DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Microbiomes Associated With Foods From Plant and Animal Sources

Journal Article · · Frontiers in Microbiology
 [1];  [2];  [3];  [4];  [4];  [4];  [5];  [5];  [2]
  1. US Food and Drug Administration, Laurel, MD (United States); DOE/OSTI
  2. US Food and Drug Administration, Laurel, MD (United States)
  3. Resphera Biosciences, Baltimore, MD (United States)
  4. US Food and Drug Administration, Jamaica, NY (United States)
  5. US Food and Drug Administration, College Park, MD (United States)

Food microbiome composition impacts food safety and quality. The resident microbiota of many food products is influenced throughout the farm to fork continuum by farming practices, environmental factors, and food manufacturing and processing procedures. Currently, most food microbiology studies rely on culture-dependent methods to identify bacteria. However, advances in high-throughput DNA sequencing technologies have enabled the use of targeted 16S rRNA gene sequencing to profile complex microbial communities including non-culturable members. In this study we used 16S rRNA gene sequencing to assess the microbiome profiles of plant and animal derived foods collected at two points in the manufacturing process; post-harvest/pre-retail (cilantro) and retail (cilantro, masala spice mixes, cucumbers, mung bean sprouts, and smoked salmon). Our findings revealed microbiome profiles, unique to each food, that were influenced by the moisture content (dry spices, fresh produce), packaging methods, such as modified atmospheric packaging (mung bean sprouts and smoked salmon), and manufacturing stage (cilantro prior to retail and at retail). The masala spice mixes and cucumbers were comprised mainly of Proteobacteria, Firmicutes, and Actinobacteria. Cilantro microbiome profiles consisted mainly of Proteobacteria, followed by Bacteroidetes, and low levels of Firmicutes and Actinobacteria. The two brands of mung bean sprouts and the three smoked salmon samples differed from one another in their microbiome composition, each predominated by either by Firmicutes or Proteobacteria. These data demonstrate diverse and highly variable resident microbial communities across food products, which is informative in the context of food safety, and spoilage where indigenous bacteria could hamper pathogen detection, and limit shelf life.

Research Organization:
Oak Ridge Institute for Science and Education (ORISE), Oak Ridge, TN (United States); US Food and Drug Administration, Laurel, MD (United States)
Sponsoring Organization:
USDOE Office of Science (SC)
Grant/Contract Number:
AC05-06OR23100
OSTI ID:
1628172
Journal Information:
Frontiers in Microbiology, Journal Name: Frontiers in Microbiology Vol. 9; ISSN 1664-302X
Publisher:
Frontiers Research FoundationCopyright Statement
Country of Publication:
United States
Language:
English

References (119)

Bacterial Diversity in the Rhizosphere of Cucumbers Grown in Soils Covering a Wide Range of Cucumber Cropping Histories and Environmental Conditions journal July 2014
Assessment of the Microbiological Safety of Dried Spices and Herbs Commercialized in Spain journal September 2010
Assessing the effect of oral exposure to Paenibacillus alvei , a potential biocontrol agent, in male, non-pregnant, pregnant animals and the developing rat fetus journal May 2017
Assessment of the microbiological safety of dried spices and herbs from production and retail premises in the United Kingdom journal February 2009
Indigenous and spoilage microbiota of farmed sea bream stored in ice identified by phenotypic and 16S rRNA gene analysis journal February 2013
Foodborne illness outbreaks from microbial contaminants in spices, 1973–2010 journal December 2013
Inhibition of Escherichia coli O157:H7 and Salmonella enterica on spinach and identification of antimicrobial substances produced by a commercial Lactic Acid Bacteria food safety intervention journal April 2014
Lettuce and fruits as a source of multidrug resistant Acinetobacter spp. journal June 2017
