What Bacteria Is in Salami What Bacteria Is in Aged Beef
Foods. 2020 Nov; ix(11): 1571.
Molecular Characterization of Microbial and Fungal Communities on Dry-Aged Beef of Hanwoo Using Metagenomic Analysis
Minhye Shin
2Section of Agricultural Biotechnology and Research Establish of Agriculture and Life Scientific discipline, Seoul National University, Seoul 08826, Korea; moc.liamg@10pgsla
Soohyun Cho
3Animal Products and Utilization Division, National Institute of Animal Science, Rural Evolution Administration, Wanju 55365, Korea; rk.aerok@5190chs
Younghoon Kim
2Section of Agricultural Biotechnology and Research Found of Agronomics and Life Science, Seoul National University, Seoul 08826, Korea; moc.liamg@10pgsla
Sangnam Oh
4Department of Functional Food and Biotechnology, Jeonju University, Jeonju 55069, Korea
Received 2020 Sep 22; Accepted 2020 Oct 27.
Abstract
Dry out aging has been widely applied for the aging of meat to produce a unique flavor and tenderness of meat. A number of microorganisms are present, forming a community with interactions that affect the meat aging process. However, their comprehensive compositions are nonetheless not well understood. In this study, we analyzed longitudinal changes in microbial and fungal communities in dry out-aged beef using a metagenomic platform. 16S rRNA sequencing revealed that dry out aging led to an increase in bacterial diversity, and Actinobacteria and Firmicutes, which are more often than not lactic acrid bacteria, were dominant on dry-anile beef. However, prolonged dry aging reduced the diversity of lactic acrid bacteria. Sequencing of the internal transcribed spacer (ITS) region showed that fungal diversity was reduced by crumbling and that Helicostylum sp. was the almost mutual species. These results propose that there are various microorganisms on dry-aged beef that interrelate with each other and bear on meat quality. Understanding microbial characteristics during the aging process will help to enhance beefiness quality and functional effects.
Keywords: microbiome, mycobiome, dry aging, lactic acrid bacteria
1. Introduction
In the last two decades, in that location has been a shift in the consumer lifestyle and eating habits, with a preference for high food quality and premium foods with essential nutrients [1]. With respect to high food quality, there are representative methods for improving the palatability and flavour of beef, including salting, curing, smoking and crumbling [2,3,4,5]. Among them, beef crumbling has been of the utmost interest recently for a wider array of purveyors and retail consumers in the United States and Commonwealth of australia and is condign more pop in Asian countries [vi].
Beefiness aging is a process of storing meat at refrigerated temperatures to enhance tenderness and flavor. In general, in that location are two forms of beefiness crumbling techniques: wet and dry, depending on the degree of aridity in the meat [6]. Wet crumbling is a technique for aging meats in a vacuum-sealed bag to retain wet, while dry-aged beef is unpackaged and left to age for several weeks. Compared to wet aging, dry crumbling creates a greater concentration of flavor and forms an external crust with sure microbial species on the meat surface [vi]. This procedure provides the unique season of dry out-aged beef and maximizes palatability [7].
Dry aging involves the growth of various microorganisms on the beefiness surface, affecting beef quality through their proteolytic and lipolytic activities as well equally their metabolic products [8,nine]. Although limited studies are available on the effect of microorganisms on dry out crumbling, a few leaner and yeasts/molds have been reported to be present on dry out-anile beef. Yeasts and molds, including Thamnidium sp., Pilaira anomala and Debaryomyces hansenii, are often detected in dry-aged beef, which direct affects beefiness quality by releasing proteases, breaking down myofibrils with collagenolytic enzymes, and producing season compounds [five,10]. In contrast to fungal composition, well-nigh bacterial analyses take focused on the reduction of pathogenic leaner, such equally generic Escherichia coli, coliforms, Eastward. coli O157:H7, Listeria monocytogenes and Salmonella sp., during the procedure of dry out crumbling [11,12,13]. Recently, nosotros reported that lactic acrid bacteria were significantly increased during all dry crumbling periods, and culturomic analysis at the fungal level showed the presence of Penicillium camemberti and D. hansenii [xiv]. However, despite the current findings, at that place is however a lack of comprehensive understanding and analysis of the microbial effects on dry aging. In particular, to date, there is very piffling data on the bacterial and fungal variety, characteristics, and safety of dry out-aged beef.
