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ISSN: 2469-5718

Costa et al. Int J Sports Exerc Med 2017, 3:069


DOI: 10.23937/2469-5718/1510069
Volume 3 | Issue 4
International Journal of Open Access

Sports and Exercise Medicine


REVIEW ARTICLE

Exercise, Nutrition and Gut Microbiota: Possible Links and Con-


sequences
AV Costa1, G Leite1, A Resende1, F Blachier2* and AH Lancha Jr1*
School of Physical Education and Sport, University of São Paulo, Brazil
1

UMR PNCA, Agro Paris Tech, INRA, University Paris-Saclay, Paris, France
2

*Corresponding authors: AH Lancha Jr, School of Physical Education and Sport, University of São Paulo, Brazil, Tel:
+33144088676, E-mail: lanchajr@usp.br;
F Blachier, UMR PNCA, Agro Paris Tech, INRA, University Paris-Saclay, Paris, France, Tel: +33144088675, Fax: +33144081858,
E-mail: francois.blachier@agroparistech.fr

Abstract commensal bacteria have been shown to be able to af-


fect gut metabolism and physiology by several mecha-
Gut microbiota plays an important role in the modulation
nisms, including the production of various bacterial me-
of physiological processes associated with the digestion
of nutrients, immune system and control of energy homeo- tabolites from dietary and endogenous substrates [2].
stasis. Changes in gut microbiota composition have been While carbohydrate fermentation is mainly considered
associated notably with obesity, diabetes, and inflammatory beneficial for the host through the production of Short-
diseases. Diet is one of the major factors capable of modu- Chain Fatty Acids (SCFA) in the intestinal luminal con-
lating the intestinal microbiota composition. In addition, the
literature has shown that exercise can affect the gut micro- tent, protein fermentation gives rise to a wide variety
biota composition and modulate the balance between the of compounds, some of which could be detrimental for
interaction of host and beneficial microbiota. Physical exer- gut health when present at excessive concentration [3].
cise improves the diversity and relative amounts of bacterial Some bacterial metabolites can be transferred through
species under different nutritional contexts. However, the
the intestinal epithelium from the intestinal luminal con-
impact of exercise associated or not with dietary changes
on the gastrointestinal environment and consequences for tent to the portal bloodstream reaching the liver, and
gut health remain poorly understood. Some proposals re- then, to the peripheral blood stream [4]. Some of these
garding the biological mechanisms possibly involved high- metabolites have been shown to be active on different
light the short chain fatty acid production and alteration in tissues, such as in the liver and adipose tissue, by inter-
intestinal pH as main forms by which exercise may affect
gut microbiota composition. Thus, the aim of the present fering with metabolism and physiology [5]. In addition,
review is to present an overview of the effects of physical high fat diet consumption may be capable of promot-
exercise associated with diet on the characteristics of the ing gram-negative bacteria growth and favoring a local
intestinal microbiota. inflammation, which would be harmful for gut health
Keywords [6]. There are several reports regarding the effects of
the diet but, recently, exercise was revealed as another
Exercise, Diet, Gut microbiota, Immune system, Short chain
fatty acid
factor capable of influencing the diversity, composition
and metabolic activity of gut microbiota, as well as its
fermentation capacity and diet SCFA production [6,7].
Introduction The aim of the present review is to present an overview
Gut microbiota is now established as a key player of the effects of physical exercise associated with diet on
in various aspects of health and diseases [1]. Recently, the characteristics of the intestinal microbiota.

Citation: Costa AV, Leite G, Resende A, Blachier F, AH Lancha Jr (2017) Exercise, Nutrition and Gut
Microbiota: Possible Links and Consequences. Int J Sports Exerc Med 3:069. doi.org/10.23937/2469-
5718/1510069
Received: July 13, 2016; Accepted: August 21, 2017; Published: August 24, 2017
Copyright: © 2017 Costa AV, et al. This is an open-access article distributed under the terms of the
Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction
in any medium, provided the original author and source are credited.