Testing commercial biopreservative against spoilage microorganisms in MAP packed Ricotta fresca cheese journal September 2017
Shifts in spinach microbial communities after chlorine washing and storage at compliant and abusive temperatures journal August 2018
Evaluation of the spoilage potential of bacteria isolated from spoiled raw salmon (Salmo salar) fillets stored under modified atmosphere packaging journal January 2013
Taxonomic evaluation of the genus Enterobacter based on multilocus sequence analysis (MLSA): Proposal to reclassify E. nimipressuralis and E. amnigenus into Lelliottia gen. nov. as Lelliottia nimipressuralis comb. nov. and Lelliottia amnigena comb. nov., respectively, E. gergoviae and E. pyrinus into Pluralibacter gen. nov. as Pluralibacter gergoviae comb. nov. and Pluralibacter pyrinus comb. nov., respectively, E. cowanii, E. radicincitans, E. oryzae and E. arachidis into Kosakonia gen. nov. as Kosakonia cowanii comb. nov., Kosakonia radicincitans comb. nov., Kosakonia oryzae comb. nov. and Kosakonia arachidis comb. nov., respectively, and E. turicensis, E. helveticus and E. pulveris into Cronobacter as Cronobacter zurichensis nom. nov., Cronobacter helveticus comb. nov. and Cronobacter pulveris comb. nov., respectively, and emended description of the genera Enterobacter and Cronobacter journal July 2013
The ecological importance of the Staphylococcus sciuri species group as a reservoir for resistance and virulence genes journal July 2014
Listeria monocytogenes in the smoked salmon industry journal December 2000
Study of the microbial ecology of cold-smoked salmon during storage at 8°C journal January 1998
Leuconostoc citreum MB1 as biocontrol agent of Listeria monocytogenes in milk journal December 2013
Nationwide outbreak of human salmonellosis in Germany due to contaminated paprika and paprika-powdered potato chips journal December 1995
Abundance, composition, diversity and novelty of soil Proteobacteria journal April 2009
Origin and ecological selection of core and food-specific bacterial communities associated with meat and seafood spoilage journal October 2014
A human gut microbial gene catalogue established by metagenomic sequencing journal March 2010
A framework for human microbiome research journal June 2012
Structure, function and diversity of the healthy human microbiome journal June 2012
Changes in urinary microbiota correlate with IC/BPS journal March 2017
High-resolution bacterial 16S rRNA gene profile meta-analysis and biofilm status reveal common colorectal cancer consortia journal November 2017
Enterotypes in the landscape of gut microbial community composition journal December 2017
Comparison of bacterial communities between midgut and midgut contents in two silkworms, Antheraea pernyi and Bombyx mori journal July 2020
Isolation and characterization of Lactococcus piscium strains from vacuum-packaged refrigerated beef journal January 2002
Microbial spoilage and formation of biogenic amines in fresh and thawed modified atmosphere-packed salmon (Salmo salar) at 2oC journal April 2002
Isolation of Acinetobacter spp including A. baumannii from vegetables: implications for hospital-acquired infections journal July 1999
An Outbreak of Salmonella Serotype Thompson Associated with Fresh Cilantro
  • Campbell, Jennifer Vernon; Mohle‐Boetani, Janet; Reporter, Roshan
  • The Journal of Infectious Diseases, Vol. 183, Issue 6 https://doi.org/10.1086/319254
journal March 2001
Outbreaks Caused by Sprouts, United States, 1998–2010: Lessons Learned and Solutions Needed journal August 2014
The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms journal September 2013
The bacterial flora of vacuum-packed cold-smoked salmon stored at 7°C, identified by direct 16S rRNA gene analysis and pure culture technique: The bacterial flora of smoked salmon journal December 2006
In Situ Evaluation of Paenibacillus alvei in Reducing Carriage of Salmonella enterica Serovar Newport on Whole Tomato Plants journal April 2014
