Trends in Analytical Chemistry 96 (2017) 14e21

Contents lists available at ScienceDirect

Trends in Analytical Chemistry

journal homepage: www.elsevier.com/locate/trac

Foodomics: A novel approach for food microbiology

Yong-Jiang Xu a, b, *
a
Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China
b
Department of Medicine, University of California San Diego, La Jolla, CA, United States

a r t i c l e i n f o a b s t r a c t

Article history: Microorganisms exert both beneficial and deleterious effects on food stuff. Foodomics is a new holistic
Available online 17 June 2017 approach that employs advanced omics technologies for the exploitation of food and nutrition sciences.
This article intends to review the methodologies of foodomics, especially in proteomics and metab-
Keywords: olomics. The applications of foodomics in food microbiology were also discussed, such as food safety
Foodomics assessment, quality control regulation, food nutrition and health study.
Food microbiology
© 2017 Elsevier B.V. All rights reserved.
Proteomics
Metabolomics
Food safety

1. Introduction On the other hand, microorganisms have both beneficial and

Food science is a study of all disciplines of food, including
physical, biological, and chemical makeup and food-processing [1].
In past decades, the research in food science has moved from
classical methodologies to advance technologies that have been
well established in medical, pharmacological, and biotechnology
studies [2e4]. More recently, food scientists are interested in
applying “omics” methods on food research (Fig. 1A). In 2009,
Cifuentes's group proposed the concept and practical approach of
“foodomics” to implement “omics” methods in food study [5]. In
just a few years, this definition has been accepted by an increasing
number of researchers [6e8].
Foodomics is defined as a discipline that studies food and
nutrition domains using advanced omics technologies, such as
genomics, transcriptomics, proteomics and metabolomics [9e11].
As shown in Fig. 1B, these methodologies have been increasingly
used for investigations of food contaminants and toxicity; active
compound profiling, authenticity, biomarker related to food quality
and effects upon human health; and development of functional
foods and transgenic foods, etc [12e15].
Abbreviations: 2-DE, two-dimensional polyacrylamide gel electrophoresis; ANN,
artificial neural network; CA, clustering analysis; DA, discriminant analysis; mRNAs,
messenger RNAs; MS, Mass spectrometry; MALDI-TOF/MS, matrix-assisted laser
desorption ionization-time-of-flight mass spectrometry; MLR, multiple linear
regression; MLVA, multiple-locus variable number tandem repeated analysis; NMR,
nuclear magnetic resonance; NGS, Next-generation sequencing; PCA, principal
component analysis; PLS, partial least square regression; PFGE, pulsed-field gel
electrophoresis; QC, quality control; SIMCA, soft independent modeling of class
analogy; WGS, whole-genome sequencing.
* Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, No
300 Fenglin Road, Shanghai 201203, China.
E-mail address: yjxutju@gmail.com.
deleterious effects on food. For example, saprophytic microor-
ganism could induce food spoilage, and pathogenic microorgan-
isms could cause infections or intoxications [16]. On the contrary,
“good” microorganisms are fundamental to fermented foods, such
as Saccharomyces cerevisiae, lactic acid bacteria, and Acetobacterium
balch [17]. The term of food microbiology focuses on all aspects of
food microorganism, and has been integrated into food science as
an important component. The study of food microbiology involves
food microbe detection, identification, growth characteristics,
quantitation, prevention and modification [18].
In recent years, foodomic technologies have been widely used
for the study of food microbiology, such as safety assessment,
quality control, nutritional component analysis [19e21]. In this
article, we attend to review the methodologies in foodomics,
especially in proteomics and metabolomics, and the application of
foodomics on food microbiology.
2. The methodologies and technologies in foodomics
Research methods and instruments of foodomics integrate
analytical chemistry, biochemistry, molecular biology, food tech-
nology, chemometrics and bioinformatics. In such a context, the full
understanding of methodologies in foodomics seems extremely
important.
2.1. Genomics
Genomics refers to sequence, assembly, and analysis of the
structure and function of genome within an organism [22]. Current
tremendous progress in genomics is largely attributed to the ability
of DNA sequence technology at increasing throughput and

http://dx.doi.org/10.1016/j.trac.2017.05.012
0165-9936/© 2017 Elsevier B.V. All rights reserved.
 Y.-J. Xu / Trends in Analytical Chemistry 96 (2017) 14e21
Fig. 1. (A) Foodolomics-related papers published between 2001-2016 (based on ISIS web of science) (B) Foodomics investigates the relationship among human health, diet and
microorganisms.
decreasing cost [23]. Next-generation sequencing (NGS) technolo-
gies have been widely used in genomic study. Compared to Sanger
capillary electrophoresis sequencing method, NGS technologies
usually do not require sequence library, and can process millions of
sequencing reactions in parallel [24]. With the help of innovative
method and development in computer, NGS technologies have
achieved many fruits over the past decades [25].
Recently, a new methodology named Sing-molecule sequencing
has been introduced in genomics. This technique sequence indi-
vidual molecules of DNA using various schemes. It produces sub-
stantially longer reads than NGS, enabling the assembly of
sequencing-read data to generate long contiguous sequences,
even for large complex genome [26].
In the field of foodomics, genomic analysis provides an oppor-
tunity to improve the understanding of the components of food
products [27]. It has accelerated the study of the relationship be-
tween food nutrient and human health [28]. As a result, the
application of genomics is conducive to the promotion of food
quality, may provide a solution to malnutrition and other diseases.
2.2. Transcriptomics
Transcriptomics is the study of all RNA in one cell or a popula-
tion of cells [29]. It provides the precise measurement of tran-
scription, giving a full picture of the extent and complexity of
transcriptomes [30]. There are now two techniques in tran-
scriptomics: microarrays and RNA-sequencing (RNA-Seq). Micro-
arrays are particularly applicable for analyzing large mammalian
transcriptomes. However, it can't be used for unknown RNA char-
acterization since microarray was designed for known sequences
[31]. Whereas, RNA-seq can be used for qualitative and quantitative
analysis on any RNA type, including messenger RNAs (mRNAs),
microRNAs, small interfering RNAs, and long noncoding RNAs [32].
In the domain of foodomics, transcriptomic analysis not only
unfolds the modulation of the global gene expression profile in food
material, but also reveals the role of food in human health. There-
fore, transcriptomics has been greatly used to assess food nutrition
for the maintenance of physiological equilibrium and disease pre-
vention [33].