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DOI: 10.23937/2469-5718/1510069 ISSN: 2469-5718

Gut Microbiota Composition Nondigested proteins or peptides might also be


substrates for microbial production of SCFA [2]. How-
The human gastrointestinal tract is colonized by ap-
ever, microbial protein fermentation by proteolytic
proximately one trillion microorganisms known as gut
bacteria (for example some bacteria of Clostridium’s
microbiota. This diversity represents a number much
group) yields a diverse range of metabolites, including
larger than human cells [8,9]. Bacterial density varies
Branched-Chain Fatty Acids (BCFA), lactate, and aromat-
along the gastrointestinal tract due to the specific con-
ic components, and amines sulfides, phenols and in-
ditions of each portion, such as differences in the gradi-
doles [22]. Many of these protein fermentation-derived
ent of pH, antimicrobial peptides (including bile acids),
metabolites might have negative consequences on ep-
and in the amount of oxygen, which limits the growth of
ithelial cell metabolism and barrier function, affecting
some bacteria [10].
the host’s gut health [23]. Moreover, high protein diets
Human gut microbiota composition varies since the are usually accompanied by a reduction in carbohydrate
birth up to two years of age, when the birth delivery intake, which may not be beneficial for host health [24].
by vaginal or cesarean mode and early nutrition by Currently, little is known about the effects of protein
breastfeeding or formula milk and the introduction of supplementation, associated (or not) with exercise.
new food modulate initially the microbial populations, Animal fat-rich diets quickly increase the abundance
quantitatively and qualitatively, of the child toward of bacteria resistant to bile acids in humans, such as
adulthood [11,12]. From there, several environmental Bacteroides and Bilophila, which can metabolize differ-
factors, mainly diet, exercise, aging, hygiene, medicine, ent types of bile acids and promote the development
geographic area, pregnancy and the presence or not of of inflammatory bowel disease [25]. Furthermore, con-
some disease will influence the microbial composition sumption of a high fat diet is capable of unbalancing the
in a host-specific way [13,14]. In this complex commu- proportions of Firmicutes/Bacteroidetes, raising Lipo-
nity of bacteria, two phyla appear to be the most pre- polysaccharide (LPS) circulation and the concentration
dominant and common among individuals: Firmicutes of inflammatory cytokines, favoring systemic inflamma-
(60-80%) and Bacteriodetes (15-30%) [15]. The first one tion [25,26].
is the most abundant phylum covering, mainly, Clostrid-
ium, Ruminococcus, Lactobacillus and the butyrate-pro- The Effect of Physical Exercise on the Gut Mi-
ducing bacteria, such as Eubacterium, Faecalibacterium crobiota
and Roseburia, which are known for their abundance in Studies in humans reporting the effects of physical
healthy individuals. The Bacteroidetes phylum is com- exercise on gut microbiota composition, diversity and
posed, primarily, by gram-negative bacteria, including metabolic activity are limited. Clarke, et al. [27] accom-
Bacteroides genus, which is recognized, mostly, for its plished the sole study performed with healthy individu-
contribution to the degradation of complex glycans [16]. als. In this pioneering work, elite rugby players were re-
Furthermore, there are others phyla, which are part of cruited, and, in agreement with several animal studies,
the gut microbiota, but in minor proportion, such as this study reported that athletes displayed an increase
Proteobacteria, Verrucomicrobia, Actinobacteria, Fuso- of the gut microbiota richness and diversity (22 distinct
bacteria and Cianobacteria [17]. phyla), and also a decrease of systemic pro-inflammato-
ry cytokines [27] (Table 1). The authors reported this bi-
The complexity between diet-related gut microbi- ota profile in individuals with exercise training program
ota and intestinal health in athletes as compared to sedentary controls group.
Diet influences gut microbiota composition since it However, the most relevant insight on the effect of
provides senergy, nutrients and oligoelements/micro- exercise on gut composition was provided by exper-
nutrients, which will be used by both the host and in- imental models. Matsumoto, et al. [28] were the first
testinal bacteria. The gut microbiota produces several authors to demonstrate that chronic voluntary physical
vitamins and a range of enzymes, which will ferment exercise is able to change the composition of rat gut mi-
the nutrients that are not digested by human digestive crobiota [28]. Some studies performed afterwards asso-
enzymes [18]. The most abundant SCFAs produced by ciated physical exercise with some pathological states
fermentation of carbohydrates are acetate, propionate or dietary intervention (Table 1).
and butyrate (which constitute > 95% of the SCFA con-
tent). It has been shown that butyrate acts locally on A study performed with polychlorinated biphenyls
intestine by affecting metabolism and gene expression (pollutant model) demonstrated that voluntary physical
in the colonic epithelium [19,20] while acetate and pro- exercise is able to cause changes in the biodiversity and
pionate reach systemic circulation and are utilized by composition of microbiota in mice, and attenuated the
other organs, such as adipose tissue and liver, and con- effects of the pollutant contamination of the microbiota
tribute up to 10% of the energy required by the host [29]. Furthermore, under different dietary conditions,
[21]. Moreover, as weak acids, they also help to main- voluntary exercise appears to reshape the gut microbi-
tain a slightly acidic pH in the proximal colon. ota. Evans, et al. [25] proposed that physical exercise

