Download Intestinal microbiota and metabolites—Implications for broiler

©2013 Poultry Science Association, Inc.
Intestinal microbiota and metabolites—Implications
for broiler chicken health and performance1
T. Rinttilä and J. Apajalahti2
Alimetrics Ltd., Koskelontie 19B, FIN-02920 Espoo, Finland
Primary Audience: Researchers, Nutritionists, Veterinarians
SUMMARY
Microbiota in the intestine of an animal species has evolved together with the host. This
coevolution has produced specific host-microbe combinations, called superorganisms, with the
best possible fitness in a given environment. Intestinal microbiota has an enormous metabolic
potential and it affects both the nutrition and health of the host. The importance of intestinal
microbiota for the performance of broiler chickens has been studied for decades. The microbial
community structure of the cecum is significantly more complex and less well characterized
than that of the crop and small intestine. Culture-independent molecular techniques have recently been introduced to bring fresh insights into the intestinal system of the broiler chicken.
As a consequence, there is growing evidence of connection between the apparent metabolizable
energy of the diet and microbiota composition in the hindgut of the host. This connection can be
due to direct conversion of some dietary components into high-energy metabolites by specialized bacteria. The utilization of such fermentation end products would provide more energy for
the host, which could be measured as improved feed conversion efficiency. However, it is also
possible that cecal microbial profile is a reflection of feed digestion and nutrient absorption efficiency in the proximal intestine. Disorders in these functions cause excess nutrient bypass to
the lower intestine, providing new, easily available substrates for bacteria that could otherwise
not compete in that habitat. The 2 causal links described are likely to coexist in real life situations, but their relative dominance warrants further well-designed studies.
Key words: metabolite, intestinal microbiota, broiler chicken health, broiler chicken performance
2013 J. Appl. Poult. Res. 22:647–658
http://dx.doi.org/10.3382/japr.2013-00742
INTRODUCTION
Microbiota in the animal intestine has evolved
together with the host. As a consequence, the
gastrointestinal tract (GIT) could be considered a metacommunity, comprising many local
microbial communities in different ecological
niches. Each individual gut compartment has its
1
unique physiochemical characteristics and each
location is inhabited by a specialized microbial
composition [1]. The microorganisms inhabiting
the intestinal tract of humans and animals outnumber the cells of a host [2]. The vast majority of gut bacteria reside in the distal intestine,
where densities approach 1011 to 1012 cells/g, the
highest recorded for any microbial habitat [3].
Presented as a part of the Informal Nutrition Symposium “Metabolic Responses to Nutrition and Modifiers” at the Poultry
Science Association’s annual meeting in Athens, Georgia, July 9, 2012.
2
Corresponding author: [email protected]
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The gut microbiota therefore extends the host’s
genome such that the host can be described as
host-microbe superorganism [4].
One of the preconditions for a long-term coadaptation of the gut microbiota is the uninterrupted transfer of maternal intestinal bacteria to
the next generation. If this lineage breaks, the
superorganism ceases to exist and the adapted
microbiota is replaced by a random selection
of bacteria from the environment that are able
to colonize the GI tract. It is worth considering
whether such natural inoculation is achieved
in today’s commercial hatchery systems and
whether the characteristics evolved are desirable
in animal production. For example, microbiota
beneficial for the broiler breeders may not be
ideal for the health and performance of shortlived broiler chickens.
Independent studies carried out with germfree mice and human volunteers have elucidated
that obesity is likely to be associated with the
capability of the colon microbiota to harvest
energy from the diet [5]. Knowledge on the intestinal microbiota of man is mainly motivated
by health applications, one sideline of which is
obesity. However, intestinal health is also highly
important for production animals. When productivity is not threatened by disease, the most
important driver of performance is the capability of the animal to convert feed into carcass as
efficiently as possible. Therefore, the question
arises as to whether the microbiota associated
with obesity in humans could provide us with
information of how to improve energy harvesting and FCR in production animals such as
broiler chickens. Humans have a highly variable genetic background, a unique microbiota
inherited from the mother, and variable dietary
preferences. Thus, finding significant associations between the structure of intestinal microbiota and various phenotypic traits is likely to be
more challenging than finding such associations
in flocks of broiler chickens with a relatively
uniform genetic background, diet, and bacterial
pressure from the environment. In spite of this
apparently easy experimental setting, there is no
consensus regarding the type of microbiota related to an ideal animal performance.
