Study of the bacterial diversity of foods: PCR-DGGE versus LH-PCR

Garofalo, Cristiana; Bancalari, Elena; Milanović, Vesna; Cardinali, Federica; Osimani, Andrea; Sardaro, Maria Luisa Savo; Bottari, Benedetta; Bernini, Valentina; Aquilanti, Lucia; Clementi, Francesca; Neviani, Erasmo; Gatti, Monica

doi:10.1016/j.ijfoodmicro.2016.11.008

Cited by 49Probiotics and Fermented FoodsMicrobial Community Ecology and PhysiologyBacterial Identification and Susceptibility Testing

Study of the bacterial diversity of foods: PCR-DGGE versus LH-PCR

Garofalo, Cristiana, Bancalari, Elena, Milanović, Vesna, Cardinali, Federica, Osimani, Andrea, Sardaro, Maria Luisa Savo, Bottari, Benedetta, Bernini, Valentina +4 more·2017·International Journal of Food Microbiology

DOI 10.1016/j.ijfoodmicro.2016.11.008

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Abstract

The present study compared two culture-independent methods, polymerase chain reaction denaturing gradient gel electrophoresis (PCR-DGGE) and length-heterogeneity polymerase chain reaction (LH-PCR), for their ability to reveal food bacterial microbiota. Total microbial DNA and RNA were extracted directly from fourteen fermented and unfermented foods, and domain A of the variable regions V1 and V2 of the 16S rRNA gene was analyzed through LH-PCR and PCR-DGGE. Finally, the outline of these analyses was compared with bacterial viable counts obtained after bacterial growth on suitable selective media. For the majority of the samples, RNA-based PCR-DGGE revealed species that the DNA-based PCR-DGGE was not able to highlight. When analyzing either DNA or RNA, LH-PCR identified several lactic acid bacteria (LAB) and coagulase negative cocci (CCN) species that were not identified by PCR-DGGE. This phenomenon was particularly evident in food samples with viable loads<5.0 Logcfug-1. Furthermore, LH-PCR was able to detect a higher number of peaks in the analyzed food matrices relative to species identified by PCR-DGGE. In light of these findings, it may be suggested that LH-PCR shows greater sensitivity than PCR-DGGE. However, PCR-DGGE detected some other species (LAB included) that were not detected by LH-PCR. Therefore, certain LH-PCR peaks not attributed to known species within the LH-PCR database could be solved by comparing them with species identified by PCR-DGGE. Overall, this study also showed that LH-PCR is a promising method for use in the food microbiology field, indicating the necessity to expand the LH-PCR database, which is based, up to now, mainly on LAB isolates from dairy products.

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PCR-DGGE enables obtaining information on the genotypes of microorganisms based on the analysis of differences in selected parts of the genome.
“PCR and its modification, polymerase chain reaction-denaturing gradient gel electrophoresis (PCR-DGGE), enables obtaining information on the genotypes of microorganisms based on the analysis of differences in selected parts of the genome.”
From Trends in designing microbial silage quality by biotechnological methods using lactic acid bacteria inoculants: a minireview. (2019) · cites this paper as Garofalo et al. 2017
Length heterogeneity PCR (LH-PCR) uses variation in the length of a particular gene between different microbial species to determine how many species may be active in the environment.
“Moreover, length heterogeneity PCR (LH-PCR) uses variation in the length of a particular gene between different microbial species to determine how many species may be active in the environment (Muck 2013; Garofalo et al. 2017).”
From Trends in designing microbial silage quality by biotechnological methods using lactic acid bacteria inoculants: a minireview. (2019) · cites this paper as Garofalo et al. 2017