2.3. Proteomics
Proteome are differed among individuals, cell types, even within
the same cell in the different state. The term of proteomics is the
scientific research of proteome, aiming to explore protein compo-
sition, structure, level and unique activity patterns [34]. Because
various proteins exist in biological samples with a magnitude of
concentration differentiation, sample preparation in proteomics
attends to reduce proteome complexity, fractionation, depletion,
and to enrich low-abundant proteins. Subsequently, protein
15
isolation and characterization are required. The traditional two-
dimensional polyacrylamide gel electrophoresis (2-DE) method is
time-consuming, sometimes tedious, and suffers from poor per-
formance on high or low molecular weight proteins. In the last few
years, multi-dimensional liquid chromatography has been gradu-
ally becoming a promising technology for protein isolation and
separation [35]. Mass spectrometry (MS) is the major method for
protein identification. Specifically, high sensitive and resolution
mass spectrometry like matrix-assisted laser desorption
ionization-time-of-flight mass spectrometry (MALDI-TOF/MS)
could differentiate microbes without protein identification: repre-
sentative peaks patterns sufficient for conclusions about species,
genus or even strain level. This technology allows for rapid and
>99% accurate identification of microorganisms (region-specific
sub-strains) cultured from routine clinical samples through the
identification of species-specific proteomic profiles [36]. In practice,
two strategies have been used in the proteomic study, i.e. “bottom-
up,” and “top-down”. In “bottom-up” approach, purified proteins or
complex mixtures of protein are digested into peptides via pro-
teolytic cleavage, and then analyzed in a mass spectrometer [37]. By
contrast, the “top-down” approach allows MS analysis of intact
proteins that have not been cleaved, meaning the labile structural
protein that are mostly destroyed in bottom-up approach are pre-
served [38]. In summary, “bottom-up” approach exhibited better
separation of peptides compared with proteins and higher sensi-
tivity than the “top-down” approach. However, the disadvantage of
“bottom-up” approach is limited protein sequence coverage by
identified peptides, loss of labile post-translational modifications,
and ambiguity of the origin for redundant peptide sequences.
Moreover, elimination of protein digestion in the “top-down”
approach results in significant time saving [39]. Recently, protein
chip technology based on microarray has also been introduced in
proteomic analysis. The developed lab-on-a-chip systems integrate
protein extraction, separation, and identification processes on one
microfluidic chip, which reduced sample consumption, analysis
time, and cost [40].
Since proteins are closely related to food compositions, prote-
omic analysis has significant implications for enhancing food
authentication, quality and safety [41]. In addition, proteomic
investigation in human blood or tissues after food helps to under-
stand the mechanism of food nutrition and its roles in human
health [42].
2.4. Metabolomics
Metabolome is the final downstream product of genome, tran-
scriptome and proteome, which reflects most phenotype of a bio-
logical system. Metabolomics refers to study all endogenous or
exogenous metabolites in a biological system and to explore their
metabolic pathway [43]. Technically, metabolomic methodologies
16 Y.-J. Xu / Trends in Analytical Chemistry 96 (2017) 14e21
were classified into two distinct groups: untargeted metabolomics,
the intended comprehensive analysis of all compounds; targeted
metabolomics, the measurement of defined groups of chemically
characterized and biochemically annotated metabolites [44]. The
most common analytical methods in metabolomics are nuclear
magnetic resonance (NMR) spectroscopy and mass spectrometry
(MS). NMR spectroscopy works well in quantitative analysis, and
doesn't require extra steps for sample preparation, such as sepa-
ration and derivatization. However, low sensitivity is a fatal defect
for NMR spectroscopy. Oppositely, MS can offer a combined high
sensitivity and high selectivity platform for metabolomic study
[45]. Especially, high-resolution mass spectrometry (HRMS), such
as TOF-MS and Orbitrap, has been increasingly used to produce
metabolomic data. In mass spectrometry, resolution measures of
the ability to distinguish two peaks of slightly different mass-to-
charge ratios. Due to high mass resolution and accuracy, HRMS
has the capable of separating mass fragments at the fourth or fifth
decimal place (exact mass) where previous instrumentation was
limited to single-digit mass units (integer mass). Therefore, HRMS
offers robust methodologies to identify metabolites in complex
matrix and will be a valuable contributor to the field of metab-
olomics [46]. In addition, These techniques either stand alone or
combined with separation techniques (typically, LCeNMR, GCeMS,
LCeMS, and CEeMS), provide a powerful tool for foodomics [47].
Metabolomics has been used to study large-scale small mole-
cule metabolites in food, and analyze the active functional com-
ponents or hazardous ingredients in food, which could help food
quality control and identification of food sources. Moreover, we can
identify markers related to health status and food nutrition so as to
evaluate the nutritional function of food, based on the knowledge
of food and human metabolome, [48].
2.5. Other technologies
Apart from the above-mentioned methods, other technologies
have also been used in foodomics, such as chemometrics and
bioinformatics.
The application of omics techniques will generate a large
amount of complex experimental data. Therefore, chemometrics
and bioinformatics have emerged and facilitated data analysis.
Chemometrics incorporates mathematics, statistics, computer sci-
ence, and other related studies into experimental design, chemical
analysis and explication of the relationships between chemical
structures and performance [49]. Common chemometric methods
were divided into two groups: unsupervised and supervised
Table 1
Summary of online available database for Foodomics technologies.
Technology Online resource
Genomics Genomes online Database (GOLD)
Microbial Genome Database (MBGD)
National Microbial Pathogen Data Resource (NMPDR)
Global Microbial Identifier (GMI)
Transcriptomics Gene Expression Omnibus (GEO)
Stanford Microarray Database (SMD)
ArrayExpress functional genomics data
ExPASY Bioinformatics Resource Portal
Proteomics High-quality Automated and Manual Annotation of Proteins (HAMAP)
Proteome Database System for Microbial Research
E. coli protein database (EcoProDB)
PRIDE-Proteomics Identifications Database
Metabolomics MetaCyc
The Yeast Metabolome Database (YMDB)
Kyoto Encyclopedia of Genes and Genomes (KEGG)
The Human Microbiome Project (HMP)
National Microbiological Database (NMD)
methods. The unsupervised analysis methods, such as principal
component analysis (PCA), discriminant analysis (DA), clustering
analysis (CA), are identified without taking into account the type or
class of the study samples. The supervised methods, such as partial
least square regression (PLS), multiple linear regression (MLR),
artificial neural network (ANN), soft independent modeling of class
analogy (SIMCA), and wavelet transform, are employed to identify
those features that associated with a phenotype of interest, and also
used to build prediction models [50].
On the other hand, biofunctions of most genes, proteins and
metabolites are not clear. Thus, bioinformatics is applied to explore
these descriptive data, and to elaborate the biological significance.
Recently, a variety of bioinformatic tools have been developed for
functional annotation and clustering of genes and proteins data
generated from omics techniques. Continually, potential bio-
markers and molecular mechanisms can be identified and evalu-
ated based on statistical analysis and the knowledge of signaling
pathways [51].
Taken together, these methodologies and technologies have
accelerated the study of food safety, quality and nutrient during
food processing. Benefitting from the wealth of information,
numerous databases have emerged and helped to speed up the
research of foodomics (Table 1).
3. The application of foodomics in food microbiology
Foodomics has emerged as a new science with the increase of
people's concern about food safety, quality and nutrients (Fig. 2). In
this section, we discussed the application of foodomics in food
microbiology.
3.1. Food safety assessments
Food safety is a crucial issue of food science, which studies food
harvesting, handling, and storing, with the aim to prevent food-
borne disease [52]. Since modern food components are diverse, and
potential hazardous matters in food might differ tremendously,
traditional method is inadequate for the detection of all contami-
nants and unsafe matters in food. In the domain of microbiology,
foodborne pathogens, mostly bacteria and fungi, could contaminate
food at any process stage from food production to consumption.