Until recently, intestinal microbiota was
studied using conventional culturing techniques,
which apply differential media to select for spe-
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cific populations of bacteria based on their metabolic requirements. Although the culture-based
techniques enable the recovery of microbial isolates for further biochemical and physiological
investigations under both anaerobic and aerobic
conditions, only a proportion (10–60%) of the
bacterial species present in the intestine are estimated to be cultivable under standard laboratory
conditions [6–9]. To overcome these drawbacks,
culture-independent molecular analysis tecniques have been introduced to obtain a better
understanding of the gut microbiota. However,
in studies involving microbiota analysis, the
complexity of interpretation increases with the
use of applied methods, all of which have inherent biases of varying degrees. Hence, the results
of independent studies with different sample
preparation and analysis techniques need to be
interpreted with caution.
INTESTINAL MICROBIOTA
Establishment of the Intestinal Microbiota
Development of the broiler chicken intestinal
microbiota starts at the moment of hatching. The
newly hatched chicks are initially exposed to
microbes that originate from the surface of the
egg shells, which are populated by bacteria from
the intestine of mother and the surrounding environment. Hence, the microbial inoculum obtained at the early stage of the posthatch period
is critical for the establishment of the gut microbial community. The effect of the first inoculum may last over the entire lifetime of a broiler
chicken by directing the development of the immune system and the intestinal microbiota [10].
Bacterial densities in the chicken GIT have
been shown to increase rapidly after hatching.
In a study by Apajalahti et al. [10], bacterial
numbers in the proximal and distal intestine of
the broiler chicks reached 108 and 1010 cells/g
of digesta 1 d posthatching, respectively. The
maximum density of 109 cells/g of ileal digesta
and 1011 per gram of cecal digesta was reached
less than 1 wk, after which the microbiota remained relatively stable for the following 30 d.
The GIT is initially colonized by facultative aerobes such as Enterobacteriaceae, Lactobacillus,
and Streptococcus, as the intestinal environment
of chicks shows a positive oxidation or reduction potential at hatching [11–14]. However,
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oxygen consumption by these bacteria alters the
lower gut environment to more reducing conditions, which facilitates subsequent growth and
colonization of the extremely oxygen-sensitive
obligate anaerobes [11, 13, 15].
Microbial Community of the Upper GIT
The small intestine, which consists of the
duodenum, jejunum, and ileum, is the GIT
compartment where most of the digestion and
absorption of nutrients occurs [16]. Bacteria in
the small intestine use the same readily fermentable nutrients that are being used by the host.
Therefore, the small intestine is a gut compartment where commensal microbiota and the host
compete for dietary nutrients [17]. The host can
recover part of the energy lost to microbes by
absorbing and metabolizing bacterial fermentation products, lactic and volatile fatty acids
(VFA). Due to the low pH and rapid passage
of intestinal contents, duodenal bacterial counts
are low. Subsequently, digesta flows from the
duodenum through the jejunum to the end of the
ileum, where the digestive enzyme activities are
reduced and bile acids are deconjugated [18]. As
a consequence, the bacterial numbers increase
up to 108 cells/mL of digesta in the distal ileum
[10]. With methods based on sequencing of specific DNA fragments, there is relatively good
consensus of the microbial community structure
of the in the chicken small intestine [12, 19–24].
By far the most dominant bacteria are lactobacilli, which represent 80 to 90% of the total
microbiota, the remainder mainly consisting of
enterobacteria and enterococci. The most dominant cecal bacteria are also found in the distal
ileum. It is possible that these bacteria enter the
ileum during cecal emptying or reverse peristalsis and are not metabolically active in the small
intestine.
Microbial Community of the Lower Intestine
Due to the low redox potential prevailing distal intestine, the numbers of obligate anaerobic
microbes are several orders of magnitude higher
than those of aerobes or facultative anaerobes
[25]. Dietary compounds and intestinal secretions that are not absorbed in the small intestine
reach the lower intestine, where they provide the
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dense microbial population with nutrients and
energy for growth [26]. Hence, intense bacterial
fermentation in the hindgut does not lead to energy losses for the host, as these bacteria scavenge energy and nutrients from feed residues
that are already beyond the endogenous digestion system of the host. Accordingly, any bacterial metabolites produced from such residues
that have any value for the host will improve the
yield of overall energy and nutrient capture from
the diet. It is possible that with poorly digestible
diets, a considerable proportion of total dietary
energy comes from bacterial fermentation.