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Method
Unveiling hákarl: A study of the microbiota of the traditional Icelandic fermented fish
Osimani, A., Ferrocino, I., Agnolucci, M., Cocolin, L., Giovannetti, M., Cristani, C., Palla, M., Milanović, V., Roncolini, A., Sabbatini, R., et al. (2019) · Food Microbiology · doi:10.1016/j.fm.2019.03.027 · Cited by 59 · see citing works
Self-citation
Investigating the core microbiota and its influencing factors in traditional Chinese pickles
An, F., Sun, H., Wu, J., Zhao, C., Li, T., Huang, H., Fang, Q., Mu, E., & Wu, R. (2021) · Food Research International · doi:10.1016/j.foodres.2021.110543 · Cited by 56 · see citing works
Assessment of Spoilage Bacterial Communities in Food Wrap and Modified Atmospheres-Packed Minced Pork Meat Samples by 16S rDNA Metagenetic Analysis
Cauchie, E., Delhalle, L., Taminiau, B., Tahiri, A., Korsak, N., Burteau, S., Fall, P. A., Farnir, F., Baré, G., & Daube, G. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.03074 · Cited by 56 · see citing works
Is there any still undisclosed biodiversity in Ciauscolo salami? A new glance into the microbiota of an artisan production as revealed by high-throughput sequencing
Belleggia, L., Milanović, V., Ferrocino, I., Cocolin, L., Haouet, M. N., Scuota, S., Maoloni, A., Garofalo, C., Cardinali, F., Aquilanti, L., et al. (2020) · Meat Science · doi:10.1016/j.meatsci.2020.108128 · Cited by 53 · see citing works
“…the use of rRNA as an indicator of the metabolic state in microbial assemblages can present some limitations (Blazewicz et al., 2013), the analysis of this nucleic acid is still widely applied to evaluate the metabolically active microbial communities in food matrices (Garofalo et al., 2017).”
Self-citation
Cucumber (Cucumis sativus L.) Seedling Rhizosphere Trichoderma and Fusarium spp. Communities Altered by Vanillic Acid
Chen, S., Yu, H., Zhou, X., & Wu, F. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.02195 · Cited by 52 · see citing works
Physiological responses of Siberian sturgeon (Acipenser baerii) juveniles fed on full-fat insect-based diet in an aquaponic system
Zarantoniello, M., Randazzo, B., Nozzi, V., Truzzi, C., Giorgini, E., Cardinaletti, G., Freddi, L., Ratti, S., Girolametti, F., Osimani, A., et al. (2021) · Scientific Reports · doi:10.1038/s41598-020-80379-x · Cited by 52 · see citing works
Self-citation
Revealing the microbiota of marketed edible insects through PCR-DGGE, metagenomic sequencing and real-time PCR.
Osimani, A., Milanović, V., Garofalo, C., Cardinali, F., Roncolini, A., Sabbatini, R., Filippis, F. D., Ercolini, D., Gabucci, C., Petruzzelli, A., et al. (2018) · Journal of food microbiology · doi:10.1016/j.ijfoodmicro.2018.04.013 · Cited by 44 · see citing works
Self-citation
Microbial dynamics of model Fabriano-like fermented sausages as affected by starter cultures, nitrates and nitrites
Cardinali, F., Milanović, V., Osimani, A., Aquilanti, L., Taccari, M., Garofalo, C., Polverigiani, S., Clementi, F., Franciosi, E., Tuohy, K. M., et al. (2018) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2018.04.032 · Cited by 47 · see citing works
Self-citation
Microbial Ecology of Greek Wheat Sourdoughs, Identified by a Culture-Dependent and a Culture-Independent Approach
Syrokou, M. K., Themeli, C., Paramithiotis, S., Mataragas, M., Bosnea, L. A., Argyri, A. A., Chorianopoulos, N., Skandamis, P. N., & Drosinos, E. H. (2020) · Foods · doi:10.3390/foods9111603 · Cited by 47 · see citing works
“Many authors have already reported the presence of multiband profile for a single microbial species, obtained through PCR-DGGE analysis [8,65].”
Background
Impact of thistle rennet from Carlina acanthifolia All. subsp. acanthifolia on bacterial diversity and dynamics of a specialty Italian raw ewes' milk cheese
