Gastrointestinal tract microbiota and probiotics in production animals.

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Gastrointestinal Tract Microbiota and Probiotics in Production Animals Carl J. Yeoman1 and Bryan A. White2 1

Department of Animal and Range Sciences, Montana State University, Bozeman, Montana 59717-2900; email: [email protected]

2

Department of Animal Science, University of Illinois, Urbana, Illinois 61801; email: [email protected]

Annu. Rev. Anim. Biosci. 2014. 2:469–86

Keywords

First published online as a Review in Advance on October 16, 2013

gut, health, dysbiosis, probiotics, agriculture, microbiome

The Annual Review of Animal Biosciences is online at animal.annualreviews.org

Abstract

This article’s doi: 10.1146/annurev-animal-022513-114149 Copyright © 2014 by Annual Reviews. All rights reserved

The gastrointestinal tract (GIT) microbiomes of production animals are now firmly established as a key feature underscoring animal health, development, and productivity. In particular, early gut colonization is critically important to the morphological and immunological development of the GIT, development of a functional fermentative environment, and neonatal resistance to pathogenic challenge. Although perturbations of an animal’s GIT microbiome at any age can have profound consequences, perturbations during early GIT development can be particularly severe and result in significant and long-lasting sequelae. As the GIT microbiome matures, it exhibits significant diversity, ostensibly an important indicator of ecosystem health. Recognition of the immense importance of the GIT microbiota to the host has led to the development of probiotic and prebiotic feedstuffs with the express aim of ensuring animal health. We herein review the current collective understanding of the GIT microbiota of production animals.

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INTRODUCTION


Microbiome: used here to represent the collection of autochthonous microbes occupying a defined environment (e.g., the gastrointestinal tract) Microbiota: used here to represent the complete microbial community (autochthonous and allochthonous) that occupies a defined environment (e.g., the gastrointestinal tract)

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When Antonie van Leeuwenhoek first observed microbes in the 1670s (1), he could not have known how important these “animalcules” were to life on earth. This importance did not escape the genius of Carl Woese, who concluded, “if you wiped all multicellular life forms off the face of the earth, microbial life might shift a tiny bit . . . If microbial life were to disappear, that would be it—instant death for the planet” (2). In the approximately 340 years since van Leeuwenhoek’s discovery, we have learned just how significant and immense microbial life is. Microbes are estimated to number more than 4 3 1030 cells throughout the earth’s biosphere (3); therefore, microbes outnumber all of the stars in the observable universe (4). Therein they play integral roles in the biogeochemical cycles on earth (5, 6), including in carbon (7) and nitrogen (8) cycles, and have significant impacts on the climate (9) and perhaps even the weather (10). However, it is their endo- and ectosymbiotic association with mammals and impacts on the nutrition, health, and development of humans and other animals that has been of particular interest in recent years. Understanding of the microbiology of production animals began with Robert Hungate. Hungate began his career interrogating microbial cellulolysis in termites before switching his attentions to the microbial ecology of the rumen (11). Hungate’s pioneering anaerobic culturing techniques led to him being described by many as the father of rumen microbiology (12). Work by Hungate and other great pioneers like Marvin Bryant, Burk Dehority, Peter Hobson, Colin Orpin, Jim Russell, and Meyer Wolin paved the way to our current knowledge. More recent discoveries indicate that culture-based techniques may overlook as much as 99% of the total microbial richness present in a biome (13). This, coupled with technological advances that have enabled us to explore these same ecosystems independent of culture, and at unprecedented levels (14), has reinvigorated research into the rumen. Furthermore, the discovery that the gastrointestinal tract (GIT) microbiome makes mutualistic contributions beyond fibrolytic activity has spurred research of non-ruminant production animals, including swine (15), gallinaceous fowl (chickens and turkeys) (16), and the rapidly expanding aquaculture industry (17). Technological advancements, particularly genomic-based techniques, have enabled us to catalog the microbial constituents of the gut, determining both their interspecific (18, 19) and intraspecific compositions (20), and to examine the elements that underscore the horizontal transmission of genetic material, by virtue of the viriome (21, 22) and the plasmidome (23). In addition to determining which microbial taxa are present, these same technologies have enabled us to interrogate the individual and collective genetic capabilities (i.e., the metagenomes) of GIT microbes (24), along with their individual (25) and collective transcriptional responses [i.e., their metatranscriptomes (26)]. All of these efforts promise a more intricate understanding of the ecology and the various biochemical contributions of the microorganisms that colonize the GITs (the GIT microbiomes; see sidebar, Coming to Terms) of production animals as well as their physiological contributions to the host. Abundant and diverse microbiota are detected in the GITs of all mammals. In humans, microbial cells present in the GIT outnumber our own cells by approximately 10 to 1. In ruminants and swine, this ratio is likely to be much higher owing to a greater proportional representation of the GIT to the animal’s anatomy (27). Mature ruminants and swine harbor an estimated 300 to 1,000 unique species (28–30). However, molecular analyses up to November 2010 had observed 5,271 different bacterial and 3,516 archaeal species-level operational taxonomic units (OTUs, 16S rRNA gene sequences sharing a researcher-defined proportion of identical nucleotides; in this study the sequences shared 97% sequence identity) across rumen surveys (19), consistent with the variable compositions observed. For gallinaceous fowl, a more diverse microbiota is predicted, with estimates of more than 2,200 species-level OTUs (31, 32), although just 915 OTUs in the chicken and 464 OTUs in the turkey have been described (33).