In recent years, the application of 16S ribosomal (r) RNA gene sequencing approaches
has provided new insights into characterization
of the broiler chicken cecal microbial composition [21, 23, 27]. Several studies have revealed
that cecal microbiota in healthy chickens is
dominated by representatives of the order Clostridiales. For a long time, representatives of
this order were grouped according to their 16S
rDNA sequence homology to Clostridial clusters I to XIX. During the last few years, several
bacterial phylotypes that previously could not
be assigned to proper taxonomic clusters have
now found a place in newly described families
and genera. In the chicken cecum, the most
common families within the order Clostridiales are Lachnospiraceae, Ruminococcaceae,
and Veillonellaceae [27]. These appear to represent more than 50% of the cecal bacteria, the
remainder belonging mainly to the orders Bacteroidales and Lactobacillales [20, 28]. The
genus Clostridium is well known to people involved in the poultry industry, mainly because
of one pathogenic species, Clostridium perfringens. Unfortunately, this species has affected
the reputation of the entire order Clostridiales,
even though the genus Clostridium is only 1
of 123 genera within the order and the species
C. perfringens is only distantly related to the
majority of the 129 species in the genus Clostridium. Therefore, the generic term clostridia
should not be automatically associated with
poor health and performance in broiler chickens. In fact, all the existing evidence suggests
that the great majority of the bacteria belonging
to the bacterial class Clostridia are nonpathogenic, and even beneficial for animals and for
farm profits.
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Functions of the Gut Microbiota
The conventional view that all microorganisms cause disease has been replaced by the
insight that most microbe-host interactions are
commensal (with the microbes benefiting while
the host is unharmed) or even mutualistic (in
which both partners benefit) [1]. The benefits of
commensal intestinal bacteria are well known:
they help in digestion and synthesis of dietary
compounds; are involved in the gastrointestinal development; regulate intestinal epithelial
proliferation, inflammatory immune responses,
and host energy metabolism; synthesize vitamins; and fill a microbiological niche that might
otherwise be colonized by potentially harmful
enteric microorganisms [29–33]. In return, the
intestinal microorganisms are provided with secure growth conditions and a constant stream of
nutrients [2].
The diet-derived complex carbohydrates
not degraded in the small intestine, such as
nonstarch polysaccharides (NSP) and resistant
starch, are the main sources of carbon and energy for the commensal microbiota in the lower
intestine. Dietary protein and protein from pancreatic enzymes and gastrointestinal secretions
also contribute, to some extent, to the supply of
substrates to intestinal bacteria [26]. In addition,
the gut microbiota degrades and processes large
quantities of substances derived from the host,
such as mucins and sloughed epithelial cells.
Hence, the intestinal microbiota has a substantial catalytic potential, which leads to the formation of microbial metabolites with beneficial or
adverse health effects. The amounts and types
of fermentation products formed by intestinal
bacteria depend on the relative amounts of each
substrate available and the fermentation strategy
(biochemical characteristics and catabolite regulatory mechanisms) of bacteria involved in the
fermentation process [34].
Importance of Short-Chain Fatty Acids
The principal end products of intestinal microbial fermentation are short-chain fatty acids
(SCFA), such as acetate, butyrate, propionate,
succinate, and lactate [21, 35, 36]. Human studies have shown that up to 95% of the SCFA
produced during carbohydrate fermentation are
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used by the host, providing 5 to 15% of the total
energy requirements; whereas pigs may obtain
as much as 30% of their energy from SCFAproducing hindgut fermentation [37, 38]. Ruminants obtain almost all their energy from SCFA
produced in the rumen. In addition to energyyielding activity, SCFA formation in chicken
cecum reduces pH of the intestinal environment,
which may inhibit acid-sensitive pathogenic
bacteria, such as members of the family Enterobacteriaceae, by dissipating the proton motive
force across the bacterial cell membrane [39].