Cardinali, F., Osimani, A., Taccari, M., Milanović, V., Garofalo, C., Clementi, F., Polverigiani, S., Zitti, S., Raffaelli, N., Mozzon, M., et al. (2017) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2017.05.018 · Cited by 39 · see citing works
Self-citation
Characterization, High-Density Fermentation, and the Production of a Directed Vat Set Starter of Lactobacilli Used in the Food Industry: A Review
Lu, Y., Xing, S., He, L., Li, C., Wang, X., Zeng, X., & Dai, Y. (2022) · Foods · doi:10.3390/foods11193063 · Cited by 39 · see citing works
The Microbial Diversity of Non-Korean Kimchi as Revealed by Viable Counting and Metataxonomic Sequencing
Maoloni, A., Ferrocino, I., Milanović, V., Cocolin, L., Corvaglia, M. R., Ottaviani, D., Bartolini, C., Talevi, G., Belleggia, L., Cardinali, F., et al. (2020) · Foods · doi:10.3390/foods9111568 · Cited by 30 · see citing works
Self-citation
Kefir: The Champagne of Fermented Beverages
Wyk, J. V. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-815271-3.00012-9 · Cited by 32 · see citing works
Profiling white wine seed vinegar bacterial diversity through viable counting, metagenomic sequencing and PCR-DGGE
Milanović, V., Osimani, A., Garofalo, C., Filippis, F. D., Ercolini, D., Cardinali, F., Taccari, M., Aquilanti, L., & Clementi, F. (2018) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2018.07.022 · Cited by 27 · see citing works
Self-citation
Molecular Phylogeny and Diversity of the Salt-Tolerant Alkaliphilic Actinobacteria Inhabiting Coastal Gujarat, India
Gohel, S. D., & Singh, S. P. (2018) · Geomicrobiology Journal · doi:10.1080/01490451.2018.1471107 · Cited by 26 · see citing works
Isolation of a Lactobacillus paracasei Strain with Probiotic Attributes from Kefir Grains
Plessas, S., Kiousi, D. E., Rathosi, M., Alexopoulos, A., Kourkoutas, Y., Mantzourani, I., Galanis, Α., & Bezirtzoglou, E. (2020) · Biomedicines · doi:10.3390/biomedicines8120594 · Cited by 31 · see citing works
“These effector strains are usually lactic acid bacteria (LAB), and various yeasts [18,19].”
Background
Insight into the bacterial diversity of fermentation woad dye vats as revealed by PCR-DGGE and pyrosequencing
Milanović, V., Osimani, A., Taccari, M., Garofalo, C., Butta, A., Clementi, F., & Aquilanti, L. (2017) · Journal of Industrial Microbiology & Biotechnology · doi:10.1007/s10295-017-1921-4 · Cited by 25 · see citing works
Self-citation
Microbiological characterization of Gioddu, an Italian fermented milk
Maoloni, A., Blaiotta, G., Ferrocino, I., Mangia, N. P., Osimani, A., Milanović, V., Cardinali, F., Cesaro, C., Garofalo, C., Clementi, F., et al. (2020) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2020.108610 · Cited by 25 · see citing works
Self-citation
Microbial and Chemical Changes during Fermentation of Coconut Water Kefir Beverage
Limbad, M., Maddox, N. G., Hamid, N., Kantono, K., Liu, T., & Young, T. (2023) · Applied Sciences · doi:10.3390/app13127257 · Cited by 24 · see citing works
Effects of organic nitrogen addition on soil microbial community assembly patterns in the Sanjiang Plain wetlands, northeastern China
Wang, M., Frey, B., Li, D., Liu, X., Chen, C. R., Liu, Y., Zhang, R., Sui, X., & Li, M. (2024) · Applied Soil Ecology · doi:10.1016/j.apsoil.2024.105685 · Cited by 23 · see citing works
Study of Bacterial Community Composition and Correlation of Environmental Variables in Rambla Salada, a Hypersaline Environment in South-Eastern Spain
Oueriaghli, N., Castro, D. J., Llamas, I., Béjar, V., & Martínez‐Checa, F. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.01377 · Cited by 23 · see citing works
“Nevertheless, in spite of DGGE has significant limitations that should be considered like the possible bias introduced through the DNA extraction, PCR amplification, selection of universal primers and different number of rRNA gene copies (Neufeled and Mohn, 2006) the technique is still used to get an idea of the predo…”
Method
Dietary Fibers and Protective Lactobacilli Drive Burrata Cheese Microbiome
