Oenococcus oeni, a species born and moulded in wine: a critical review of the stress impacts of wine and the physiological responses

Abstract

Oenococcus oeni is a lactic acid bacterium highly adapted to the stressful environment of wine, and is widely used as an industrial starter culture to conduct malolactic fermentation (MLF), the conversion of L-malate to L-lactate. Some cold-climate wine regions still produce wines which prove too stressful for the application of a starter culture, resulting in sluggish or stuck MLFs which compromise the quality and stability of the wine. The literature on the three primary stress factors, low pH, ethanol and SO 2 , is reviewed as well as their toxic mechanisms; possible interactions between the stress factors are also discussed. In particular, the toxic mechanisms of SO 2 , an extremely inhibitory compound, are poorly understood. in vitro studies as well as in vivo studies in other prokaryotes point to numerous mechanisms which could have widespread impacts on the cell envelope, proteins and DNA in O. oeni. We also review the responses of O. oeni to these stress factors and offer a simplified model of events which cultures inoculated into particularly stressful wines may experience. Although significant advances have been made in our understanding of the stress responses in recent years, many fundamental aspects still require study.

Analysis of Transcriptomic Response to SO2by Oenococcus oeni Growing in Continuous Culture

“…The highest induced and repressed genes, with a log 2 FC of 6.55 and −3.73, correspond to the small heat shock protein Hsp20 and a LysR-type transcriptional regulator (Table S4). Hsp20 (referred to as Hsp18 in several studies) has previously been identified as a response to ethanol and acid stress in O. oeni ( 22 ) and has also been associated with the SO 2 stress response ( 36 ). The involvement of this protein in SO 2 stress is discussed in subsequent sections.…”

“…The toxic mechanisms of SO 2 toward O. oeni are currently unknown; however, modes of action have been suggested, including adduct formation via nucleophilic attack ( 39 ) or, more likely in winemaking environments, oxidative damage through autoxidation of SO 2 and generation of sulfuroxy radicals ( 22 ). Under oxidative stress caused by radicals, proteins containing cysteine and methionine residues are prone to oxidation at their electron-rich sulfur atoms.…”

“…Molecular chaperones play an essential role in the response of LAB against environmental stresses by protecting and refolding proteins, allowing them to continue functioning during exposure to stress ( 46 ). In O. oeni , a small heat shock protein belonging to the Hsp20 family is considered the most important molecular chaperone associated with the response to heat, ethanol, acid, and oxidative stress ( 15 , 22 ). Besides its demonstrated role in protein protection ( 19 , 47 ), studies have shown its involvement in the rigidification of the membrane lipid bilayer after stress-induced fluidization ( 13 , 19 ).…”

“…Lactic acid bacteria can adapt to environmental stress by modulating the flux through alternative pathways for sugar consumption and making use of diverse carbon sources ( 46 ). It is well known that O. oeni relies on pathways, such as MLF and citrate metabolism, to counteract common wine stresses such as low pH and ethanol ( 22 ). However, the adaptations in relation to SO 2 stress are less well understood, with a single study reporting a reduction in the activity of (F 1 F o ) H + -ATPases ( 5 ).…”

“…A role for the molecular chaperone Hsp20 in the SO 2 stress response was also proposed after a weak induction of this gene was observed under high SO 2 conditions ( 21 ). Several mechanisms of action of SO 2 have been hypothesized based on studies investigating other bacterial species, including damage to proteins, cell membranes, and DNA through nucleophilic substitutions and oxidative stress ( 22 ). However, the majority of these studies were conducted at pH values ranging from 5 to 7, which do not resemble the environment encountered by O. oeni in wine or grape juice containing SO 2 .…”