Among the SCFA, butyrate has gained particular interest, as it is the preferred energy source
for the enterocytes and is known to regulate cellular differentiation and proliferation within the
intestinal mucosa, thereby increasing intestinal
tissue weight [40, 41]. The epithelium provides
a highly selective barrier that prevents the passage of toxic and proinflammatory molecules
from the external milieu into the submucosa and
systemic circulation [42]. Hence, the contribution of butyrate and other SCFA to epithelial
development is essential in the maintenance of
normal intestinal barrier functions. Although
butyrate production is distributed across many
Clostridial clusters of the phylum Firmicutes
[43], it is mainly produced by members of Roseburia spp. and Eubacterium rectale, both members of the family Lachnospiraceae, as well as
by Faecalibacterium prausnitzii-like organisms
of family Ruminococcaceae [21, 44, 45]. These
bacterial groups are susceptible to changes in
dietary carbohydrate intake, which has an effect
on lower intestine butyrate concentrations [46].
Lactic acid is the strongest of the common
SCFA produced by GIT bacteria, and therefore
it tends to reduce residual pH more than other
SCFA. Lactate produced by lactic acid bacteria
is rarely present in the hindgut in high quantities, as it is normally rapidly absorbed from the
intestine or used as a substrate for lactate-utilizing bacteria, such as representatives of the genera Eubacterium, Anaerostipes, Veillonella, and
Megasphaera [47, 48]. However, human studies
have shown that, in certain conditions, abnormal
accumulation of lactic acid occurs as a result of
carbohydrate malabsorption in the upper intestine and subsequent overgrowth of lactic acidproducing bacteria due to increased delivery of
readily metabolized carbohydrates to the lower
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intestine [49]. Consequently, production of lactic acid exceeds the buffering and absorptive
capacity of the colon and the pH of the habitat
decreases, with concomitant inhibition of the
activity of lactate-utilizing microorganisms.
This cascade of events may eventually lead to
impaired well-being of the host. There is only a
little evidence of the lactic acid accumulation in
chicken cecum. Taylor [50] discovered elevated
d-lactic acid concentrations in the hindgut of the
laying hens caused by sudden changes in diet
type or processing.
Protein and Amino Acid Fermentation
in the Lower Intestine
The lower intestine of warm-blooded animals
has been described as a site of intense protein
turnover [51]. The active proteolytic microbial
community in the hindgut includes species belonging to the genera Bacteroides, Clostridium,
Fusobacterium, Streptococcus, and Enterococcus [52]. Once carbohydrate sources are exhausted in the broiler chicken cecum, sources of
protein material are fermented and metabolized
to salvage energy. Although proteins and amino
acids provide a less significant energy source in
the lower intestine, their importance lies mainly
in the formation of potential systemic toxins and
carcinogens as a result of protein or amino acid
fermentation by putrefactive bacteria. Common
examples of undesired metabolic end products
include phenols and indoles (as a result of anaerobic fermentation of the aromatic amino acids,
tyrosine and tryptophan, by intestinal bacteria),
ammonia (as a result of oxidative or reductive
deamination of amino acids), and amines (as
a result of amino acid decarboxylation in the
gut). Ammonia is easily absorbed through the
intestinal epithelium into the blood circulation
of broiler chickens and has toxic effects on enterocytes, whereas amines have been associated
in several physiological processes in living cells
[53, 54].
In addition to being toxic to the host, these
end products of protein fermentation tend to
increase the pH of the intestinal contents. The
general assumption is that low pH is beneficial
for gut health, as the growth of the acid-sensitive pathogenic microorganisms is suppressed
in such conditions [17]. As the bacteria gener-
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ally favor fermentable sources of carbohydrates,
protective measures against excessive putrefactive activity and the undesired metabolites in the
hindgut can be achieved by adding dietary fiber
in the diet or limiting the intake of poorly digested proteins.
Role of Intestinal Microbiota
Against Enteric Pathogens
The mucosal surface of the broiler chicken
GIT is the largest body surface in contact with
the external environment. It is a complex ecosystem combining the gastrointestinal epithelium, immune cells, and resident microbiota [55].