Application of Metagenomic Sequencing to Food Safety: Detection of Shiga Toxin-Producing Escherichia coli on Fresh Bagged Spinach journal September 2015
Multilocus Sequence Typing of Leuconostoc gelidum subsp. gasicomitatum, a Psychrotrophic Lactic Acid Bacterium Causing Spoilage of Packaged Perishable Foods journal January 2015
Molecular characterization of genes involved in the production of the bacteriocin leucocin A from Leuconostoc gelidum. journal January 1995
UniFrac: a New Phylogenetic Method for Comparing Microbial Communities journal December 2005
Draft Genome Sequences of Paenibacillus alvei A6-6i and TS-15 journal August 2013
Characterization of leucocin A-UAL 187 and cloning of the bacteriocin gene from Leuconostoc gelidum. journal January 1991
Cilantro microbiome before and after nonselective pre-enrichment for Salmonella using 16S rRNA and metagenomic sequencing journal August 2015
Enrichment dynamics of Listeria monocytogenes and the associated microbiome from naturally contaminated ice cream linked to a listeriosis outbreak journal November 2016
Mungo bean sprout microbiome and changes associated with culture based enrichment protocols used in detection of Gram-negative foodborne pathogens journal September 2016
Co-Enriching Microflora Associated with Culture Based Methods to Detect Salmonella from Tomato Phyllosphere journal September 2013
Comparative Genomic Analysis Indicates that Niche Adaptation of Terrestrial Flavobacteria Is Strongly Linked to Plant Glycan Metabolism journal September 2013
Strain-Level Discrimination of Shiga Toxin-Producing Escherichia coli in Spinach Using Metagenomic Sequencing journal December 2016
Outbreak of Salmonella Oslo Infections Linked to Persian Cucumbers — United States, 2016 journal December 2016
An outbreak of Salmonella Newport associated with mung bean sprouts in Germany and the Netherlands, October to November 2011 journal January 2014
Large outbreak of Salmonella Thompson related to smoked salmon in the Netherlands, August to December 2012 journal October 2014
High-Resolution Microbiome Profiling for Detection and Tracking of Salmonella enterica journal August 2017
Assessment of the Microbiological Quality of Spices and Herbs journal December 1986
Microbiological Survey of Retail Herbs and Spices from Mexican Markets journal January 2001
Bacterial Diversity in the Rhizosphere of Cucumbers Grown in Soils Covering a Wide Range of Cucumber Cropping Histories and Environmental Conditions journal July 2014
Assessment of the Microbiological Safety of Dried Spices and Herbs Commercialized in Spain journal September 2010
Identification and Structural Characterization of Naturally-Occurring Broad-Spectrum Cyclic Antibiotics Isolated from Paenibacillus journal August 2015
Listeria monocytogenes in the smoked salmon industry journal December 2000
Food spoilage—interactions between food spoilage bacteria journal September 2002
Study of the microbial ecology of cold-smoked salmon during storage at 8°C journal January 1998
Assessing the effect of oral exposure to Paenibacillus alvei , a potential biocontrol agent, in male, non-pregnant, pregnant animals and the developing rat fetus journal May 2017
Assessment of the microbiological safety of dried spices and herbs from production and retail premises in the United Kingdom journal February 2009
Indigenous and spoilage microbiota of farmed sea bream stored in ice identified by phenotypic and 16S rRNA gene analysis journal February 2013
Foodborne illness outbreaks from microbial contaminants in spices, 1973–2010 journal December 2013
Inhibition of Escherichia coli O157:H7 and Salmonella enterica on spinach and identification of antimicrobial substances produced by a commercial Lactic Acid Bacteria food safety intervention journal April 2014
Psychrotrophic members of Leuconostoc gasicomitatum, Leuconostoc gelidum and Lactococcus piscium dominate at the end of shelf-life in packaged and chilled-stored food products in Belgium journal May 2014
Lettuce and fruits as a source of multidrug resistant Acinetobacter spp. journal June 2017