Minervini, F., Conte, A., Nobile, M. A. D., Gobbetti, M., & Angelis, M. D. (2017) · Applied and Environmental Microbiology · doi:10.1128/aem.01494-17 · Cited by 22 · see citing works
“were the only Proteobacteria detected in burrata cheeses (44).”
Background
Microbiota profiles and dynamics in fermented plant‐based products and preliminary assessment of their in vitro gut microbiota modulation
Lavefve, L., Cureau, N., Rodhouse, L., Marasini, D., Walker, L. M., Ashley, D., Lee, S., Gadonna‐Widehem, P., Anton, P. M., & Carbonero, F. G. (2021) · Food Frontiers · doi:10.1002/fft2.75 · Cited by 20 · see citing works
Effect of inoculated azotobacteria and Phanerochaete chrysosporium on the composting of olive pomace: Microbial community dynamics and phenols evolution
Milanović, V., Osimani, A., Cardinali, F., Taccari, M., Garofalo, C., Clementi, F., Ashoor, S., Mozzon, M., Foligni, R., Canonico, L., et al. (2019) · Scientific Reports · doi:10.1038/s41598-019-53313-z · Cited by 18 · see citing works
Self-citation
Lactiplantibacillus plantarum, the Integral Member of Vegetable Fermentations
Paramithiotis, S. (2025) · Applied Biosciences · doi:10.3390/applbiosci4010007 · Cited by 21 · see citing works
“Such limitations included the inability to differentiate between closely related species, the formation of heteroduplexes, and the display of multiple bands for a single species [60,61].”
Autochthonous microbes and their key properties in browning reduction during soy sauce fermentation
Det-udom, R., Prakitchaiwattana, C., & Mahawanich, T. (2019) · LWT · doi:10.1016/j.lwt.2019.05.042 · Cited by 15 · see citing works
Investigating Antibiotic Resistance Genes in Marketed Ready‐to‐Eat Small Crickets ( Acheta domesticus )
Roncolini, A., Cardinali, F., Aquilanti, L., Milanović, V., Garofalo, C., Sabbatini, R., Abaker, M. S. S., Pandolfi, M., Pasquini, M., Tavoletti, S., et al. (2019) · Journal of Food Science · doi:10.1111/1750-3841.14818 · Cited by 15 · see citing works
Self-citation
Fate of Escherichia coli artificially inoculated in Tenebrio molitor L. larvae rearing chain for human consumption
Cesaro, C., Mannozzi, C., Lepre, A., Ferrocino, I., Corsi, L., Franciosa, I., Belleggia, L., Milanović, V., Cardinali, F., Garofalo, C., et al. (2022) · Food Research International · doi:10.1016/j.foodres.2022.111269 · Cited by 14 · see citing works
“Moreover, RNAs were also checked for quantity, purity, and integrity as described by Garofalo et al. (2017).”
MethodSelf-citation
Bacterial and Fungal Communities of Gioddu as Revealed by PCR–DGGE Analysis
Maoloni, A., Milanović, V., Cardinali, F., Mangia, N. P., Murgia, M. A., Garofalo, C., Clementi, F., Osimani, A., & Aquilanti, L. (2019) · Indian Journal of Microbiology · doi:10.1007/s12088-019-00838-6 · Cited by 14 · see citing works
Self-citation
Integrative liquid chromatography–tandem mass spectrometry metabolomics and high-throughput sequencing technology reveal physicochemical characteristics and bacterial diversity of traditionally pickled mustard tuber from different regions of China
Liu, S., Luo, J., Liu, X., Shi, Y. H., & Chen, Q. (2024) · Food Quality and Safety · doi:10.1093/fqsafe/fyae022 · Cited by 13 · see citing works
Identification of the Microbiota in Coconut Water, Kefir, Coconut Water Kefir and Coconut Water Kefir-Fermented Sourdough Using Culture-Dependent Techniques and Illumina–MiSeq Sequencing
Limbad, M., Maddox, N. G., Hamid, N., Kantono, K., & Higgins, C. M. (2024) · Microorganisms · doi:10.3390/microorganisms12050919 · Cited by 12 · see citing works
Exploring the spoilage microbiota of raw and processed meats under different storage environments and its related profiling methods: a review
Ndoye, B., Dicko, M. H., & Gill, C. O. (2025) · Cogent Food & Agriculture · doi:10.1080/23311932.2025.2562177 · Cited by 11 · see citing works
“Therefore, a way to avoid this situation is the use of nested PcR prior to dgge analysis to increase its sensitivity (garofalo et al., 2017; ndoye et al., 2022).”