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Greater microbial diversity in the gallinaceous fowl GIT may reflect their less-active innate and humoral immune systems (34, 35). However, caution must be used when interpreting these numbers in the context of a resident microbiome, as ecological surveys based on DNA do not distinguish transitory allochthonous microbes from resident microbes, nor do they distinguish intact live from dead or lysed cells. GIT microbiota exhibit a clearly delineated biogeographical distribution. Microbial densities and diversity vary along the length of the GIT, being maximal in the pregastric rumen (36), the postgastric cecum (37, 38), and the postgastric ceca (39) of ruminants, swine, and gallinaceous fowl, respectively, where fermentation is most active (Figure 1). Although fecal material is used as a necessary proxy for human microbiome studies, the microbiota of the rumen are distinct from the microbiota detected in a ruminant’s fecal material (40), which likely reflects the gastric barrier. Work from Davies and colleagues (41) has shown that anaerobic fungi found in the ruminant hindgut and feces were significantly fewer and enriched for members that were more resistant to desiccation compared to the rumen. The later observation was hypothesized to reflect an enrichment of fungi with a thicker walled zoosporangium, which would enable their passage through the gastric abomasum unscathed. Evidence in chickens indicates that the microbiota detected in the feces originate from cecal, colonic, ileal, crop, and gizzard microbiomes, along with distinct, possibly rectal-colonizing microbiota (42). Representation of the upper GIT can be reduced through stimulation of the gizzard to reduce its pH, which is proposed to simulate a gastric barrier (42). In ruminants, swine, and chickens, the mucosal microbiota are distinct from the luminal microbiota (39, 43, 44), and in ruminants the luminal rumen microbiota can be further subdivided into organisms physically associated with plant fiber and distinct planktonic communities (45, 46). Methanogenic communities differ between those physically associated with protozoa and those that are free-living (47), though the term free-living may be misleading owing to their endosymbiotic association with the ruminant and propensity to aggregate with fibrolytic microbes (48). Evidence indicates that each of these unique, biogeographically delineated communities may be independently affected by dietary and therapeutic interventions (43). For all mammals, including ruminants and swine, as well as galliformes, the primary fermentative organ is typically dominated by microbes of two bacterial phyla, the Firmicutes and Bacteroidetes (32, 46, 49), although occasionally Proteobacteria outnumber the Bacteroidetes (31, 46). At more

Diversity: a measure of richness and evenness Evenness: a measure of how evenly taxon abundance is distributed Richness: the total number of unique microbial taxa Allochthonous microbe: a microbe that did not originate from the biome it is identified in Autochthonous microbe: a microbe that originated from the biome it is identified in

