Effects of microbiota dynamics on the color stability of chilled beef steaks stored in high oxygen and carbon monoxide packaging
Graphical abstract
Introduction
Meat color is an important estimate of meat freshness and wholesomeness, which directly determines consumer’s purchase decisions, and any deviation from a bright-red color often leads to discounting of meat (Mancini & Hunt, 2005). Modified atmosphere packaging (MAP) is now widely employed to ensure chilled fresh meats have an attractive appearance, where high-oxygen MAP (HiOx-MAP) containing 80% O2 and 20% CO2, or carbon monoxide MAP (CO-MAP) with 0.4% CO, 30% CO2, and 69.6% N2 are two common MAP types used in the meat industry.
To extend the color shelf-life of meat and avoid the drawbacks of aerobic packaging, an anaerobic CO-MAP technology has been approved in the U.S., Canada, Australia and New Zealand, while the EU member states ban it from food processing (Djenane & Roncalés, 2018). Although carboxymyoglobin (COMb) formed in CO-MAP steaks is more stable than oxymyoglobin (OxyMb) formed in HiOx-MAP steaks, the resistance to brown metmyoglobin (MetMb) formation and thus color stability for both MAP steaks is still dependent on oxygen consumption (OC) and metmyoglobin reducing activity (MRA; Hunt et al., 2004, English et al., 2016). In practice, both OC and MRA are influenced by different microbes (Faustman et al., 1990, Motoyama et al., 2010), so their growth will directly affect the meat color.
Previous studies that explored bacteria-mediated meat discoloration mainly focused on the effects of one individual bacterial species by inoculating them on sterile meat under normal atmosphere (Bala et al., 1977, Faustman et al., 1990, Chan et al., 1998, Motoyama et al., 2010). However, the deteriorative phenomenon of microbial spoilage is known as a result of microbiota development represented by more than one microorganism, and their interactions among species are important for this process (Zagorec & Champomier-Vergès, 2017). Different packaging conditions will induce meat microbes to undergo distinct ecological successions, and these specific microbiota dynamics in turn affect their living environment, resulting in the organoleptic onset of perceptible spoilage (Mansur et al., 2019, Hilgarth et al., 2018). To our knowledge, few have characterized the influence that entire microbial communities have on meat color under both HiOx-MAP and CO-MAP.
The browning reason for HiOx-MAP beef has been commonly explained by lipid and protein oxidation (Yang et al., 2016), whereas microbiota influences during meat discoloration in this packaging have received little attention. Microbial spoilage of meat with appearance defects (e.g., discoloration, off-odor, gas or slime production) depends on the combination of different microbes and their biological activities, which may interact and render the meat unacceptable for consumers (Comi, 2017, Nychas et al., 2008). High-throughput DNA sequencing (HTS) can provide a comprehensive view of bacterial ecology in meat, and predict bacterial metabolic functions associated with the observed microbiota changes as well (Langille et al., 2013). Therefore, the HTS technique is essential to improve our knowledge about meat discoloration caused by microbiota dynamics, and investigate several potential microbial metabolic pathways that may affect meat color under modified atmospheres.
This study aimed to establish the inter-relationships between microbiota successions and color changes during the chilled storage of HiOx-MAP and CO-MAP beef steaks. Moreover, the predictive functional information regarding microbial communities under both MAP types was also gathered to further understand the underlying mechanisms for microbial-induced discoloration of packaged meats.