A Glimpse into the Microbiota of Marketed Ready-to-Eat Crickets (Acheta domesticus)
Milanović, V., Cardinali, F., Aquilanti, L., Garofalo, C., Roncolini, A., Sabbatini, R., Clementi, F., & Osimani, A. (2019) · Indian Journal of Microbiology · doi:10.1007/s12088-019-00817-x · Cited by 10 · see citing works
Self-citation
The Dynamics Analysis of Fungal Community Diversity During the Fermentation Process of Chinese Traditional Soybean Paste
Ge, J., Wang, J., Chen, L., Song, G., & Ping, W. (2019) · Waste and Biomass Valorization · doi:10.1007/s12649-019-00800-z · Cited by 8 · see citing works
Study of the bacterial profile of raw milk butter, made during a challenge test with Listeria monocytogenes, depending on cream maturation temperature
El‐Hajjaji, S., Gérard, A., Laubier, J. D., Laine, A., Patz, V., & Sindic, M. (2021) · Food Microbiology · doi:10.1016/j.fm.2021.103778 · Cited by 7 · see citing works
Phenological Stages and Aluminum Presence Influences Arbuscular Mycorrhizal Fungi Communities in Roots of Plant Cereals
Aguilera, P., Romero, J. K., Becerra, N., Martínez, O. A., Vilela, R., BORIE, F. R., Cornejo, P., Marysol Alvear, Z., & López‐Gómez, M. (2021) · Journal of soil science and plant nutrition · doi:10.1007/s42729-021-00453-9 · Cited by 7 · see citing works
Advancement in LH-PCR methodology for multiple microbial species detections in fermented foods
Sardaro, M. L. S., Perin, L. M., Bancalari, E., Neviani, E., & Gatti, M. (2018) · Food Microbiology · doi:10.1016/j.fm.2018.03.008 · Cited by 6 · see citing works
Self-citation
Advanced Molecular Tools in Microbial Community Profiling in the Context of Bioremediation Applications
Panigrahi, S., Saranya, E., & Rao, T. S. (2024) · Elsevier eBooks · doi:10.1016/b978-0-443-13320-6.00009-3 · Cited by 4 · see citing works
Establishment of a rapid counting method for lactic acid bacteria and yeast in dairy products
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The Development and Application of DDPCR Technology on Quantification of Total Coliforms in Water
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Authors: Garofalo, C., Bancalari, E., Milanović, V., Cardinali, F., Osimani, A., Sardaro, M. L. S., Bottari, B., Bernini, V., Aquilanti, L., Clementi, F., Neviani, E., & Gatti, M.
Affiliations: Marche Polytechnic University (IT)
University of Parma (IT)
Corresponding author: Milanović, Vesna
ORCID: Garofalo, Cristiana
Bancalari, Elena
Milanović, Vesna
Osimani, Andrea
Sardaro, Maria Luisa Savo
Bottari, Benedetta
Bernini, Valentina
Aquilanti, Lucia
Neviani, Erasmo
Gatti, Monica
Venue: International Journal of Food Microbiology
Publisher: Elsevier BV
Published: 2017-02
Volume: 242
Pages: 24-36
ISSN: 0168-1605 (ISSN-L)
DOI: 10.1016/j.ijfoodmicro.2016.11.008
OpenAlex: W2556207200
Cited by: 49
References: 71
Citations by year: 2025: 2 · 2024: 6 · 2023: 1 · 2022: 2 · 2021: 7 · 2020: 7 · 2019: 12 · 2018: 8 · 2017: 4
FWCI: 10.07
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
Locations: International Journal of Food Microbiology (publishedVersion)
PubMed (publishedVersion)
Università Politecnica delle Marche (Università Politecnica delle Marche) (submittedVersion)
Topics: Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
Life Sciences › Biochemistry, Genetics and Molecular Biology › Clinical Biochemistry › Bacterial Identification and Susceptibility Testing
Keywords: PCR-DGGE, 16S rRNA gene, lactic acid bacteria, fermented foods, culture-independent detection, RNA detection, lactic acid bacteria identification
MeSH terms: Bacteria, DNA, Bacterial, Food Microbiology, RNA, Ribosomal, 16S, Polymerase Chain Reaction, Biodiversity, Denaturing Gradient Gel Electrophoresis

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Study of the bacterial diversity of foods: PCR-DGGE versus LH-PCR

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