Abstract
Besides intrinsic and extrinsic factors such as antagonism for organic substrates or temperature, the storage atmosphere of meat has a high influence on the development of its initial microbiota. Specific modified atmospheres (MAs) selectively suppress growth of aerobic and anaerobic bacteria, thus reshaping the initial microbiota. As some microorganisms are more tolerant to MA, they overgrow competitors and produce metabolites that cause rejection of the product. In order to elucidate responses to different MA by means of metabolic adaptation and competition for organic substrates on meat, the typical representative meat spoilage bacteria Brochothrix (B.) thermosphacta TMW2.2101 and four lactic acid bacteria Carnobacterium (C.) divergens TMW2.1577, C. maltaromaticum TMW2.1581, Leuconostoc (L.) gelidum subsp. gelidum TMW2.1618 and L. gelidum subsp. gasicomitatum TMW2.1619 were chosen. Bacteria were grown in sterile glass bottles filled with a meat simulation medium, which was aerated constantly with either air, 100%_N2, 30%_CO2/70%_O2 or 30%_CO2/70%_N2. Growth of bacteria during incubation at 25°C and stirring at 120 rpm was monitored over 48 h and a label-free quantitative mass spectrometric approach was employed to determine changes within the bacterial proteomes in response to oxygen and carbon dioxide. Both Leuconostoc subsp. were intrinsically tolerant to MA, exhibiting no proteomic regulation of enzymes, whereas the other species provide a set of metabolic adaptation mechanism, enabling higher resistance to the detrimental effects of MA. Those mechanisms comprise: enhanced oxidative stress reduction, adjustment of the pyruvate metabolism and catabolic oxygen consumption in response to oxygen and intracellular pH homeostasis, maintenance of osmotic balance and alteration of the fatty acid composition in response to carbon dioxide. We further evaluated the potential of industrial used MA to inhibit specific bacterial spoilage. No bacterial inhibition is predicted for 30%_CO2/70%_O2 for the analyzed species, whereas 30%_CO2/70%_N2 predictively inhibits C. divergens TMW21577 and B. thermosphacta TMW2.2101. Furthermore, species-specific metabolic pathways enabling different and preferential carbon source utilization were identified, which enable non-competitive coexistence of respective bacteria on meat, resulting in synergistic spoilage. In conclusion, this study gives mechanistically explanations of their acknowledged status as typical spoilage organisms on MAP meats.
Highlights
Food packaging under different modified atmospheres (MAs) has become a common method to counteract deteriorative effects of long time storage of meat, e.g., discoloration and formation of off-odors (Yam et al, 2005; McMillin, 2008)
We demonstrated that different spoilers encode for different metabolic pathways to cope with the detrimental effects of oxygen and carbon dioxide on their metabolism
By controlled regulation of those metabolic pathways, bacteria developed strategies to cope with high oxygen amounts, e.g., consumption of oxygen, reduction of oxidative stress or regulation of oxygen sensitive enzymes as well as high amounts of carbon dioxide, e.g., maintenance of intracellular pH, maintenance of osmotic balance and adaptation of the cell membrane by altering the fatty acid composition
Summary
Food packaging under different modified atmospheres (MAs) has become a common method to counteract deteriorative effects of long time storage of meat, e.g., discoloration and formation of off-odors (Yam et al, 2005; McMillin, 2008) These effects are due to growth of spoilage microorganisms, found as initial contaminations on meat. Those bacteria grow concomitantly upon MAP meat and induce spoilage They are called ephemeral spoilage organisms (ESOs) as described in previous studies of Nychas et al (2008) and comprise lactic acid bacteria (LAB), Brochothrix (B.) thermosphacta, Pseudomonas species, Enterobacterales and Shewanella and Aeromonas species (Lambert et al, 1991; Borch et al, 1996; Ercolini et al, 2006; Nychas et al, 2007; Höll et al, 2016; Hilgarth et al, 2018). As their growth rate and metabolism differs depending on the MA, shelf life can be extended and the sensorial changes can be different (Kakouri and Nychas, 1994; Esmer et al, 2011; Degirmencioglu et al, 2012)
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