Even worse, some microbes can be resistant to inactivation, and
survive harsh treatment during food processing [53]. As a result,
microbial food safety has complex problems, including spore
forming bacteria, thermostable bacterial toxins and mycotoxins,
URL
https://gold.jgi.doe.gov/
http://mbgd.genome.ad.jp/
http://www.nmpdr.org
http://www.globalmicrobialidentifier.org
https://www.ncbi.nlm.nih.gov/geo/
http://genome-www.stanford.edu/microarray/
https://www.ebi.ac.uk/arrayexpress/
https://www.expasy.org
http://hamap.expasy.org
http://www.mpiib-berlin.mpg.de/2D-PAGE
http://eecoli.kaist.ac.kr/main.html
https://www.ebi.ac.uk/pride/archive/
https://metacyc.org
http://www.ymdb.ca
www.genome.jp/kegg/
http://www.hmpdacc.org
http://www.foodsafety.govt.nz/industry/general/nmd/
 Y.-J. Xu / Trends in Analytical Chemistry 96 (2017) 14e21
Fig. 2. Study contents, study methods and study objects in the application of foodomics on food microbiology.
biofilm forming microorganisms, and marine biotoxins. Therefore,
there has been an active demand for the fast, reliable and sensitive
method for the detection of food pathogens and determination of
mycotoxins.
Foodomic methodologies offer powerful tools to address the
issue of microbial food safety. For example, whole-genome
sequencing (WGS) that associated with the scalable, flexible na-
ture of NGS technology has exceeded some shortcomings in current
methods for subtyping (such as pulsed-field gel electrophoresis
(PFGE) and multiple-locus variable number tandem repeated
analysis (MLVA)), allowing to improve outbreak detection of
foodborne bacteria. WGS provided improved discriminatory power
over PFGE or MLVA on various microbes, including highly clonal
bacterial pathogens (such as Bacillus anthracis and Yersinia pestis
[54e57]), specific subtypes within a given pathogen species (such
as B. anthracis, Escherichia coli, Shigella spp and Salmonella serovars
[58,59]) and foodborne viruses and parasites [60,61]. In addition,
many foodborne viruses were also detected by NGS technologies,
such as norovirus [61], adenovirus [62] and gyrovirus [63].
17
In order to understand the physiological state of food pathogens,
transcriptomics has been used to determine the modulation of gene
and protein expression of pathogens in response to the different
condition. The gene expressions of pathogens inoculated onto
different food products were evaluated using microarrays, such as
Salmonella on cilantro and lettuce [64], E. coli on lettuce [65]. These
studies suggested several gene expressions are increased when
these pathogens colonize in food stuff, such as cell envelope stress
response and the oxidative stress response. These findings provide
a potential food preservation approach through activating these
stress responses. Besides, RNA-Seq has also been employed to study
foodborne pathogens. For instance, Wurtzel et al. used strand-
specific RNA-Seq approach to discriminate pathogenic and non-
pathogenic Listeria species, i.e. L. monocytogenes and L. innocua
[66]. Another RNA-Seq based transcriptomic analysis on persistent
and presumed nonpersistent L. monocytogenes strains reported
three gene operons, pdu, cob-cbi, and eut, might play a role in the
persistence of L. monocytogenes outside the human host [67]. Be-
sides, RNA-Seq analysis shed light on the survival mechanisms of
18 Y.-J. Xu / Trends in Analytical Chemistry 96 (2017) 14e21
pathogens, e.g. the cultivation of Salmonella enterica in peanut oil
under desiccation and starvation stress [68].
Analogously, proteomics has also been well documented to
provide a valuable approach to detect and identify foodborne
pathogens. Among proteomic approaches, MALDI-TOF/MS repre-
sents a powerful tool in pathogens detection. For instance, Frager-
quist et al. successfully applied MALDI-TOF/MS and tandem MS to
characterize different E. coli subtype based on top-down approach
[69]. In another case, the conventional detection of Listeria mono-
cytogenes requires four to five days to have a result. Jadhav
et al. recently developed an easy and sensitive MALDI-TOF-MS
method to detect L. monocytogenes directly from selective enrich-
ment broth within 30 h [70]. Theoretically, 2DEeMS and LCeMS are
both useful in pathogen identification. For example, Gagliardi
et al. performed proteomic analysis on a long-term survival strain
of E. coli K-12 by 2DEeMS approach, identifying several differen-
tially expressed proteins related to the growth advantage in
stationary-phase [71]. In a second study, Gilquin et al. employed
LCeMS-based proteomic assay to detect five pathogens in food,
including Clostridium perfringens, Staphylococcus aureus, Shigella
dysenteriae and E. coli and Campylobacter jejuni [72]. The finding
from proteomic studies can provide huge support in the compre-
hension of the mechanisms of infection, antibiotic resistance and
biofilm formation of foodborne pathogens [73].
During pathogens growth, many toxins will be secreted into the
extracellular environment, while a few harmful substances are
liberated and contaminate food after the disintegration of food
pathogens (Table 2). There are a lot of literature reported metab-
olomic studies manage to determine food pathogen through
scanning mycotoxins. In 2014, Cajka et al. employed LCeMS based
metabolomics to distinguish Fusarium-infected and control barley
samples [74]. Another LCeMS based metabolomic analysis on my-
cotoxins from the surface of 15 different medicinal herbs lead to
characterize a total of 126 fungi, with Aspergillus and Penicillium
genera as the predominant contaminants [75].
Assuring food safety, especially microbial contaminants, is still a
very complex task. Foodomic technologies have matured in recent
years and provided precise identification of food pathogens and
their toxins even on the strain/subtype level from highly complex
food samples.
3.2. Food quality control regulations
Quality control (QC) of food refers to the control of authenticity,
origin, properties, composition, and safety involving all steps of food
production. Especially, the authenticity and origin of fermented
Table 2
Summary of food pathogens and mycotoxins.
Pathogens Major mycotoxin
Clostridium Bacteriocins, Boticin, Clostocins, Cytotoxin, Ethylamine, etc
Staphylococcus Aflastain, Albonoursin, Baccatin A, Diemenensin A,
Hydnocarpin, etc
Escherichia coli Phagicin, Siroheme, Lysidine, Colicin E3, etc
Listeria Enterocin CTC 492
Vibrio Amphibactins, Fluvibactin, Kailuin etc
Bacillus Amicoumacin B, C; Baciferacin, Bacileucine A, B; Bacilipin,
Bacilaene, Bacilomycin A, B, C, D, E F. etc
Toxoplasma Plakortolid F
Aspergillus Aflatoxin B, Ochratoxin, Aculeacin A, B, C, D, E, F, G;
Aflatrem, etc
Fusarium Deoxynivalenol, Zearalenone, Fumonisins, Trichothecenes,
etc
Penicillium Agroclavine, Amauromine, Patulin, Citrinin etc
Claviceps Aflatrem, Chanoclavine I, Ergobine, Ergobutine,
Ergobutyrine, Ergochromes, etc
foods predetermine their palatability, nutritional value, medicinal
properties [76]. Moreover, fermentation process has significant ef-
fects on taste, flavor and nutrition of fermented foods. Therefore, QC
plays an extremely important role in fermented food. However,
traditional QC methods in food analysis like targeted detection are
not insufficient capable of monitoring and appraisal of raw material
and processing of fermented food to ensure food quality [77].