Testing commercial biopreservative against spoilage microorganisms in MAP packed Ricotta fresca cheese journal September 2017
Shifts in spinach microbial communities after chlorine washing and storage at compliant and abusive temperatures journal August 2018
Characterization and evaluation of the spoilage potential of Lactococcus piscium isolates from modified atmosphere packaged meat journal May 2012
Evaluation of the spoilage potential of bacteria isolated from spoiled raw salmon (Salmo salar) fillets stored under modified atmosphere packaging journal January 2013
Taxonomic evaluation of the genus Enterobacter based on multilocus sequence analysis (MLSA): Proposal to reclassify E. nimipressuralis and E. amnigenus into Lelliottia gen. nov. as Lelliottia nimipressuralis comb. nov. and Lelliottia amnigena comb. nov., respectively, E. gergoviae and E. pyrinus into Pluralibacter gen. nov. as Pluralibacter gergoviae comb. nov. and Pluralibacter pyrinus comb. nov., respectively, E. cowanii, E. radicincitans, E. oryzae and E. arachidis into Kosakonia gen. nov. as Kosakonia cowanii comb. nov., Kosakonia radicincitans comb. nov., Kosakonia oryzae comb. nov. and Kosakonia arachidis comb. nov., respectively, and E. turicensis, E. helveticus and E. pulveris into Cronobacter as Cronobacter zurichensis nom. nov., Cronobacter helveticus comb. nov. and Cronobacter pulveris comb. nov., respectively, and emended description of the genera Enterobacter and Cronobacter journal July 2013
The ecological importance of the Staphylococcus sciuri species group as a reservoir for resistance and virulence genes journal July 2014
Leuconostoc citreum MB1 as biocontrol agent of Listeria monocytogenes in milk journal December 2013
Nationwide outbreak of human salmonellosis in Germany due to contaminated paprika and paprika-powdered potato chips journal December 1995
Salmonella infections associated with mung bean sprouts: epidemiological and environmental investigations journal February 2008
Measurement of Diversity journal April 1949
Abundance, composition, diversity and novelty of soil Proteobacteria journal April 2009
Origin and ecological selection of core and food-specific bacterial communities associated with meat and seafood spoilage journal October 2014
A human gut microbial gene catalogue established by metagenomic sequencing journal March 2010
Enterotypes of the human gut microbiome journal April 2011
A framework for human microbiome research journal June 2012
Structure, function and diversity of the healthy human microbiome journal June 2012
High-resolution bacterial 16S rRNA gene profile meta-analysis and biofilm status reveal common colorectal cancer consortia journal November 2017
Enterotypes in the landscape of gut microbial community composition journal December 2017
Reconstructing hotspots of genetic diversity from glacial refugia and subsequent dispersal in Italian common toads (Bufo bufo) journal January 2021
Isolation and characterization of Lactococcus piscium strains from vacuum-packaged refrigerated beef journal January 2002
Microbial spoilage and formation of biogenic amines in fresh and thawed modified atmosphere-packed salmon (Salmo salar) at 2oC journal April 2002
Isolation of Acinetobacter spp including A. baumannii from vegetables: implications for hospital-acquired infections journal July 1999
An Outbreak of Salmonella Serotype Thompson Associated with Fresh Cilantro
  • Campbell, Jennifer Vernon; Mohle‐Boetani, Janet; Reporter, Roshan
  • The Journal of Infectious Diseases, Vol. 183, Issue 6 https://doi.org/10.1086/319254
journal March 2001
Outbreaks Caused by Sprouts, United States, 1998–2010: Lessons Learned and Solutions Needed journal August 2014
Urinary Microbiome and Cytokine Levels in Women With Interstitial Cystitis journal January 2017
Urinary Microbiome and Cytokine Levels in Women With Interstitial Cystitis journal January 2017
The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms journal September 2013