In recent decades, culture-contained methods based on metagenomics analysis have been applied to elucidate the genomic label of the microbiome associated with food and meat sciences [5,xv,16]. In this study, we aimed to identify the diversity and characteristics of microorganisms on the surface of dry out-aged beef based on a metagenomics platform. We compared microbial and mycobial compositions using 16S- and internal transcribed spacer (ITS)-based amplicon sequencing in dry-aged beef at different aging periods. Our results suggested that a number of microbial and fungal communities were present on dry-anile beef, interrelating with each other and affecting the aging procedure.
two. Materials and Methods
2.i. Dry Aging of Beef and Sample Collection
8 carcasses (1st form Hanwoo cattle) were selected and anile at 1–4 °C and a relative humidity of 80–90% until 160 days after slaughter. At 12-, 30-, 70- and 160-days postmortem during crumbling, a single 5.0-cm-thick longissimus thoracis and biceps femoris section was taken from the surface of each carcass. Samples from the dry out-anile beef were transported to the laboratory at 4 °C inside iii h later beingness cut, without being vacuum packed.
ii.2. DNA Preparation and Sequencing
Ten grams of surface samples were homogenized in 90 mL of Ringer's solution (Oxoid, Basingstoke, UK), and 1 mL aliquot of the homogenate was centrifuged at ten,000× one thousand for 5 min. The pellet containing microorganisms was nerveless, followed by DNA extraction using the Powerfood Microbial Dna Isolation kit (Mo Bio Laboratories, Inc., Carlsbad, CA, USA) according to the manufacturer'due south instructions. Each DNA sample was adjusted to a concentration of 1 ng/µL and subjected to PCR according to the 16S Metagenomic Sequencing Library protocols (Illumina, San Diego, CA, Us). The V4 region of the 16S rRNA genes (primer ready: forward, 5′-CCT ACG GGN GGC WGC AG-3′; reverse, v′-GAC TAC HVG GGT ATC TAA TCC-three′) and the ITS region (primer set: forward, five′-TCG TCG GCA GCG TCA GAT GTG TAT AAG AGA CAG GCA TCG ATG AAG AAC GCA GC-3′; reverse, 5′-GTC TCG TGG GCT CGG AGA TGT GTA TAA GAG ACA GTC CTC CGC TTA TTG ATA TGC-3′) were analyzed using the Illumina MiSeq platform (Illumina, San Diego, CA, The states). Subsequently measuring the concentration of the index PCR products using PicoGreen (Invitrogen, Carlsbad, CA, USA), equimolar PCR amplicons were pooled and sequenced using the MiSeq®Reagent Kit v3 (600 cycles) for 301 paired-terminate bases, post-obit the manufacturer's protocol based on the MiSeq organisation platform (Macrogen, Seoul, Republic of korea). The sequencing issue was received in the format of a fastq file.
ii.three. Metagenomic Analysis
Fastq files obtained from MiSeq paired-finish sequencing data were analyzed using the Mothur (v. ane.41). In Mothur, reads were merged using the make.contig control and quality-filtered by the screen.seqs control. We aligned the sequences to the SILVA database v. 138 and the chimeric sequences were removed using the VSEARCH program v2.eleven.1 [17]. Taxonomic classification was analyzed using the Greengenes-formatted database xiv released in 2013 and and then Chloroplast, Archaea, Mitochondria, and Eukaryota sequences were removed from the dataset. Depression abundance operational taxonomical units and singletons were removed using the Mothur subroutine "divide.abund", and operational taxonomic units (OTUs) were classified using the altitude 0.03 adding (97% sequence similarity). Rarefaction curves were calculated using Mothur and the OTU and taxonomy tabular array from Mothur were further analyzed on the R platform 5. 3.6.two using the Phyloseq and Vegan packages. Plots were generated using GraphPad Prism 8.0 (San Diego, CA, The states).