Recently, foodomics has facilitated systematic research on QC in
fermentation, such as fast identification of origination of microbial
food, and the monitoring of fermentation procedures. Genomics has
already contributed precious insights into the determination of
genes related to production traits of fermented food [78]. For
example, the genome sequences of several lactic acid bacteria have
been completed by WGS techniques, indicating different lactic acid
bacteria make different contribution to the flavor and texture of
cheeses [79e81]. Another genomic study using NGS technology has
elucidated genetic diversity of Oenococcus oeni in industrially-
relevant pathways, which improved understanding and harnessing
the phenotypic variation presence of economically-important spe-
cies [82]. Therefore, these genomic studies are of great assistance in
the understanding of microbe behavior in fermentation process.
The high-throughput sequencing technology has innovated the
study of food microbial ecology, deepening insight into complex
fermentation systems [83]. Nagalakshmi et al. outlined the tran-
scriptional landscape of the yeast genome based on RNA-Seq
method [84]. Wang et al. applied RNA-Seq to study the tran-
scriptome of Aspergillus oryzae under four different culture condi-
tions. The result indicated higher levels of protein production in
solid-state culture than that in liquid culture [85].
Proteomic research revealed different duplicated genes and
metabolic pathways of Saccharomyces cerevisiae and S. uvarum in
grape must fermentation [86]. In the aspect of authentication,
many types of food have the similar appearance but different
nutritional values, which requires a reliable authentication method.
For this reason, proteomics serves as a valuable tool to discover
reliable biomarkers for authentication. A fast and simple method of
MALDI-TOF/MS was performed to allow a direct comparison and
classification of 33 croatian white wines based on assuming pro-
tein/peptide fingerprints [87]. Another proteomic study based on
liquid chromatographyetriple quadrupole mass spectrometer
(LCeQQQ/MS) revealed lysozyme and its productions can be used
as certified reference materials of wine [88]. By utilizing LCeMS,
casein deriving peptides has been identified as allergenic proteins
markers in fined white wines [89].
Metabolomics has been applied to study traceability, authen-
ticity, production and processing of fermented foods. Several
metabolomic studies were carried out for the investigation of food
metabolic changes during fermentation. For example, Xu
et al. employed LCeMS based metabolomics to investigate
biochemical compositional changes during the microbial fermenta-
tion of Fu brick tea [90]. In addition, metabolomic approaches were
also used for authentication [91], such as GCeMS based metab-
olomics was used to differentiate brewing yeasts [92], Italian buffalo
mozzarella cheese or cow cheese [93], and NMR based metabolomics
for determination of the geographical origin of Kimchi [94].
In conclusion, foodomics has been proven a powerful tool for
many different aspects of food quality. Its high-throughput capa-
bility can improve our capability of food quality, helping the char-
acterization and the definition of specific quality features that make
certain foods unique.
3.3. Food nutrition and human health study
In recent years, we have getting to understand the connections
between our resident microbes and physiology as the increase of
 Y.-J. Xu / Trends in Analytical Chemistry 96 (2017) 14e21
knowledge on human microbiome. Mechanistically, foodstuffs have
been shown to cause alteration in the human gut microbial content,
and to impact human health. In this context, foodomics has made a
significant contribution to food nutritional studies, aimed to un-
derstand how food compositions influence human metabolism and
health, in order to achieve healthier conditions by personalized
balanced diets.
In the field of nutrition, nutritional value of food is influenced in
part by a person's gut microbial community (microbiota) and its
component genes (microbiome). Genomic study demonstrated that
gut microbiome could rapidly respond to altered diet, potentially
facilitating the diversity of human dietary lifestyles [95]. Besides,
genomic analysis foodstuffs revealed adaptations for food utiliza-
tion within host microbiome [96].
Transcriptomics has been proved to be a successful strategy for
understanding the interventions of food composition on human
nutrition. Using transcriptomic approaches, Garrido et al. revealed
the changes of infant gut-associated bifidobacteria in the response
to milk oligosaccharides [97]. The microarrays transcriptomic
studies indicated dietary fatty acids directly impact central nervous
system autoimmunity via the small intestine [98], artificial
sweeteners induce glucose intolerance by altering the gut micro-
biota [99].
In parallel, proteomic approaches can bridge the gap between
the content of particular ingredients in food and their biological
activity for mammals. For example, the proteomic study based on
“bottom-up” strategy indicated that oxyR-dependent proteins
AhpF and Dps in intestinal E. coli in gnotobiotic mice are stimu-
lated by a lactose-rich diet as osmotic and oxidative stress re-
sponses [100]. Another LCeMS/MS analysis identified the
significant changes of several proteins involved in nutrient
transport, energetic metabolism, drug transport, drug metabolism,
immune defense and susceptibility to inflammation in mouse
small intestinal mucosa because of Western-type hypercaloric
high-fat diet (HFD) [101]. Martinez-Medina et al. employed pro-
teomic approaches to reveal western diet induced dysbiosis with
increased E. coli in CEABAC10 mice, altered host barrier function
favoring AIEC colonization [102]. Tachon et al. performed proteo-
mic study to explain diet could alter probiotic Lactobacillus
persistence and function in the intestine [103]. Proteomic analysis
performed on liver, muscle and white adipose tissue of diet-
induced obese mice has demonstrated supplemented fatty acids
not only are effective in reducing fat mass, but also induces liver
steatosis [104].
Metabolomics focuses on two research directions in food
nutrition: characterization of food composition, and the relation-
ship between nutrition and health. Hence, spectroscopy-based
methodologies provide a central, vital tool for the characteriza-
tion of metabolites from food or human gut [105]. In fact, most
dietary compounds currently have been identified based on our
knowledge of food chemistry. However, researchers still face many
hurdles, such as fast identification of hundreds unknown metabo-
lites, accurate quantitation of trace composition and discrimination
of isomers. All of these factors slowed progress and need to be
resolved to bring this emerging field of research to maturity [106].
On the other side, metabolomic studies exposed the relationship
between food composition and physiology, such as high-fat diet
will alter gut microbiota physiology in mice [107], saturated and
unsaturated dietary fats modulate gut microbiome of the ethanol-
induced alcoholic liver disease model [108].
In summary, foodomic technologies are valuable tools for food
nutrition because they allow the identification of bioactive com-
pounds, monitoring of nutritional intervention studies, the mea-
surement of biochemical changes associated with physiology status
related to diet, and the elaboration of molecular mechanisms.
19
4. Conclusions and future outlook
Foodomics has greatly accelerated our understanding of food
safety, traceability, quality, and nutraceuticals. However, there still
remain many shortages and limitations. First, the genomics, tran-
scriptomics and proteomics are potent enough to generate massive
amount of data, but the bottle-neck resides on the metabolomics,
because of the wide diversity of metabolites, the actual limited
knowledge, and the lack of commercial standards for metabolite
identification. Second, each omics technology currently has oper-
ated in self-feature of fragmentation. The integration of all levels of
information to interpret the data generated by these technologies is
still absence in foodomics. In addition, experiments of cytobiology
and molecular biology are rarely used to serve as important com-
plements to foodomic study. In this case, researchers working in
food chemistry, analytical chemistry, biochemistry, microbiology,
molecular biology, food technology, bioinformatics and clinical
sciences should work together, trying to create more favorable
conditions for future development of foodomics.
References
[1] N.N. Potter, J.H. Hotchkiss, Food Science, Springer Science & Business Media,
2012.