The bacterial flora of vacuum-packed cold-smoked salmon stored at 7°C, identified by direct 16S rRNA gene analysis and pure culture technique: The bacterial flora of smoked salmon journal December 2006
Evaluation of antimicrobial activity in Paenibacillus spp. strains isolated from natural environment journal November 2006
In Situ Evaluation of Paenibacillus alvei in Reducing Carriage of Salmonella enterica Serovar Newport on Whole Tomato Plants journal April 2014
Application of Metagenomic Sequencing to Food Safety: Detection of Shiga Toxin-Producing Escherichia coli on Fresh Bagged Spinach journal September 2015
Multilocus Sequence Typing of Leuconostoc gelidum subsp. gasicomitatum, a Psychrotrophic Lactic Acid Bacterium Causing Spoilage of Packaged Perishable Foods journal January 2015
Molecular characterization of genes involved in the production of the bacteriocin leucocin A from Leuconostoc gelidum. journal January 1995
UniFrac: a New Phylogenetic Method for Comparing Microbial Communities journal December 2005
Draft Genome Sequences of Paenibacillus alvei A6-6i and TS-15 journal August 2013
Characterization of leucocin A-UAL 187 and cloning of the bacteriocin gene from Leuconostoc gelidum. journal January 1991
Cilantro microbiome before and after nonselective pre-enrichment for Salmonella using 16S rRNA and metagenomic sequencing journal August 2015
Enrichment dynamics of Listeria monocytogenes and the associated microbiome from naturally contaminated ice cream linked to a listeriosis outbreak journal November 2016
Mungo bean sprout microbiome and changes associated with culture based enrichment protocols used in detection of Gram-negative foodborne pathogens journal September 2016
Bacterial Communities Associated with the Surfaces of Fresh Fruits and Vegetables journal March 2013
Co-Enriching Microflora Associated with Culture Based Methods to Detect Salmonella from Tomato Phyllosphere journal September 2013
Comparative Genomic Analysis Indicates that Niche Adaptation of Terrestrial Flavobacteria Is Strongly Linked to Plant Glycan Metabolism journal September 2013
Strain-Level Discrimination of Shiga Toxin-Producing Escherichia coli in Spinach Using Metagenomic Sequencing journal December 2016
Outbreak of Salmonella Oslo Infections Linked to Persian Cucumbers — United States, 2016 journal December 2016
An outbreak of Salmonella Newport associated with mung bean sprouts in Germany and the Netherlands, October to November 2011 journal January 2014
Large outbreak of Salmonella Thompson related to smoked salmon in the Netherlands, August to December 2012 journal October 2014
Early Recovery of Salmonella from Food Using a 6-Hour Non-selective Pre-enrichment and Reformulation of Tetrathionate Broth journal December 2016
High-Resolution Microbiome Profiling for Detection and Tracking of Salmonella enterica journal August 2017
Assessment of the Microbiological Quality of Spices and Herbs journal December 1986
Microbiological Survey of Retail Herbs and Spices from Mexican Markets journal January 2001
Mungo bean sprout microbiome and changes associated with culture based enrichment protocols used in detection of Gram-negative foodborne pathogens text January 2016
Additional file 1: Figure S1. of Enrichment dynamics of Listeria monocytogenes and the associated microbiome from naturally contaminated ice cream linked to a listeriosis outbreak image January 2016
Additional file 1: Figure S1. of Enrichment dynamics of Listeria monocytogenes and the associated microbiome from naturally contaminated ice cream linked to a listeriosis outbreak image January 2016
Cilantro microbiome before and after nonselective pre-enrichment for Salmonella using 16S rRNA and metagenomic sequencing collection January 2015

Cited By (3)

Effects of an Eco-Friendly Sanitizing Wash on Spinach Leaf Bacterial Community Structure and Diversity journal April 2020
Plant-associated and soil microbiota composition as a novel criterion for the environmental risk assessment of genetically modified plants journal December 2019
Microbiota in foods from Inuit traditional hunting journal January 2020