two.4. Statistical Assay
All statistical tests were performed using R software (http://world wide web.r-project.org/) to evaluate diversity. The α-diversity indices (Shannon index, Chao1, and Simpson index) were calculated using the vegan package. Taxonomic profiles were used to deport principal component analysis (PCA) which was performed on log-transformed data using the ADE4 package to analyze the distance matrices for visualization and they plotted against each other to compile the microbiota compositional differences between samples.
3. Results
3.ane. Dry Aging Leads to Changes in Species Diversity in Beef
The dry aging process involves the growth of diverse microorganisms on the beef surface with interactions between species. To compare compositional changes of microorganisms with meat ripening in dry-aged beefiness, we conducted next-generation sequencing of bacterial 16S rRNA and ITS sequencing. We selected incubation periods of 12, xxx, 70 and 160 days, as numerous researchers have reported the most frequent range for dry-aged beefiness every bit between 14 and 40 days [6]. Initially, a total of 1,567,714 and one,147,534 reads were obtained for 16S and ITS sequences, respectively. The mean number of effective reads per sample was 368,560 and 265,564 for 16S and ITS sequences, respectively, subsequently removing adapter sequences. The ratio of reads that had a phred quality score over 30 (Q30%) ranged from 62.two% to 68.6%. The total assembled sequencing of 16S and ITS sequences came in 874,298 and 875,878, respectively. The filtered read counts of clustering with 97% similarity were 172,274 and 645,514 for 16S and ITS sequences, respectively.
Species richness represents the number of different species in a sample. The rarefaction measure of bacterial 16S rRNA sequencing was lowest at day 12 and increased during the process of beef aging (Figure 1). However, the fungal mycobiome profile did non show a significant trend with time of aging. Nosotros next evaluated species diverseness, represented by Chao1, Shannon, and Simpson indices, which show how evenly the microbes are distributed in a sample. As shown in Figure 2, all iii bacterial species diversity estimates were lowest at day 12 and increased as the aging process continued. In contrast, fungal species variety indices indicated notably high fungal diversity at twenty-four hours 12, but relevant changes past time were not establish. At that place was a big divergence amid the fungal species richness estimators between Shannon/Simpson and Chao1, possibly because the Chao richness computer gives more weight to the low-affluence species, skewing the data sets toward the depression-abundance species [18]. These results propose that dry crumbling led to bacterial species diversity, while fungal species were influenced differentially during the process.
Rarefaction plots of the microbial (A) and mycobial (B) communities on the surface of dry out-anile beef with respect to the aging periods. Rarefaction curves brandish the number of operational taxonomic units (OTUs) detected based on the sampling intensity of the libraries. ●, mean solar day 12; ▲, solar day 30; ♦, 24-hour interval 70; and ●, day 160.
Alpha-variety indices of the microbial (A–C) and mycobial (D–F) communities on the surface of dry-anile beef with respect to the aging periods. Alpha-multifariousness indices are composite indices reflecting abundance and consistency measured on the basis of Shannon, Chao1, and Simpson indices.
Principal component and nomenclature analysis were conducted to compute the principal components based on the correlation matrix and visualize the classification of variables and cases (Figure iii). We compared the datasets and confirmed that each grouping was composed of a distinct microbial species. The fungal communities of dry-anile beef at 24-hour interval lxx and twenty-four hours 160 were more similar than those at the earlier stages of crumbling. Various species of Lactobacillus and Mucoraceae family strains were major determinants of the classification for the microbiome and fungal mycobiome, respectively. Overall, metagenomic analysis results showed a complex interrelation of the microbiome and mycobiome with respect to the dry out crumbling procedure.