[2] F. Cellini, A. Chesson, I. Colquhoun, A. Constable, H.V. Davies, K.H. Engel,
A.M. Gatehouse, S. Karenlampi, E.J. Kok, J.J. Leguay, S. Lehesranta,
H.P. Noteborn, J. Pedersen, M. Smith, Unintended effects and their detection
in genetically modified crops, Food Chem. Toxicol. 42 (2004) 1089e1125.
[3] A.J. Parr, F.A. Mellon, I.J. Colquhoun, H.V. Davies, Dihydrocaffeoyl polyamines
(kukoamine and allies) in potato (Solanum tuberosum) tubers detected dur-
ing metabolite profiling, J. Agric. Food Chem. 53 (2005) 5461e5466.
[4] S. Moco, R.J. Bino, O. Vorst, H.A. Verhoeven, J. de Groot, T.A. van Beek,
J. Vervoort, C.H. de Vos, A liquid chromatography-mass spectrometry-based
metabolome database for tomato, Plant Physiol. 141 (2006) 1205e1218.
[5] A. Cifuentes, Food analysis and foodomics, J. Chromatogr. A 1216 (2009)
7109.
[6] C.A. Browne, T.P. Forbes, E. Sisco, Detection and identification of sugar
alcohol sweeteners by ion mobility spectrometry, Anal. Methods 8 (2016)
5611e5618.
[7] G. Picone, A. Trimigno, P. Tessarin, S. Donnini, A.D. Rombola, F. Capozzi, 1H
NMR foodomics reveals that the biodynamic and the organic cultivation
managements produce different grape berries (Vitis vinifera L. cv. Sangio-
vese), Food Chem. 213 (2016) 187e195.
[8] K. Inoue, C. Tanada, T. Hosoya, S. Yoshida, T. Akiba, J.Z. Min, K. Todoroki,
Y. Yamano, S. Kumazawa, T. Toyo'oka, Principal component analysis of
molecularly based signals from infant formula contaminations using LC-MS
and NMR in foodomics, J. Sci. Food Agric. 96 (2016) 3876e3881.
[9] M. Gallo, P. Ferranti, The evolution of analytical chemistry methods in foo-
domics, J. Chromatogr. A 1428 (2016) 3e15.
[10] T. Acunha, C. Ibanez, V. Garcia-Canas, C. Simo, A. Cifuentes, Recent advances
in the application of capillary electromigration methods for food analysis and
foodomics, Electrophoresis 37 (2016) 111e141.
[11] N. Canela, M.A. Rodriguez, I. Baiges, P. Nadal, L. Arola, Foodomics imaging by
mass spectrometry and magnetic resonance, Electrophoresis 37 (2016)
1748e1767.
[12] A. Vallverdu-Queralt, R.M. Lamuela-Raventos, Foodomics: a new tool to
differentiate between organic and conventional foods, Electrophoresis 37
(2016) 1784e1794.
[13] S.P. Claus, Development of personalized functional foods needs metabolic
profiling, Curr. Opin. Clin. Nutr. Metab. Care 17 (2014) 567e573.
[14] A. Bordoni, F. Capozzi, Foodomics for healthy nutrition, Curr. Opin. Clin. Nutr.
Metab. Care 17 (2014) 418e424.
[15] I. Ortea, A. Pascoal, B. Canas, J.M. Gallardo, J. Barros-Velazquez, P. Calo-Mata,
Food authentication of commercially-relevant shrimp and prawn species:
from classical methods to foodomics, Electrophoresis 33 (2012) 2201e2211.
[16] B. Kabak, A.D. Dobson, Mycotoxins in spices and herbs-An update, Crit. Rev.
Food. Sci. Nutr. 57 (2017) 18e34.
[17] M.L. Marco, D. Heeney, S. Binda, C.J. Cifelli, P.D. Cotter, B. Foligne, M. Ganzle,
R. Kort, G. Pasin, A. Pihlanto, E.J. Smid, R. Hutkins, Health benefits of fermented
foods: microbiota and beyond, Curr. Opin. Biotechnol. 44 (2016) 94e102.
[18] J.M. Jay, Modern Food Microbiology, Springer Science & Business Media,
2012.
[19] P. Nardini, R.A. Nahui Palomino, C. Parolin, L. Laghi, C. Foschi, R. Cevenini,
B. Vitali, A. Marangoni, Lactobacillus crispatus inhibits the infectivity of Chla-
mydia trachomatis elementary bodies, in vitro study, Sci. Rep. 6 (2016) 29024.
[20] C. Parolin, A. Marangoni, L. Laghi, C. Foschi, R.A. Nahui Palomino, N. Calonghi,
R. Cevenini, B. Vitali, Isolation of vaginal lactobacilli and characterization of
anti-candida activity, PLoS One 10 (2015) e0131220.
20 Y.-J. Xu / Trends in Analytical Chemistry 96 (2017) 14e21
[21] C. Leon, V. Garcia-Canas, R. Gonzalez, P. Morales, A. Cifuentes, Fast and
sensitive detection of genetically modified yeasts in wine, J. Chromatogr. A
1218 (2011) 7550e7556.
[22] J. Pevsner, Bioinformatics and Functional Genomics, John Wiley & Sons,
2015.
[23] E.R. Mardis, DNA sequencing technologies: 2006-2016, Nat. Protoc. 12 (2017)
213e218.
[24] E.R. Mardis, Next-generation sequencing platforms, Annu. Rev. Anal. Chem.
(Palo Alto Calif) 6 (2013) 287e303.
[25] S. Goodwin, J.D. McPherson, W.R. McCombie, Coming of age: ten years of
next-generation sequencing technologies, Nat. Rev. Genet. 17 (2016)
333e351.
[26] K. Berlin, S. Koren, C.S. Chin, J.P. Drake, J.M. Landolin, A.M. Phillippy,
Assembling large genomes with single-molecule sequencing and locality-
sensitive hashing, Nat. Biotechnol. 33 (2015) 623e630.
[27] S. Zhang, A.J. Hao, Y.X. Zhao, X.Y. Zhang, Y.J. Zhang, Comparative mito-
chondrial genomics toward exploring molecular markers in the medicinal
fungus Cordyceps militaris, Sci. Rep. 7 (2017) 40219.
[28] A. Weimann, K. Mooren, J. Frank, P.B. Pope, A. Bremges, A.C. McHardy, From
genomes to phenotypes: Traitar, the microbial trait analyzer, mSystems 1
(2016).
[29] F. Ozsolak, P.M. Milos, RNA sequencing: advances, challenges and opportu-
nities, Nat. Rev. Genet. 12 (2011) 87e98.
[30] Z. Wang, M. Gerstein, M. Snyder, RNA-Seq: a revolutionary tool for tran-
scriptomics, Nat. Rev. Genet. 10 (2009) 57e63.
[31] M. Alvarez, A.W. Schrey, C.L. Richards, Ten years of transcriptomics in wild
populations: what have we learned about their ecology and evolution? Mol.
Ecol. 24 (2015) 710e725.
[32] G. Chen, T. Shi, L. Shi, Characterizing and annotating the genome using RNA-
seq data, Sci. China Life Sci. (2016), http://dx.doi.org/10.1007/s11427-015-
0349-4.
[33] J. Keijer, Y.G. van Helden, A. Bunschoten, E.M. van Schothorst, Transcriptome
analysis in benefit-risk assessment of micronutrients and bioactive food
components, Mol. Nutr. Food Res. 54 (2010) 240e248.