The host is normally protected by the physical
barrier created by colonized commensal microbes, which protects the epithelium from attack by invading harmful microorganisms or
opportunistic species usually present in the gut
in low numbers. However, the intestinal mucosa
can be exposed to various enteric pathogens. In
the first step of the infection process, pathogenic
microorganisms adhere to the brush border of
intestinal cells, enabling them to exploit the underlying signaling pathways [56, 57]. Furthermore, some enteric microbial pathogens have
developed specialized systems to produce virulence factors. After normal host-cell processes
have been weakened, these systems enable the
pathogen to penetrate and cross the epithelial
barrier [58]. The enteric microbial pathogens
commonly target the host cell cytoskeleton during the cell penetration step. It is exploited for
various purposes, such as gaining entry into
cells, moving within and between cells, and
forming vacuoles to create a specialized niche,
which facilitates the pathogen’s chances of survival and ability to proliferate [59].
The role of the commensal GIT microbiota in
suppressing pathogen colonization is likely to be
multifactorial. In addition to the production of a
wide variety SCFA, which are bacteriostatic for
a subset of bacterial species either directly or by
reducing pH of the intestinal environment, the
commensal microbiota contribute to the colonization resistance against pathogenic microbes.
Moreover, some members of the microbiota also
generate bacteriocins, small peptide molecules
with microbicidal or microbiostatic properties
[60]. In addition, intestinal microbes apply a
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delicate microbe-to-microbe signaling network
against pathogenic invaders, as well as using
it to optimize the composition and numbers of
appropriate members of the microbial ecosystem. This coordinated bacterial communication, termed quorum sensing, can occur within
a single bacterial species or between diverse
species, and enables the regulation of different
processes, especially when environmental conditions are appropriate [61]. A variety of different molecules can be used as signals. Common
classes of soluble signaling molecules include
oligopeptides in gram-positive bacteria, N-acyl
homoserine lactones in gram-negative bacteria,
and a family of autoinducers known as autoinducer-2 in both gram-negative and positive bacteria [62].
Cecal Microbial Community
and Metabolizability of Dietary Energy
The composition of the broiler chicken microbial community is likely to be affected by the
source of the microbes that first meet the virgin
intestine by the diet. If hatching takes place in
an environment where the microbial load has
been minimized, individual chicks may pick
up a random inoculum from their surroundings,
which may lead to differences in the intestinal
physiology of individual birds in a flock. It is
worth noting that intentional inoculation of the
chicks with a competitive exclusion culture at
hatch might render a flock more uniform, not
only with regard to microbiota composition, but
also to FCR.
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In our studies on microbiota of the chicken
intestine over the years, it has become apparent
that on farms with good health and FCR history, the between-bird variability of the dominant microbial community is small, whereas on
problem farms the flock is less uniform. Figure
1 clearly illustrates this. Ten commercial Finnish
farms were randomly sampled for microbiota
analysis 3 wk after arrival of the chicks. Three
pools of 3 birds per farm were analyzed for cecal microbiota structure by a PCR-independent
DNA-based method that fractionates total bacterial chromosomes according to their guanine +
cytosine content (G+C). Three weeks later, the
flock was taken to slaughter and carcass weights
were recorded for each farm. Final FCR was
calculated and compared against the G+C profiles. The results clearly demonstrated that, on
farms with better overall FCR, the variability in
the cecal microbiota composition 3 wk before
slaughter was much lower than on farms with
poorer FCR.
It is intriguing to think that on any farm there
may be individual birds that have highly different efficiency to convert diet into body mass.
The flock may appear uniform in size, but some
animals may consume much more feed than others. The farm- and flock-specific situation can
be revealed by determining a variability index
by G+C profiling.
In a study carried out by McCracken at
Queen’s University (Belfast, Northern Ireland),
broiler chickens were individually caged, fed
with the same wheat-based diet, and analyzed
Figure 1. Chicken cecal microbial profiles arranged according to the FCR of the farm from which they originated.
Bacterial profiles from 5 farms with the lowest FCR are on the left and those from 5 farms with the highest FCR on
the right. G+C = guanine + cytosine.
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for metabolizable energy from 7 to 28 d. Cecal
bacterial profile was determined by G+C profiling and compared against the ability of the individual chicken to harvest energy from the diet.