Plots of principal component and classification analysis based on cases (A,C) and variables (B,D). Taxonomy affluence counts of the microbial (A,B) and mycobial (C,D) communities on the surface of dry out-aged beefiness with respect to the aging periods were projected into master components based on the correlation matrix. Notable bacterial species on the factor coordinates are indicated (B,D). ●, solar day 12; ▲, 24-hour interval xxx; ♦, day 70; and ●, mean solar day 160.
3.2. Dry Aging Alters Microbial Compositions in Beef
In our previous study, nosotros reported that lactic acid bacteria were significantly increased for fifty days during all dry crumbling periods [14]. However, there is no information on the individual strain composition of microorganisms in dry-aged beefiness later on 60 days of incubation. Here, we demonstrated the taxonomic limerick of the microbiome and mycobiome at the phylum and genus levels by dry crumbling periods.
At the phylum level, Firmicutes were well-nigh ascendant in all fourth dimension periods (Figure 4). The relative abundances of the following 2 phyla, Actinobacteria and Bacteroidetes, were high only dependent on each period, and dry out-aged beefiness at day seventy had higher Actinobacteria and Bacteroidetes than other time periods. Information technology is noted that the abundance of Blue-green alga was high only at twenty-four hours 12.
Relative abundance (%) plots of the microbial communities on the surface of dry-aged beef with respect to the aging periods. The top ten most abundant bacteria at the phylum level (A) and genus level (B) are represented, and the balance of the bacteria were pooled in the 'others' category.
At the genus level, well-known lactic acid bacteria, including Lactobacillus, Bifidobacterium, and Streptococcus, were the most arable bacterial strains. At days 12 and 30, the lactic acid bacteria composition was more than 50% of the total detected bacterial abundance, but it decreased with the ripening process. Pseudomonas sp., peculiarly Pseudomonas psychrophila, was present at high levels at solar day xxx and day 160 and is considered a pathogenic bacterium causing the deterioration of beef and failure of dry aging. Prevotella, known to mainly inhabit the man gut, was present at lower levels on twenty-four hour period 12 only increased during aging. The existence of food-borne pathogens, including Bacillus cereus, Staphylococcus aureus, Listeria monocytogenes, or Escherichia coli, was not detected. From these results, we speculate that Firmicutes, including lactic acrid bacteria, are dominant at the beginning of dry aging only reduced by time interacting with other bacterial species.
3.3. Dry out Aging Alters Fungal Compositions in Beefiness
The dry aging process encourages the growth of beneficial molds [half-dozen]. Thamnidium sp. and D. hansenii are common microorganisms constitute in dry out-aged beefiness, while potentially harmful yeasts and molds such as Candida sp., Cladosporium sp., and Rhodotorula sp. are sometimes detected [five]. In the current study, fungal mycobial community analysis showed that Ascomycota and Zygomycota phyla were the dominant taxa in dry out-aged beefiness (Figure 5). In detail, Zygomycota was prevalent at day 30 and day 160. The relative abundance of the Basidiomycota phylum decreased with aging fourth dimension. Combined with the taxonomic fungal composition at the genus level, most of the Zygomycota phylum was composed of Helicostylum sp. (33, 86, 33 and 91% at day 12, xxx, 70 and 160, respectively), which is a genus in the family Mucoraceae, but its biological activeness is unknown. On day 12, Mucor sp. and Malassezia sp. were nowadays, merely their composition decreased as aging progressed. Cryptococcus sp., which is an invasive fungus causing cryptococcosis and mostly found in soil, was detected but at day 50. Collectively, fungal communities on dry-aged beef were dominated past Zygomycota, specifically Helicostylum sp., and their compositional changes were differentially influenced by the crumbling procedure compared to the microbial communities.
