and oxidative stresses. An overview of benefits and of the potential applications of Lactobacillus cultures grown under aerobic or respiratory conditions is also discussed.

Oxygen-Inducible Conversion of Lactate to Acetate in Heterofermentative Lactobacillus brevis ATCC 367

“…We found that PDH played the predominant role in the aerobic conversion of pyruvate to acetate and POX had a secondary role. L. brevis, having both functional PDH and POX under aerobic conditions, was different from the other lactobacilli reported previously (20).…”

“…The extra energy provided in aerobic growth might be produced in three ways, as follows. (i) Oxygen repressed the expression of alcohol dehydrogenase (20) and thus shifted ethanol production to acetate. (ii) When glucose levels were substantial, pyruvate was channeled to acetyl-CoA followed by acetate production, instead of reduction of pyruvate to lactate (23,24).…”

“…Moreover, to maintain the intracellular redox balance, oxygen was used as an electron acceptor to regenerate NAD ϩ through NADH oxidase, which had a higher affinity for NADH than did lactate dehydrogenase and alcohol dehydrogenase (26)(27)(28). In these three pathways, acetate resulted from dephosphorylation of acetyl-P i by the action of acetate kinase (AK), accompanied by ATP generation (20). Our data demonstrated that, under aerobic conditions, L. brevis ATCC 367 converted part of pyruvate to acetate in the logarithmic growth phase when glucose was present ( Fig.…”

“…Similar aerobic acetate formation was observed in heterofermentative Lactobacillus spicheri (19). However, genomic evidence indicates that Lactobacillus reuteri and Lactobacillus fermentum lack the lox and pox genes, and their aerobic pyruvate conversion pathways are under investigation (19,20). Metabolic net prediction indicates that pyruvate dehydrogenase (PDH) might be an alternative to POX for aerobic pyruvate-acetate conversion in LAB.…”

“…However, the implication of PDH under aerobic conditions remains controversial, because several researchers reported that the pdh gene was transcriptionally activated when oxygen was present but others reported the opposite results (19,21,22). Therefore, it is now thought that most industrially relevant lactobacilli can use the POX pathway (20), but PDH effects on aerobic acetate production are inconclusive for lactobacilli.…”