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DOI: 10.23937/2469-5718/1510069 ISSN: 2469-5718

Table 1: Exercise and microbiota studies.


Reference Exercise Subjects Groups Analyses of gut Results
training microbiota
Matsumoto, et Voluntary Animals Exercised and PCR-TGGE and a Increase of n-butyrate
al. [28] exercise; 5 sedentary sequencing analysis concentrations and butyrate-
weeks group for bacterial DNA and producing bacteria in exercise
HPLC for organic group.
acids
Choi, et al. [29] Voluntary Animals Model of PhyloChip Array Exercise attenuates the decrease
exercise; 5 Polychlorinated of the abundance of bacterial taxa
weeks Biphenyls and the phylum Proteobacteria after
(PCB) PCB-treatment in both groups.
administration Exercise was capable to attenuate
in exercise PCB-induced changes on gut
and sedentary microbiota. Activity level was
groups positively correlated with a shift in
abundance of the microbiota.
Queipo-Ortuño, Voluntary Animals Model of caloric V2-V3 regions 16S Increase of the phylum
et al. [30] exercise; 6 restriction in rRNA, PCR-DGGE Proteobacteria, decrease of
days exercise and and qPCR phyla richness and of the genus
sedentary Bifidobacteria was observed in
groups exercise plus CR group. Moreover,
this group showed increase in
Clostridium and Enterococcus
and decrease of B. coccoides-E.
rectal and Lactobacillus unlike the
changes in exercise group without
CR.
Evans, et al. Voluntary Animals Model of LFD V4 region 16S rRNA, Exercise increased Bacteroidetes
[25] exercise; 12 and HFD in TRFLP and qPCR and decreased Firmicutes in
weeks exercise and both LFD and HFD groups and
sedentary displayed a trend toward to
groups increase Bacteroidetes/Firmicutes
ratio. Actinobacteria levels were
lower in LFD-e than LFD-s. Also,
exercise increased the content of
the families Lachnospiraceae and
Ruminococcaceae and decreased
Lactobacillaceae in both diets.
Kang, et al. [45] Controlled Animals Model of ND V3-V5 regions 16S Exercise was capable to reduce
exercise; 60 and HFD in rRNA, Illumina MiSeq the levels of Streptococcus genus
min/d; 5 d/ exercise and and qPCR in HFD group. Also, there was a
week; sedentary significant increase in Firmicutes
16 weeks groups and decrease in Bacteroidetes
phyla in HFD-e compared to HFD-s.
Petriz, et al. Controlled Animals Control, V5-V6 regions Exercise reduced Streptococcus
[32] exercise; 30 hypertensive 16S rRNA, 454 genus in control rats, increased of
min/d; 5 d/ and obese GS FLX Titanium Allobaculum genus and reduced
week; 4 weeks groups sequencer platform Aggregatibacter and Suturella in
(pyrosequecing) hypertensive rats and increased
Lactobacillus levels in obese rats.
At post exercise, only obese rats
showed more abundance of some
bacteria species.
Lambert, et al. Controlled Animals Diabetic type qPCR Exercise increased the abundance of
[35] exercise; LIT; II and control Firmicutes species (Lactobacillus spp.
5 d/week; 6 groups and Clostridium leptum cluster IV)
weeks and reduced Bacteroides/Prevotella
spp. and Methanobrevibacter spp.
in both control and diabetic groups.
Bifidobacterium spp. was greater
in exercised control but not diabetic
group.