[34] M. Larance, A.I. Lamond, Multidimensional proteomics for cell biology, Nat.
Rev. Mol. Cell Biol. 16 (2015) 269e280.
[35] Q. Wu, H. Yuan, L. Zhang, Y. Zhang, Recent advances on multidimensional
liquid chromatography-mass spectrometry for proteomics: from qualitative
to quantitative analysis e a review, Anal. Chim. Acta 731 (2012) 1e10.
[36] S. Sauer, M. Kliem, Mass spectrometry tools for the classification and iden-
tification of bacteria, Nat. Rev. Microbiol. 8 (2010) 74e82.
[37] Y. Zhang, B.R. Fonslow, B. Shan, M.C. Baek, J.R. Yates 3rd, Protein analysis by
shotgun/bottom-up proteomics, Chem. Rev. 113 (2013) 2343e2394.
[38] A.D. Catherman, O.S. Skinner, N.L. Kelleher, Top Down proteomics: facts and
perspectives, Biochem. Biophys. Res. Commun. 445 (2014) 683e693.
[39] A.F. Altelaar, J. Munoz, A.J. Heck, Next-generation proteomics: towards an
integrative view of proteome dynamics, Nat. Rev. Genet. 14 (2013) 35e48.
[40] H. Sedgwick, F. Caron, P.B. Monaghan, W. Kolch, J.M. Cooper, Lab-on-a-chip
technologies for proteomic analysis from isolated cells, J. R. Soc. Interface 5
(Suppl. 2) (2008) S123eS130.
[41] I. Ortea, G. O'Connor, A. Maquet, Review on proteomics for food authenti-
cation, J. Proteomics 147 (2016) 212e225.
[42] A. D'Alessandro, L. Zolla, We are what we eat: food safety and proteomics,
J. Proteome Res. 11 (2012) 26e36.
[43] P. Newsholme, Overview: metabolomics and lipidomics in nutrition and
metabolism research, Essays Biochem. 60 (2016) 407.
[44] Y.-J. Xu, C. Wang, W.E. Ho, C.N. Ong, Recent developments and applications
of metabolomics in microbiological investigations, Trends Anal. Chem. 56
(2014) 37e48.
[45] A.H. Emwas, The strengths and weaknesses of NMR spectroscopy and mass
spectrometry with particular focus on metabolomics research, Methods Mol.
Biol. 1277 (2015) 161e193.
[46] E. Rathahao-Paris, S. Alves, C. Junot, J.-C. Tabet, High resolution mass spec-
trometry for structural identification of metabolites in metabolomics,
Metabolomics 12 (2016) 10.
[47] W.B. Dunn, D.I. Ellis, Metabolomics: current analytical platforms and meth-
odologies, Trends Anal. Chem. 24 (2005) 285e294.
[48] J.M. Cevallos-Cevallos, J.I. Reyes-De-Corcuera, E. Etxeberria, M.D. Danyluk,
G.E. Rodrick, Metabolomic analysis in food science: a review, Trends Food
Sci. Technol. 20 (2009) 557e566.
[49] T. SkOV, S.B. Engelsen, Chemometrics, Mass Spectrometry, and Foodomics:
Foodomics Advanced Mass Spectrometry Modern Food Science and Nutri-
tion, Wiley, Hoboken, 2013, pp. 507e538.
[50] L. Yi, N. Dong, Y. Yun, B. Deng, D. Ren, S. Liu, Y. Liang, Chemometric methods
in data processing of mass spectrometry-based metabolomics: a review,
Anal. Chim. Acta 914 (2016) 17e34.
[51] R. Bao, L. Huang, J. Andrade, W. Tan, W.A. Kibbe, H. Jiang, G. Feng, Review of
current methods, applications, and data management for the bioinformatics
analysis of whole exome sequencing, Cancer Inf. 13 (2014) 67e82.
[52] L. Cocolin, M. Gobbetti, E. Neviani, D. Daffonchio, Ensuring safety in artisanal
food microbiology, Nat. Microbiol. 1 (2016) 16171.
[53] T. Martinovic, U. Andjelkovic, M.S. Gajdosik, D. Resetar, D. Josic, Foodborne
pathogens and their toxins, J. Proteomics 147 (2016) 226e235.
[54] F.I. Rume, A. Affuso, L. Serrecchia, V. Rondinone, V. Manzulli, E. Campese,
P. Di Taranto, P.K. Biswas, C.R. Ahsan, M. Yasmin, A. Fasanella, M. Hugh-Jones,
Genotype analysis of Bacillus anthracis strains circulating in Bangladesh,
PLoS One 11 (2016) e0153548.
[55] T.D. Read, S.N. Peterson, N. Tourasse, L.W. Baillie, I.T. Paulsen, K.E. Nelson,
H. Tettelin, D.E. Fouts, J.A. Eisen, S.R. Gill, E.K. Holtzapple, O.A. Okstad,
E. Helgason, J. Rilstone, M. Wu, J.F. Kolonay, M.J. Beanan, R.J. Dodson,
L.M. Brinkac, M. Gwinn, R.T. DeBoy, R. Madpu, S.C. Daugherty, A.S. Durkin,
D.H. Haft, W.C. Nelson, J.D. Peterson, M. Pop, H.M. Khouri, D. Radune,
J.L. Benton, Y. Mahamoud, L. Jiang, I.R. Hance, J.F. Weidman, K.J. Berry,
R.D. Plaut, A.M. Wolf, K.L. Watkins, W.C. Nierman, A. Hazen, R. Cline,
C. Redmond, J.E. Thwaite, O. White, S.L. Salzberg, B. Thomason,
A.M. Friedlander, T.M. Koehler, P.C. Hanna, A.B. Kolsto, C.M. Fraser, The
genome sequence of Bacillus anthracis Ames and comparison to closely
related bacteria, Nature 423 (2003) 81e86.
[56] W. Duchemin, V. Daubin, E. Tannier, Reconstruction of an ancestral Yersinia
pestis genome and comparison with an ancient sequence, BMC Genomics 16
(Suppl. 10) (2015) S9.
[57] M.P. Barros, V.M. Silveira-Filho, R.H. Lins, M.B. Oliveira, A.M. Almeida,
T.C. Leal-Balbino, Subtyping Brazilian Yersinia pestis strains by pulsed-field
gel electrophoresis, Genet. Mol. Res. 12 (2013) 1294e1302.
[58] K.K. Amoako, M.C. Thomas, T.W. Janzen, N. Goji, Rapid SNP detection and
genotyping of bacterial pathogens by pyrosequencing, Methods Mol. Biol.
1492 (2017) 203e220.
[59] M.L. Ranieri, C. Shi, A.I. Moreno Switt, H.C. den Bakker, M. Wiedmann,
Comparison of typing methods with a new procedure based on sequence
characterization for Salmonella serovar prediction, J. Clin. Microbiol. 51
(2013) 1786e1797.
[60] N.N. Gaudreault, C.E. Mayo, D.C. Jasperson, B.M. Crossley, R.E. Breitmeyer,
D.J. Johnson, E.N. Ostlund, N.J. MacLachlan, W.C. Wilson, Whole genome
sequencing and phylogenetic analysis of Bluetongue virus serotype 2 strains
isolated in the Americas including a novel strain from the western United
States, J. Vet. Diagn. Investig. 26 (2014) 553e557.