It was found that metabolizable or gross energy
was significantly different between individual
birds, ranging from less than 60 to more than
80%, and there was no good correlation between
FCR and BW gain [63]. Figure 2 shows the microbial profiles of the 8 most efficient birds in
terms of energy harvesting and the 8 least efficient birds. There was a highly significant correlation between cecal microbial community
structure and the energy harvesting efficiency
of the host. Cecal bacteria from the most efficient birds were dominated by bacteria with
G+C content around 45%. In inefficient birds,
this peak was replaced by 2 major peaks, representing bacteria with G+C content around 37
and above 60%, respectively.
These 2 totally independent studies demonstrated that cecal bacterial composition was
similarly related to FCR on commercial farms
in Finland and to metabolizable energy at the experimental facility in Northern Ireland. In both
cases bacteria with G+C ~45% represented birds
with good performance, whereas an increased
proportion of bacteria with G+C ~37% and
~65% represented broiler chickens with reduced
efficiency to harvest energy from the diet and
convert feed into carcass mass.
Chromosomal DNA representing the diagnostics peaks of the G+C profiles was collected
and analyzed in more detail by 16S rRNA gene
sequencing to identify the actual bacterial phy-
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lotypes behind the shifts in the G+C profiles.
Eight taxonomic units were identified and a
rapid quantitative real-time PCR assays were
designed for their quantification. The abundance
of these bacterial groups was used to design an
algorithm that correlated with performance.
The algorithm provided a value referred to as
Performance-linked Microbial Index (PMI),
which was first applied to all samples from the 2
studies. In Figure 3, the PMI values are plotted
against FCR and ME/gross energy. As expected,
FCR and PMI showed a highly significant negative correlation, whereas ME and PMI showed a
positive correlation.
The association of broiler chicken gut microbiota and bird performance as measured by FE
was also investigated in a study by Torok et al.
[27]. Three feeding trials were performed in various geographic locations with differences in diet
composition, broiler breed, and bird age. The results of the gut microbial profiling with terminal
restriction fragment length polymorphism technique revealed 8 common performance-linked
operational taxonomic units within both the ilea
and ceca across the trials. Targeted 16S rRNA
gene cloning and sequencing of these operational taxonomic units revealed that they represented 26 bacterial species or phylotypes, which
clustered phylogenetically into 7 groups related
to Lactobacillus spp., Ruminococcaceae, Clostridiales, Gammaproteobacteria, Bacteroidales,
Clostridiales, or Lachnospiraceae, and unclassified bacteria or clostridia. Some of the potential performance-related phylotypes showed
high sequence identity with classified bacteria
Figure 2. Chicken cecal microbial profiles of individually caged birds arranged according to diet metabolizability.
The profiles on the left are from the 8 birds with the highest metabolizability and those on the right from the 8 birds
with the lowest metabolizability. The black line in each diagram represents the mean of the 8 profiles. GE = gross
energy; G+C = guanine + cytosine.
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Figure 3. Relationship between performance-linked microbial index and feed utilization efficiency expressed as
FCR (upper panel) and ME (lower panel). GE = gross energy.
such as Lactobacillus salivarius, Ruminococcus
torques, and Faecalibacterium prausnitzii. It is
also noteworthy that birds on diets exhibiting
significantly lower performances in this study
generally showed more pronounced betweenbird variation in gut microbial communities.
As demonstrated by the trials described
above, there is a correlation between cecal microbiota composition and the efficiency of the
host to extract energy from the diet and to deposit that energy into improved FCR. However,
the question of how the intestinal bacterial community composition relate to relevant metabolic
changes and to broiler chicken performance is
not completely understood. Turnbaugh et al.
[64] discovered in a study with obese and lean
twins that obese individuals had a larger proportion of genes for digesting fat, protein, and
carbohydrates, which possibly facilitates their
ability to extract and store energy from food.
Furthermore, the same researchers demonstrated that the transfer of microbes from a conventional mouse to a germ-free individual led to different energy-harvesting efficiency depending
on whether the inoculum was derived from an
obese or a lean mouse, suggesting that specific
microbes are able to provide the host with an
energy-efficient phenotype [5]. Consequently, it
is likely that certain microbial species or groups
in the gut microbiome encode substantial specialized metabolic capacities, including the efficient degradation of otherwise indigestible components of the diet with subsequent production
of SCFA. As mentioned previously, SCFA are
a valuable energy source for the host, with butyrate being especially important as a preferred
energy source for the intestinal epithelium, thus
ensuring that dietary nutrients and high-energy
SCFA are taken up by the host at the best possible efficiency. Accordingly, butyrate-producing
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representatives of the bacterial order Clostridiales can be expected to be especially beneficial
for the animal performance.