Section snippets
Meat materials
The longissimus lumborum muscles were collected from four Chinese Luxi yellow cattle (24–26 months old, 607–689 kg live weight). Diets were based on Chinese feeding standards for beef cattle (NY/T815-2004). The left and right loins from all carcasses were obtained after conventional chilling for 48 h (2–4 °C). The muscles were vacuum packaged, and transported to the lab on ice within 2 h. In the lab, muscles were cut into 2.54 cm thick steaks, and then steaks were packaged in both MAP
Bacterial enumeration
Packaging and storage time interacted to influence TVC, Pseudomonas spp. and B. thermosphacta counts (P < 0.05). Compared with CO-MAP steaks, HiOx-MAP steaks exhibited higher (P < 0.05) TVC from day 15 and reached the spoilage threshold of 7 log CFU/g at day 20, indicating that the steaks were considered as microbiologically spoiled on this day (ICMSF, 1986; Fig. 1a). Bevilacqua and Zaritzky (1986) suggested that oxygen consumption by bacterial populations at 7 log CFU/cm2 enhanced pigment
Conclusions
Our results support the importance of microbiota dynamics in affecting meat color and color stability during HiOx-MAP and CO-MAP storage. B. thermosphacta and Pseudomonas spp. were predominant during HiOx-MAP storage. However, Pseudomonas spp. gradually prevailed over other bacteria from day 10, and promoted meat discoloration through elevating OCR. Regarding CO-MAP, Vagococcus spp., and LAB including Leuconostoc spp., Lactobacillus spp. and Lactococcus spp. dominated alternately from day 10,
CRediT authorship contribution statement
Xiaoyin Yang: Conceptualization, Investigation, Formal analysis, Data curation, Writing - original draft. Xin Luo: Methodology, Resources, Supervision. Yimin Zhang: Investigation, Data curation. David L. Hopkins: Supervision, Writing - review & editing. Rongrong Liang: Writing - review & editing. Pengcheng Dong: Formal analysis, Data curation. Lixian Zhu: Methodology, Supervision.
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
This work was supported by the earmarked fund for China Agriculture Research System-beef (CARS-37), special fund for Innovation Team of Modern Agricultural Industrial Technology System in Shandong Province (SDAIT-09-09), and the projects of National Natural Science Foundation of China (31901757) and National Natural Science Foundation of China (31871731).
References (49)
Metabolic pathways: Release of energy (Aerobic)
- et al.
Prevalence and antimicrobial susceptibility of Acinetobacter spp. isolated from meat
International Journal of Food Microbiology
(2017) - et al.
Bacterial populations and the volatilome associated to meat spoilage
Food Microbiology
(2015) - et al.
Effect of Pseudomonas fluorescens on beef discoloration and oxymyoglobin oxidation in vitro
Journal of Food Protection
(1998) Spoilage of meat and fish
- et al.
Influence of dissolved carbon dioxide on the growth of spoilage bacteria
LWT-Food Science and Technology
(2000) Brochothrix
- et al.
Shelf life extension of lamb meat using thyme or oregano essential oils and modified atmosphere packaging
Meat Science
(2011) - et al.
Formation of red myoglobin derivatives and inhibition of spoilage bacteria in raw meat batters by lactic acid bacteria and Staphylococcus xylosus
LWT-Food Science and Technology
(2016) - et al.
Current research in meat color
Meat Science
(2005)
Comparative evaluation of spoilage-related bacterial diversity and metabolite profiles in chilled beef stored under air and vacuum packaging
Food Microbiology
Effects of malate, lactate, and pyruvate on myoglobin redox stability in homogenates of three bovine muscles
Meat Science
Pseudomonas spp. convert metmyoglobin into deoxymyoglobin
Meat Science
Meat spoilage during distribution
Meat Science
Predominant enterobacteria on modified-atmosphere packaged meat and poultry
Food Microbiology
Evaluation of the spoilage potential of bacteria isolated from chilled chicken in vitro and in situ
Food Microbiology
Microbiological condition of retail beef steaks: A Canadian survey
Journal of Food Research
Effect of packaging atmospheres on storage quality characteristics of heavily marbled beef longissimus steaks
Meat Science
Meat microbiology and spoilage
Effect of Pseudomonas fragi on the color of beef
Journal of Food Science
Rate of pigment modifications in packaged refrigerated beef using reflectance spectrophotometry
Journal of Food Processing and Preservation
QIIME allows analysis of high-throughput community sequencing data
Nature Methods
Cited by (22)
Shelf-life extension of chilled and superchilled dark-cutting beef held under combined anoxic master packaging and high-oxygen packaging both enriched with carbon dioxide
2022, Food Packaging and Shelf LifeCitation Excerpt :Counts were expressed as logarithms of the number of colony-forming units per gram (log CFU/g). Bacterial communities were investigated using the MiSeq Illumina Sequencing Platform during storage and display, as described by Yang et al. (2020). Briefly, the bacterial total DNA was extracted using a GenElute™ Bacterial DNA Kit (Sigma Aldrich, St. Louis, MO), and the DNA concentration was determined using a NanoDrop 1000 (Thermo Fisher Scientific, Waltham, MA).