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DOI: 10.23937/2469-5718/1510069 ISSN: 2469-5718

Liu, et al. [31] Voluntary Animals Model of LCR V4 region 16S rRNA, Exercise decreased the abundance
exercise; 11 (Ovariectomized and HCR in Illumina MiSeq of Firmicutes in LCR and increased
weeks female rats) exercise and in HCR group. Also, it was capable
sedentary to increase Proteobacteria and
groups; all Cyanobacteria phyla in LCR, but
groups with decreased in HCR group. At family
HFD level, exercise decreased the
abundance of Ruminococcaceae
and Lachnospiraceae in LCR,
but increased in HCR. Exercise
increased Clostridiaceae and,
mainly, Clostridium genus, in both
exercise groups.
Mika, et al. [34] Voluntary Animals Healthy V4 region 16S rRNA, The juvenile runners, although
exercise; 6 juveniles and qPCR less diverse and richness than
weeks adults with their adults counterparts, showed
exercise and more changes as an increase in
sedentary Bacteroidetes and a decrease in
groups Firmicutes and Proteobacteria
phyla, which remains over 25 days
even without exercise.
Campbell, et al. Voluntary Animals Model of ND TRFLP and 454 GS Allobaculum spp. and Clostridiales
[26] exercise; 12 and HFD in FLX 454 Genome were enriched within the exercise
weeks exercise and Sequencer platform group in ND. Faecalibacterium
sedentary (pyrosequencing) prausnitzi was detected only in
groups exercise groups in both ND and
HFD and Lachnospiraceae was
not present in the HFD-e or HFD-s
groups.
Denou, et al. Controlled Animals Model of ND V3 region 16S rRNA, HIIT increased the overall
[33] exercise; HIIT; and obesity- Illumina MiSeq and richness of the microbiota in the
3 d/week; 6 inducing HFD qPCR colon of obese mice, mainly,
weeks in exercise within Bacteroidetes phylum and
and sedentary Bacteroidales order unlike to the gut
groups microbiota composition in HFD-s
group.
Clarke, et al. No intervention Humans Athletes V4 region 16S Athletes showed a higher
[27] (rugby players) rRNA, 454 Genome richness with less abundance of
and healthy Sequencer Bacteroidetes phylum. The family
untrained FLX platform Akkermansiaceae and the genus
controls (pyrosequencing) Akkermansia showed higher
levels in athletes when compared
to control group with high BMI
and lower levels of Bacteroides,
Lactobacillaceae and Lactobacillus
when compared to control group
with low BMI.
d: day; LIT: Low Intensity Training; HIIT: High Intensity Interval Training; LFD: Low Fat Diet; ND: Normal Diet; HFD: High Fat Diet;
LFD-e: Low Fat Diet plus exercise; LFD-s: Low Fat Diet within sedentary group; HFD-e: High Fat Diet plus exercise; HFD-s: High
Fat Diet within sedentary group; LCR: Low Capacity Running; HCR: High Capacity Running.

modifies the bacterial balance in the gut, with alteration only in the group submitted to exercise, as we observe
of the major phyla levels, and increase of the relative on Evans, et al. [25] research, hence supporting the hy-
proportion of butyrate-producing bacteria (Clostridia- pothesis that exercise causes changes in gut microbiota
ceae, Lachnospiraceae and Ruminococcaceae). The au- independent of changes in diet [26].
thors appoint that the exercise practice would be able
Short term (6 days) voluntary exercise showed that
to prevent the effects of a High Fat Diet (HFD) [25]. In
nutritional status and physical activity alter gut micro-
fact, Campbell, et al. [26] showed that exercise is able
biota diversity in different manners. When exercise is
to modify not only the specific populations of commen-
sal bacteria in the gut, but also cause morphological combinated with food restriction protocol (restricting
changes in gut microenvironment. In the Campbell et al. access for 23 hours per day and confined to running
study [26], the exercised group showed reduced intes- wheels except during a 60 min meal), a negative impact
tinal inflammation due to a high-fat diet and morpho- on bacterial richness is reported with respect to the Lac-
logical characteristics similar to the control. Likewise, in tobacillus and Bifidobacterium genera [30]. The caloric
a previous study, Faecalibacterium prausnitzi and Lach- restriction was also able to modify the phyla, even in
nospiraceae group (a Clostridia-cluster) were detected the presence of exercise [30] (Table 1). It seems that ex-

