Effects of microbiota dynamics on the color stability of chilled beef steaks stored in high oxygen and carbon monoxide packaging

Highlights

• HiOx-MAP aggravated microbial-induced meat discoloration compared to CO-MAP.

• B. thermosphacta and Pseudomonas dominated in HiOx-MAP, but the latter prevailed.

• Pseudomonas enhanced beef discoloration by elevating OCR in HiOx-MAP.

• The dominated LAB (Lactobacillus & Lactococcus) in CO-MAP improved beef color.

Abstract

The microbiota influence on meat color stability of chilled beef steaks under two modified atmosphere packaging (MAP) systems was studied: HiOx-MAP (80% O₂/20% CO₂) and CO-MAP (0.4% CO/30% CO₂/69.6% N₂). Steaks were stored for up to 20 days at 2 °C. Headspace gas composition and color stability were evaluated. High-throughput sequencing analyses were performed to characterize bacterial community dynamics. For HiOx-MAP steaks, Pseudomonas spp. became the dominant species, and an increased oxygen consumption caused by these bacteria contributed to metmyoglobin (MetMb) formation from day 10. Functional analysis based on 16S rDNA sequencing predicted higher abundance of genes related to amino acid and lipid metabolism in HiOx-MAP bacterial communities compared to CO-MAP bacterial communities, which probably accelerated meat discoloration. Lactic acid bacteria dominated in CO-MAP steaks, in which Lactobacillus spp. and Lactococcus spp. contributed to improve redness and chroma, and reduce MetMb%, respectively. These findings help our understanding of color stability in CO-MAP steaks in comparison to HiOx-MAP steaks as influenced by the microbial community.

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.