COMING TO TERMS Lederberg & McCray (148) coined the term “microbiome” as an “ecological community of commensal, symbiotic [meant as mutualistic], and pathogenic microorganisms.” Shannahan (149) subsequently used it in the context of the collective microbial gene content. The subsequent use is based on the “-ome” suffix, which implies a molecular relationship, as with other “omic” words (e.g., genome, transcriptome, metabolome), whereas the former definition is based on the “-biome” suffix. In the macrobial world, “biome” refers to the collection of plants, animals, and microbes that occupy a specific geographical location and are sustained by its climatic conditions. These definitions are dually used throughout the literature, and it is unclear if the term will ever synchronize. It is not the purpose of this review to weigh in on the validity of either use, as each can be equally justified. For the purpose of this review, we have elected to use the term “microbiota” to reflect a collection of microbes (of any symbiotic relationship) occupying the GIT and “microbiome” to specifically refer to those that are autochthonous. We then use “metagenome” to specifically refer to the microbial genetic content, though the true sense of the word additionally includes the host’s genetics.

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Macrobiotics and Probiotics

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Crop Proventriculus

Reticulum Stomach

Gizzard


Rumen

Omasum

Abomasum

Duodenum Jejunum

Cecum

Ileum Ceca Cecum

Colon

104 106

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1010 1012

Microbial density Figure 1 Microbial density across the production animal gastrointestinal tract. Approximate densities of microbiota throughout the gastrointestinal tracts of cattle, swine, and poultry are shown.

informative taxonomic levels, Prevotella have repeatedly been shown to be the dominant genus in both ruminants and swine (49, 50). Clostridium is most commonly reported as the dominant genus of the chicken ceca (51). However, gut systems, and especially the rumen, make a strong case for segregating the ideas of numerical abundance and ecological importance because critical functions, such as cellulolysis and hydrogenotrophy, are imparted by microbes of very low abundance (52–54). These microbes illustrate the concept of keystone species, that is, species whose impact on an ecosystem far exceeds their numerical abundance. Maintenance of a healthy GIT microbiome is becoming increasingly well recognized as a critical factor in an animal’s overall health (55), development (56), and productivity (57). In ruminant livestock, the GIT microbiota are required to fulfill approximately 70% of the animal’s daily energy requirements (58). This is due to the recalcitrant nature of structural carbohydrates, such as 472