An alternative explanation for the connection between FCR and the composition of cecal
microbiota is that digestive disorders or compromised absorption of nutrients in the small
intestine results in an abnormal nutrient bypass
to the lower intestine. Hence, dietary components, which under normal circumstances would
be digested and absorbed in the upper intestine,
fail to do so for some reason. This could be a
consequence of epithelial damage caused by
coccidiosis, necrotic enteritis, or a high level of
antinutritional lectins in the diet. It is also possible that an exceptionally high passage rate of digesta leads to poor nutrient absorption and high
nutrient bypass [65]. Poor nutrient absorption
reduces FCR and, simultaneously, the overflow
of nutrients to the lower intestine favors bacteria
that grow rapidly on easily available substrates.
In such situations, a correlation between FCR
and cecal microbiota is apparent but the favored
bacteria do not directly affect FCR. Instead, the
shift in microbiota composition is a reflection of
reduced nutrient absorption.
It is most likely that both of the abovementioned causal links exist in real life situations.
Even though there are 2 clearly different mechanisms, they are not mutually exclusive and most
likely coexist. In the ideal situation, the main dietary nutrients, starch and protein, are effectively digested and absorbed in the small intestine.
The only dietary components that reach cecum
are NSP, which are hydrolyzed and metabolized
by cecal bacteria to high-energy SCFA, with a
sufficient proportion of butyrate. In this situation the proportion of bacteria capable of utilizing NSP is high, and butyrate-producing bacteria
of the order Clostridiales are well represented.
POTENTIAL STRATEGIES
TO OPTIMIZE CECAL
MICROBIOTA COMPOSITION
There is mounting evidence that intestinal
microbiota of the broiler chickens is associated with good animal performance. However,
if poor bacterial profile cannot be transformed
into a good profile, with a concomitant improvement in animal performance, this knowledge has
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no practical value. If optimization of microbial
balance in the cecal environment leads to good
performance, it would be of great importance to
establish or develop strategies to provide a competitive advantage for representatives of taxa
identified as being beneficial or taxa providing similar functions. There are many potential
ways of achieving this. One option could be to
develop starter cultures that directly provide the
most important bacterial species. This is challenging because the desirable beneficial bacteria
are strict anaerobes. Such products are commercially available for ruminants (e.g., Megasphaera elsdenii), but significant development
work is required for poultry applications.
An alternative to early inoculation is to provide dietary ingredients that favor the growth
of the desirable bacteria. In principle, it is possible to affect microbial balance by nutritional
strategies including an appropriate selection of
the main feed raw materials. In addition, various
special feed additives, such as prebiotics, feed
enzymes, and other products that potentially
provide substrates for the NSP-digesting and
SCFA-producing cecal bacteria, could serve as
efficient microbiota modulators and indirectly
inhibit the growth of pathogenic bacteria.
In some cases it is possible that cecal microbiota composition does not directly affect FCR,
but only reflects feed digestibility, conditions in
the proximal intestine, and consequent nutrient
bypass to the cecum. In such cases, the potential use of knowledge obtained is different. One
approach to use that information could be in
diagnostic testing on the farm to determine the
intestinal condition and uniformity of the flock.
In wider farm surveys, common factors that lead
to a lack of between-bird uniformity and ways to
improve the situation could be identified. With
early diagnosis, it could even be possible to take
corrective actions before the birds are slaughtered.
CONCLUSIONS AND APPLICATIONS
1. Growing evidence exists of a connection between good animal performance
and microbiota composition in the lower
GIT of broiler chickens.
2. More well-designed research is warranted to investigate the influence of dietary
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factors on physiology and metabolism of
the microorganisms residing in the intestinal tract, as well as on absorption of
fermentation end products.
3. Today, numerous potential in vitro methods are available for prescreening a wide
range of dietary ingredients under laboratory conditions for the properties described in this paper.
4. It is essential that the microbial modulators with the most potential would be
tested in in vivo broiler chicken feeding
trials to elucidate the interactions of the
dietary composition and microbial fermentation, especially with regard to animal health and performance.
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