Relative abundance (%) plots of the mycobial communities on the surface of dry out anile beef with respect to the crumbling periods. The top ten most abundant fungi at the phylum level (A) and genus level (B) are represented, and the residual of the fungal strains were pooled in the 'others' category.
three.4. Prolonged Dry Aging Reduces the Composition of Lactic acid Bacteria
Lactic acid leaner role in the preservation of the beef product through the generation of lactic acrid during metabolic changes and contest with pathogenic microorganisms [19]. To investigate alteration of the lactic acid bacterial composition in dry-aged beef during maturation, we compared the relative abundance of total lactic acrid bacterial strains consisting of four families, Bifidobacteriaceae, Lactobacillaceae, Leuconostocaceae, and Streptococcaceae.
At day 12, the bacterial family unit composition occupied 80.sixteen% of the total bacterial species merely gradually decreased to 43.78% at day 160. Each bacterial family composition was unlike amidst the crumbling periods. For example, Lactobacillaceae was the nearly prevalent family at solar day 12 and 24-hour interval 30, while Bifidobacteriaceae was dominant at day 70. As shown in Effigy six and Figure vii, Bifidobacterium breve and Bifidobacterium longum were more arable in the day lxx sample, but Lactobacillus paracasei and Lactobacillus plantarum were more abundant on days 12 and 30. This outcome implies that relatively aerobic Lactobacillaceae would exist during the earlier period of dry crumbling and then alternate with anaerobic bifidobacterial strains as oxygen availability decreased.
Relative abundance (%) plots of lactic acid bacteria on the surface of dry-anile beefiness with respect to the aging periods. A full of 36 lactic acid bacterial species (A) were detected, including families of Bifidobacteriaceae, Lactobacillaceae, and Streptococcaceae (B). Major species with high relative affluence are indicated in (A).
Heatmap of lactic acid bacterial abundance on the surface of dry-aged beef with respect to the aging periods. The blue–white colour organisation was used to represent the relative affluence of each bacterial strain belonging to the families Bifidobacteriaceae, Lactobacillaceae, and Streptococcaceae. Inset: relative abundance (%) of the most dominant lactic acid bacterial species on dry out-aged beefiness.
4. Word
Dry aging is a process of storing meat at refrigerated temperatures, and diverse microorganisms are involved in enhancing the meat aging process. In this study, we compared microbial and mycobial compositions based on a metagenomics platform in dry-aged beef at different aging periods. Bacterial species multifariousness increased during the process, while fungal diverseness was highest at the offset of aging. At the phylum level, Actinobacteria and Firmicutes, mostly lactic acid bacteria, were dominant simply were reduced in relative affluence by aging. Proteobacteria, by and large Pseudomonas, were detected at day 30 and day 160. The dry aging process also altered fungal composition with Helicostylum sp. as the almost dominant strain, while the relative abundances of Mucor sp. and Malassezia sp. decreased during the aging process.
In the current study, we showed a loftier relative abundance of lactic acid bacteria on dry out-aged beef until 30 days of aging, only their composition decreased as aging proceeded. To date, only a few studies take been associated with lactic acrid bacteria in dry-aged beef. Oh et al. reported increased lactic acrid bacterial composition from approximately log 2 colony forming units (CFU) to log 3 CFU in 7 days of wrap packaging after completion of aging [five]. In the study by Ryu et al., lactic acid bacterial abundance increased to log 6 CFU on the surface of dry-aged beef samples of longissimus thoracis and biceps femoris during aging for 60 days [14]. Lactic acid leaner are frequently practical equally starter cultures in the production of salami, yielding a sour meat scent and oily mouth feel as well as inhibiting pathogenic bacterial growth by bacteriocins [xx,21,22]. Because that the usual dry crumbling menstruation is less than 30 days, lactic acid bacteria would be dominant, conferring benign effects on dry-aged beefiness.