[61] S. Kundu, J. Lockwood, D.P. Depledge, Y. Chaudhry, A. Aston, K. Rao,
J.C. Hartley, I. Goodfellow, J. Breuer, Next-generation whole genome
sequencing identifies the direction of norovirus transmission in linked pa-
tients, Clin. Infect. Dis. 57 (2013) 407e414.
[62] L. Ogorzaly, C. Walczak, M. Galloux, S. Etienne, B. Gassilloud, H.M. Cauchie,
Human adenovirus diversity in water samples using a next-generation
amplicon sequencing approach, Food Environ. Virol. 7 (2015) 112e121.
[63] W. Zhang, L. Li, X. Deng, B. Kapusinszky, E. Delwart, What is for dinner? Viral
metagenomics of US store bought beef, pork, and chicken, Virology 468e470
(2014) 303e310.
[64] D.M. Goudeau, C.T. Parker, Y. Zhou, S. Sela, Y. Kroupitski, M.T. Brandl, The
salmonella transcriptome in lettuce and cilantro soft rot reveals a niche
overlap with the animal host intestine, Appl. Environ. Microbiol. 79 (2013)
250e262.
[65] R.C. Fink, E.P. Black, Z. Hou, M. Sugawara, M.J. Sadowsky, F. Diez-Gonzalez,
Transcriptional responses of Escherichia coli K-12 and O157:H7 associated
with lettuce leaves, Appl. Environ. Microbiol. 78 (2012) 1752e1764.
[66] O. Wurtzel, N. Sesto, J.R. Mellin, I. Karunker, S. Edelheit, C. Becavin,
C. Archambaud, P. Cossart, R. Sorek, Comparative transcriptomics of patho-
genic and non-pathogenic Listeria species, Mol. Syst. Biol. 8 (2012) 583.
[67] E.M. Fox, N. Leonard, K. Jordan, Physiological and transcriptional character-
isation of persistent and non-persistent Listeria monocytogenes isolates, Appl.
Environ. Microbiol. 77 (2011) 6559e6569.
[68] X. Deng, Z. Li, W. Zhang, Transcriptome sequencing of Salmonella enterica
serovar Enteritidis under desiccation and starvation stress in peanut oil, Food
Microbiol. 30 (2012) 311e315.
[69] C.K. Fagerquist, W.J. Zaragoza, O. Sultan, N. Woo, B. Quinones, M.B. Cooley,
R.E. Mandrell, Top-down proteomic identification of Shiga toxin 2 subtypes
from Shiga toxin-producing Escherichia coli by matrix-assisted laser
desorption ionization-tandem time of flight mass spectrometry, Appl. En-
viron. Microbiol. 80 (2014) 2928e2940.
[70] S. Jadhav, D. Sevior, M. Bhave, E.A. Palombo, Detection of Listeria mono-
cytogenes from selective enrichment broth using MALDI-TOF mass spec-
trometry, J. Proteomics 97 (2014) 100e106.
[71] A. Gagliardi, E. Lamboglia, L. Bianchi, C. Landi, A. Armini, S. Ciolfi, L. Bini,
L. Marri, Proteomics analysis of a long-term survival strain of Escherichia coli
K-12 exhibiting a growth advantage in stationary-phase (GASP) phenotype,
Proteomics 16 (2016) 963e972.
[72] B. Gilquin, M. Jaquinod, M. Louwagie, S. Kieffer-Jaquinod, A. Kraut, M. Ferro,
F. Becher, V. Brun, A proteomics assay to detect eight CBRN-relevant toxins
in food, Proteomics 17 (2017) 1e2.
[73] C. Piras, P. Roncada, P.M. Rodrigues, L. Bonizzi, A. Soggiu, Proteomics in food:
quality, safety, microbes, and allergens, Proteomics 16 (2016) 799e815.
[74] T. Cajka, M. Vaclavikova, Z. Dzuman, L. Vaclavik, J. Ovesna, J. Hajslova, Rapid
LC-MS-based metabolomics method to study the Fusarium infection of
barley, J. Sep. Sci. 37 (2014) 912e919.
[75] R.S. Zheng, W.L. Wang, J. Tan, H. Xu, R.T. Zhan, W.W. Chen, An investigation
of fungal contamination on the surface of medicinal herbs in China, Chin.
Med. 12 (2017) 2.
[76] J.P. Tamang, K. Watanabe, W.H. Holzapfel, Review: diversity of microor-
ganisms in global fermented foods and beverages, Front. Microbiol. 7 (2016)
377.
[77] E. Ferri, A. Galimberti, M. Casiraghi, C. Airoldi, C. Ciaramelli, A. Palmioli,
V. Mezzasalma, I. Bruni, M. Labra, Towards a universal approach based on
 Y.-J. Xu / Trends in Analytical Chemistry 96 (2017) 14e21
omics technologies for the quality control of food, Biomed. Res. Int. 2015
(2015) 365794.
[78] C.T. Hittinger, A. Rokas, F.Y. Bai, T. Boekhout, P. Goncalves, T.W. Jeffries,
J. Kominek, M.A. Lachance, D. Libkind, C.A. Rosa, J.P. Sampaio, C.P. Kurtzman,
Genomics and the making of yeast biodiversity, Curr. Opin. Genet. Dev. 35
(2015) 100e109.
[79] E. Stefanovic, A. Casey, P. Cotter, D. Cavanagh, G. Fitzgerald, O. McAuliffe,
Draft genome sequence of Lactobacillus casei DPC6800, an isolate with the
potential to diversify flavor in cheese, Genome Announc. 4 (2016).
[80] H. Velly, P. Renault, A.L. Abraham, V. Loux, A. Delacroix-Buchet, F. Fonseca,
M. Bouix, Genome sequence of the lactic acid bacterium Lactococcus lactis
subsp. Lactis TOMSC161, isolated from a nonscalded curd pressed cheese,
Genome Announc. 2 (2014).
[81] P. Ludin, U. von Ah, D. Rollier, A. Roetschi, E. Eugster, Lactic acid bacteria as
markers for the authentication of Swiss cheeses, Chimia (Aarau) 70 (2016)
349e353.
[82] A.R. Borneman, J.M. McCarthy, P.J. Chambers, E.J. Bartowsky, Comparative
analysis of the Oenococcus oeni pan genome reveals genetic diversity in
industrially-relevant pathways, BMC Genomics 13 (2012) 373.
[83] N.A. Bokulich, D.A. Mills, Next-generation approaches to the microbial
ecology of food fermentations, BMB Rep. 45 (2012) 377e389.
[84] U. Nagalakshmi, Z. Wang, K. Waern, C. Shou, D. Raha, M. Gerstein, M. Snyder,
The transcriptional landscape of the yeast genome defined by RNA
sequencing, Science 320 (2008) 1344e1349.
[85] B. Wang, G. Guo, C. Wang, Y. Lin, X. Wang, M. Zhao, Y. Guo, M. He, Y. Zhang,
L. Pan, Survey of the transcriptome of Aspergillus oryzae via massively par-
allel mRNA sequencing, Nucleic Acids Res. 38 (2010) 5075e5087.
[86] M. Blein-Nicolas, W. Albertin, B. Valot, P. Marullo, D. Sicard, C. Giraud,
S. Huet, A. Bourgais, C. Dillmann, D. de Vienne, M. Zivy, Yeast proteome
variations reveal different adaptive responses to grape must fermentation,
Mol. Biol. Evol. 30 (2013) 1368e1383.