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DOI: 10.23937/2469-5718/1510069 ISSN: 2469-5718

ercise cannot attenuate the effect of caloric restriction, more plastic and sensitive to environmental changes
whereas it would be able to cause improvements on gut during early life. Then, exercise initiated during the ju-
microbiota composition even under high fat diets. venile period may show a more robust impact on the
Voluntary exercise with different aerobic capacities, gut microbiota than exercise initiated in adulthood [34].
intensity, volume and frequency may present differ- In other words, the changes that occur in childhood may
ent outcomes. Evans, et al. [25] showed a significant last longer even with the absence of exercise than the
increase in the abundance of Bacteroidetes, while the changes occurring later. The authors show that exer-
evidence provided by Liu, et al. [31] showed a reduc- cise-induced alterations in microbiota during early life
tion in the abundance of Firmicutes and Proteobacteria contribute to metabolic consequences such as increased
phylum. Apart from both studies exposing the animals SCFA production, increased energy expenditure and re-
to the same diet (HFD), these differences observed be- duced fat accumulation in the adipose tissue. Indeed,
tween these two studies may originate from the differ- increased Bacteroidetes phyla along with decreased Fir-
ent experimental models used. Liu, et al. [31] study was micutes phyla within the gut have been associated with
performed with ovariectomized female rats fed with these metabolic consequences. The results obtained by
HFD, divided in High Capacity Running (HCR) and Low Denou, et al. [33] reinforce this proposition [33-35].
Capacity Running (LCR), performed 11 weeks of volun- It is important to observe that only one study regard-
tary exercise whereas Evans, et al. [25] performed 12 ing gut microbiota and exercise science was carried out
weeks voluntary exercise in male rats [25,31].
with athletes [27], a population in which the amount of
Petriz, et al. [32] proposed that training status and exercise training is very large and intense, and its out-
intensity may be favorable to the proliferation of spe- comes are different when compared with voluntary ex-
cific families of bacteria [32]. The authors reported an ercise performed in some animals’ protocols or short
inverse correlation between exercise and Clostridiace- session of moderate exercise performed by active indi-
ae/Bacteroideae families and Ruminococus genera, and viduals, as shown in Table 1.
a positive correlation between Oscillospira in exercise
intensity. Aerobic training may be associated with a Possible Mechanisms Connecting Physical Ex-
favorable environment for Clostridiaceae, Bacteroide- ercise and Gut Microbiota
ae and Ruminococus, but an unfavorable environment The effect of exercise on microbiota is still largely un-
for Oscillospira due to acidification of the intestinal known. They are likely to be mediated, at least in part,
environment. The proposition by Petriz, et al. [32] is in by altering parameters that influence the intestinal mi-
agreement with modification of the gut environment croenvironment.
following high intensity or long period exercise. Exer-
cise should modify the environment in a favorable way Short chain fat acids
in terms of anaerobic bacteria population, or acidic en- Exercise may increase butyrate-producing bacteria
vironment since a decrease splanchnic blood flow and species [25,28]. Matsumoto, et al. [28] were the first to
oxygen supply occurs [32]. show that chronic voluntary physical exercise in animals
A recent study performed using High Intensity In- is able to change SCFA production (n-butyrate) in the ce-
terval Training (HIIT), demonstrated that HIIT exerts cum with modifications in butyrate-producing bacteria
opposed changes to the gut microbiota compared to species. In addition, this study reported alteration in the
those imposed by obesity profile. Indeed, HIIT reduces cecal microbiota profile after exercise. These authors
the predicted metabolic genetic capacity of the fecal explain that part of the beneficial effects of exercise re-
microbiota, alters microbiota metabolic pathways, and lated to microbiota and subsequent variations in intesti-
raises the possibility that this type of exercise training nal health may be related to changes in the SCFA profile,
may elicit some of its beneficial effects on metabolism especially for butyrate concentrations [28]. This shift in
through alterations in the gut microbiome [33]. Howev- butyrate bacteria production in exercise group was also
er, this same study did not compare the different types shown by Evans, et al. [25].
of exercise, such as continuous versus intermittent, or
voluntary versus controlled exercise. These parameters The influence of physical exercise on the composi-
should be taken into consideration in future investiga- tion of the microbial environment has been linked to a
tions, since it remains unclear if the different types of decreased pH in the gut from SCFA production. Specifi-
exercise can cause similar beneficial effects regarding cally butyrate promotes cell differentiation and cell cy-
gut microbiota, and intestinal health as suggested by cle arrest, inhibits the enzyme histone deacetylase, and
Liu, et al. and Petriz, et al. [31,32]. decreases the transformation of primary to secondary
bile acids promoting colonic acidification [36]. Changes
Related to the beneficial impact of exercise on the in intestinal luminal pH may modify the environment in
microbiota composition and diversity in the early life, such way that it becomes more favorable for the prolif-
Mika, et al. [34] propose, “The sooner, the better”. This eration of some bacterial species [37].
proposition is related with the fact that microbiota is