Meat deterioration past pathogenic bacteria is problematic. In the current study, we detected Pseudomonas sp., mostly Pseudomonas psychrophila. The strain is a cold-adaptable facultatively psychrophilic bacterium and can grow at −1 to 35 °C with maximum growth at 25 °C [23,24]. Information technology is a major spoilage organism plant in fish meats or food processing facilities [25,26]. Infection by P. psychrophila could result in the degradation of proteins and the production of volatile nitrogen-based metabolites such every bit putrescine and ammonia [27]. P. psychrophila has never been reported in livestock, but it is possible for the strain to be present on dry out-aged beefiness during the procedure of packaging or storage. Notably, the bacterial strain appeared at mean solar day 30, but its presence was reduced at day seventy, possibly by the interaction with total microbiota in the beef sample, and then appeared again at day 160. To reduce potential infection by the organism, caution is required regarding processing management practices.
Recently, Capouya et al. reported a survey of microbial communities on dry-aged beef processed from commercial dry aging facilities [28]. They institute that the microbial community structures were highly dependent on the processing facilities and may be associated with beneficial enzymatic digestion of the tissue contributing to beef quality. Although their specific microbial and mycobial taxa and distributions were dissimilar from our electric current study, Pseudomonas sp. and Mucor sp. were found to be present in both studies, establishing a general core microbiome for dry-aged beef. It is noted that Lactobacillius genus was also establish in their written report to have a relative affluence of 36.57% in a facility simply less than one% abundance in other locations.
In general, diverse yeasts and molds tin grow on the surface of dry-aged beef, including Thamnidium sp., Pilaira anomala and D. hansenii [5,14]. In this study, we beginning report the presence of Helicostylum sp. based on the metagenomic platform. Information technology was described by Corda in 1842 and has a sporangium without an apophysis, forming globose sporangiola borne on straight or recurved branches and lacking stolons and rhizoids [29]. However, its biological and physiological characteristics are nevertheless unidentified. Interestingly, the social club of Malasseziales, including Malassezia sp., was only detected at the starting time of dry aging. Malassezia is naturally found on the skin surfaces of many animals, sometimes causing hypo- or hyper-pigmentation [thirty]. In a recent paper, the presence of Malassezia was reported in dried carmine snapper during storage for fifty days [31]. It is speculated that the bacteria could exist included from cows or during the training procedure by purveyors, and their composition could be reduced past interacting with microbial communities every bit crumbling proceeds. However, a possible route of contamination needs a more specific investigation.
five. Conclusions
In the nowadays study, we adamant the characteristics of microorganisms on the surface of dry-aged beef based on the metagenomic analysis. Nosotros found the longitudinal changes of microbial and mycobial compositions, including lactic acid bacteria. Overall, the current study conspicuously shows that there are various microorganisms on dry-aged beef interrelating with each other and affecting the meat aging process. Understanding microbial characteristics during aging will aid to enhance beef quality and functional effects.
Author Contributions
Conceptualization, Southward.R., Y.K. and S.O.; methodology, S.R., M.S., Southward.C., I.H., Y.K. and S.O.; validation, Due south.R., Thou.South.; formal analysis, S.R., M.S.; investigation, S.R., Chiliad.South.; information curation, Southward.R., M.S.; writing—original typhoon preparation, S.R., M.S., Y.K. and S.O.; writing—review and editing, S.R., Thousand.South., S.C., I.H., Y.1000. and South.O.; visualization, S.R., M.S.; supervision, Y.Chiliad. and S.O.; projection administration, Y.Yard. and S.O.; funding conquering, Y.K. and Due south.O. All authors take read and agreed to the published version of the manuscript.
Funding
This research was supported past National Research Foundation of Korea (NRF) funded by the Ministry of Scientific discipline, Data and Communications Engineering (ICT) and Futurity Planning (2016M3C1B5907057) and a grant from the Next-Generation BioGreen 21 Program (PJ01322302), Rural Evolution Administration, Korea.
Conflicts of Involvement
The authors declare no conflict of interest.
Footnotes
Publisher's Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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Source: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7693710/
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