[87] D. Re
setar, M. Marchetti-Deschmann, G. Allmaier, J.P. Katalini c, S.K. Paveli
c,
Matrix assisted laser desorption ionization mass spectrometry linear time-
of-flight method for white wine fingerprinting and classification, Food
Control 64 (2016) 157e164.
[88] A. Cryar, C. Pritchard, W. Burkitt, M. Walker, G. O'Connor, M. Quaglia, A mass
spectrometry-based reference method for the analysis of lysozyme in wine
and the production of certified reference materials, J. Assoc. Public Anal. 40
(2012) 77e78.
[89] L. Monaci, I. Losito, F. Palmisano, A. Visconti, Identification of allergenic milk
proteins markers in fined white wines by capillary liquid chromatography-
electrospray ionization-tandem mass spectrometry, J. Chromatogr. A 1217
(2010) 4300e4305.
[90] J. Xu, F.L. Hu, W. Wang, X.C. Wan, G.H. Bao, Investigation on biochemical
compositional changes during the microbial fermentation process of Fu brick
tea by LC-MS based metabolomics, Food Chem. 186 (2015) 176e184.
[91] E. Cubero-Leon, R. Pen ~ alver, A. Maquet, Review on metabolomics for food
authentication, Food Res. Int. 60 (2014) 95e107.
[92] G.A. Pope, D.A. MacKenzie, M. Defernez, M.A. Aroso, L.J. Fuller, F.A. Mellon,
W.B. Dunn, M. Brown, R. Goodacre, D.B. Kell, M.E. Marvin, E.J. Louis,
I.N. Roberts, Metabolic footprinting as a tool for discriminating between
brewing yeasts, Yeast 24 (2007) 667e679.
[93] M.B. Pisano, P. Scano, A. Murgia, S. Cosentino, P. Caboni, Metabolomics and
microbiological profile of Italian mozzarella cheese produced with buffalo
and cow milk, Food Chem. 192 (2016) 618e624.
[94] J. Kim, Y. Jung, Y.S. Bong, K.S. Lee, G.S. Hwang, Determination of the
geographical origin of kimchi by (1)H NMR-based metabolite profiling,
Biosci. Biotechnol. Biochem. 76 (2012) 1752e1757.
21
[95] L.A. David, C.F. Maurice, R.N. Carmody, D.B. Gootenberg, J.E. Button,
B.E. Wolfe, A.V. Ling, A.S. Devlin, Y. Varma, M.A. Fischbach, S.B. Biddinger,
R.J. Dutton, P.J. Turnbaugh, Diet rapidly and reproducibly alters the human
gut microbiome, Nature 505 (2014) 559e563.
[96] D.A. Sela, J. Chapman, A. Adeuya, J.H. Kim, F. Chen, T.R. Whitehead,
A. Lapidus, D.S. Rokhsar, C.B. Lebrilla, J.B. German, N.P. Price, P.M. Richardson,
D.A. Mills, The genome sequence of Bifidobacterium longum subsp. infantis
reveals adaptations for milk utilization within the infant microbiome, Proc.
Nat. Acad. Sci. U. S. A. 105 (2008) 18964e18969.
[97] D. Garrido, S. Ruiz-Moyano, D.G. Lemay, D.A. Sela, J.B. German, D.A. Mills,
Comparative transcriptomics reveals key differences in the response to milk
oligosaccharides of infant gut-associated bifidobacteria, Sci. Rep. 5 (2015)
13517.
[98] A. Haghikia, S. Jorg, A. Duscha, J. Berg, A. Manzel, A. Waschbisch, A. Hammer,
D.H. Lee, C. May, N. Wilck, A. Balogh, A.I. Ostermann, N.H. Schebb, D.A. Akkad,
D.A. Grohme, M. Kleinewietfeld, S. Kempa, J. Thone, S. Demir, D.N. Muller,
R. Gold, R.A. Linker, Dietary fatty acids directly impact central nervous sys-
tem autoimmunity via the small intestine, Immunity 43 (2015) 817e829.
[99] J. Suez, T. Korem, D. Zeevi, G. Zilberman-Schapira, C.A. Thaiss, O. Maza,
D. Israeli, N. Zmora, S. Gilad, A. Weinberger, Y. Kuperman, A. Harmelin,
I. Kolodkin-Gal, H. Shapiro, Z. Halpern, E. Segal, E. Elinav, Artificial sweet-
eners induce glucose intolerance by altering the gut microbiota, Nature 514
(2014) 181e186.
[100] M. Rothe, C. Alpert, W. Engst, S. Musiol, G. Loh, M. Blaut, Impact of nutritional
factors on the proteome of intestinal Escherichia coli: induction of OxyR-
dependent proteins AhpF and Dps by a lactose-rich diet, Appl. Environ.
Microbiol. 78 (2012) 3580e3591.
[101] J.R. Wisniewski, A. Friedrich, T. Keller, M. Mann, H. Koepsell, The impact of
high-fat diet on metabolism and immune defense in small intestine mucosa,
J. Proteome Res. 14 (2015) 353e365.
[102] M. Martinez-Medina, J. Denizot, N. Dreux, F. Robin, E. Billard, R. Bonnet,
A. Darfeuille-Michaud, N. Barnich, Western diet induces dysbiosis with
increased E coli in CEABAC10 mice, alters host barrier function favouring
AIEC colonisation, Gut 63 (2014) 116e124.
[103] S. Tachon, B. Lee, M.L. Marco, Diet alters probiotic Lactobacillus persistence
and function in the intestine, Environ. Microbiol. 16 (2014) 2915e2926.
[104] J.R. Mujico, G.C. Baccan, A. Gheorghe, L.E. Diaz, A. Marcos, Changes in gut
microbiota due to supplemented fatty acids in diet-induced obese mice, Br. J.
Nutr. 110 (2013) 711e720.
[105] W.R. Russell, S.H. Duncan, Advanced analytical methodologies to study the
microbial metabolome of the human gut, Trends Anal. Chem. 52 (2013)
54e60.
[106] A. Scalbert, L. Brennan, C. Manach, C. Andres-Lacueva, L.O. Dragsted,
J. Draper, S.M. Rappaport, J.J. van der Hooft, D.S. Wishart, The food metab-
olome: a window over dietary exposure, Am. J. Clin. Nutr. 99 (2014)
1286e1308.
[107] H. Daniel, A.M. Gholami, D. Berry, C. Desmarchelier, H. Hahne, G. Loh,
S. Mondot, P. Lepage, M. Rothballer, A. Walker, C. Bohm, M. Wenning,
M. Wagner, M. Blaut, P. Schmitt-Kopplin, B. Kuster, D. Haller, T. Clavel, High-
fat diet alters gut microbiota physiology in mice, ISME J. 8 (2014) 295e308.
[108] I.A. Kirpich, J. Petrosino, N. Ajami, W. Feng, Y. Wang, Y. Liu, J.I. Beier,
S.S. Barve, X. Yin, X. Wei, X. Zhang, C.J. McClain, Saturated and unsaturated
dietary fats differentially modulate ethanol-induced changes in gut micro-
biome and metabolome in a mouse model of alcoholic liver disease, Am. J.
Pathol. 186 (2016) 765e776.