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DOI: 10.23937/2469-5718/1510069 ISSN: 2469-5718

Studies also have shown that butyrate may induce stantial changes in the cecal microbiome composition
mucin synthesis [38], and improve gut integrity by in- by stimulating the growth of Firmicutes at the expense
creasing tight junction assembly [34,39,40]. Mucins are of Bacteroidetes; and provoked outgrowth of several
the protective layer consisting of glycoproteins that help bacteria in the Clostridia and Erysipelotrichi classes [44].
forming the mucosal barrier lining of gastrointestinal Antimicrobial activity of the bile acids may elicit selec-
tract. This mucin layer has been recognized to play an tive pressure on the bacterial communities in exercised
important role for the interaction with gut microbiota, mice, leading to a shift of the gut microbiota composi-
and may serve as a substrate for intestinal bacteria, as tion [11].
Akkermansia muciniphila, and may alter the microbial
community composition [41].
Conclusion and Perspectives
Exercise and diet are considered as possible factors
Butyrate production in the large intestine is associ-
ated with production of Heat shock protein 70 (Hsp70). capable of modulating the intestinal balance between
Hsp70 maintains the functional and structural proper- the hosts by independent manners. Exercise has been
ties of intestinal epithelial cells in response to intense shown to improve the diversity of bacterial species and
exercise [42]. Since physical exercise and butyrate stim- richness under different nutritional strategies thus al-
ulate epithelial cell Hsp70 production, this may provide lowing for instance to reduce the negative effects of
structural and functional stability to intestinal epithelial high fat diet. The modification in short chain fatty acids
cells undergoing unfavorable conditions [25] ( Figure 1). production and alteration in intestinal pH appear to be
the main forms by which exercise may affect gut micro-
Bile acids biota composition.
Physical activity has been reported to increase excre- It is important to note that, the studies performed up
tion of primary bile acids in the gastrointestinal tract. to now, used solely the voluntary exercise as model. The
Since butyrate (that has been reported to be increased influence of specific features related to exercise train-
by physical activity) diminishes the conversion of bile ac- ing, such as volume, intensity, types of exercise (aerobic
ids into secondary bile acids, physical activity may con- or anaerobic or combination) may impact gut microbio-
sequently favor the rising of primary bile acids concen- ta in different ways. Likewise, changes in the diet and/
trations in the intestinal luminal content [23]. or different pathological conditions in the experimen-
The primary bile acids have established anti-micro- tal design raise some difficulties in evaluating only the
bial activity. In agreement with this hypothesis, Islam, exercise effect on the gut microbiota composition and
et al. [43] demonstrated that cholic acid induced sub- metabolic activity, as well as in comparing the results

Figure 1: Schematic view representing the possible ways by which physical exercise may impact the gut microbiota. This
includes Short-Chain Fatty Acid (SCFA) production by the microbiota, and bile acid production, as well as related alteration
of the luminal pH. Exercise may also impact gut transit time and intestinal immune response, which in turn may modify the
microbiota composition and metabolic activity.

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obtained in different studies and this may hinder our The universality of maternal microbial transmission. PLoS
understanding. Biol 11: e1001631.
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