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cellulose, xylans, mannans, pectins, inulin, beta glucans, and resistant starches being indigestible by most, if not all animals (58). These structural carbohydrates account for the vast majority of plant biomass (59). Fibrolytic members of the GIT microbiome collectively possess the diverse enzymatic capabilities necessary to hydrolyze these structural fibers (46, 60), using them for their own carbohydrate requirements. Anaerobic microbial fermentation of the simpler carbohydrate products derived from these structural fibers results in the production of short-chain fatty acids (SCFAs), principally acetate, propionate, and butyrate (61). These SCFAs must then be excreted by the microbes to maintain physiological pH within the microbial cell cytoplasm. Mammals have evolved to exploit these SCFAs, rapidly absorbing and metabolizing them for energy and other physiological purposes (62). Each of these SCFAs has unique but critical roles in animal health and nutrition. The most abundant SCFA, acetate, is one of the major carbon sources for de novo fatty acid synthesis (63). Butyrate is the primary energy source for colonic and ruminal epithelia (64, 65). The production of butyrate and its availability in the host GIT is essential to the physiological development of the host’s GIT (see below) and maintenance of host health (66). Propionate is primarily used for gluconeogenesis, which accounts for the majority of a ruminant’s daily glucose requirement. Owing to the pregastric location of the rumen, rumen microbes rapidly deplete the glucose and other readily metabolizable simple sugars that are available in feed. This typically results in less than 10% of a ruminant’s daily glucose requirement being met by dietary glucose (67). Gluconeogenesis is also a major source of glucose for both ruminant and non-ruminant neonatal animals (68). The importance of glucose comes from its role as the primary energy source of the developing fetus (69) and mammary gland (70), as well as its role as one of the primary, and one of few, energy sources that can be used by the brain (71). Nutritional contributions of the GIT microbiome are not limited to carbon, energy, and fatty acid metabolisms; microbes also make important contributions to nitrogen metabolism. The GIT microbiome enables ruminants to maintain nitrogen homeostasis by converting hepatically produced urea to ammonia and microbial protein (72). This process occurs in the rumen, with the urea being recycled to the fermentative organ as an inverse function of dietary crude protein levels, illustrating an evolved mutualism of host and microbiome (72). Microbes are also directly responsible for meeting more than half of a ruminant’s protein requirements. Microbial biomass continuously flows from the rumen into the gastric, pepsin and lysozyme-enhanced abomasum, which lyses the majority of microbes that remain intact, prior to their arrival into the distal GIT. Within the distal GIT, the cellular components of the microbiota are absorbed as nutrients (73). Beyond nutritional contributions, the GIT microbiome can attenuate toxins (74) and other xenobiotics (75), increase the host’s resistance to pathogenic bacteria (76), and play critical roles in the maturation of the immune (77, 78) and endocrine systems (79). Therefore, nurture of the GIT microbiome of production animals is now firmly established as a key feature underscoring the profitability of livestock agricultural systems. With new research technologies enabling the exploration of these microbiomes at unprecedented depths, we are now exploring their ecology in a more holistic fashion. Systems-based approaches have provided (and promise to continue to provide) fresh insights into the properties that define the collective colonizing microbial communities as they relate to the host’s nutrition, development, health, and disease. The current major directions of research into the GIT microbiomes of production animals focus on improving animal health (78) and thereby reducing animal morbidity and mortality, reducing the potential for impacts of animal production on human health (80), reducing the environmental impacts of animal production (48), defining the microbial determinants of animal productivity (81, 82), and improving the health attributes and quality of meat and milk products (83, 84). Although separate entities, these research foci are intimately associated (81, 84). www.annualreviews.org


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GUT MICROBIOME DEVELOPMENT


Climax community: a microbial ecosystem that has reached a steady state (i.e., is exhibiting little temporal variation)

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Unlike some insects, mammalian fetuses remain sterile until birth. Infection of the fetus often results in abortion, stillbirth, perinatal mortality, or preterm births that often include severe and long-term developmental issues (85). Colonization of the GIT is initiated at birth and begins with rapid colonization by aerobic and facultatively anaerobic populations (86). In conventionally born humans, initial colonization occurs during transit down the vaginal tract (87). Although it remains to be determined if this is true of other animals, conventionally born and caesarean-delivered piglets show distinct early gut microbiomes (88). Aerobic and facultatively anaerobic populations are rapidly replaced by a diverse population of strictly anaerobic bacteria (86) as the GIT is continually exposed to microbes. Microbial richness increases with age for both cattle (86) and gallinaceous fowl (31) and gradually exhibits greater interindividual similarity as it tends toward a climax community (86). Work by Schmidt and colleagues (89) indicates that excessively hygienic conditions may obstruct the development of a climax community in pigs. Key functional groups appear to colonize the GIT early. Jami and colleagues (86) found a successional colonization of cellulolytic bacteria in the bovine rumen: Ruminococcus flavefaciens was detected as early as one day of age, whereas Ruminococcus albus and Fibrobacter succinogenes did not appear until three days and two months of age, respectively. Methanogenic archaea are observed as early as one day of age (90) in ruminants and three days in chickens (52). Great functional diversity is observed in the rumen by fourteen days of age, including fibrolytic and methanogenic capabilities (91). Growing evidence points toward early colonization events as being most critical to the longterm health and development of an animal. Early microbial exposure may also influence the subsequent development of the microbial community (92). Mechanisms through which early colonizing microbiota could determine subsequent community composition have been described previously (93). Microbial colonization is critical to the development of GIT morphology, maturation of the immune system, and development of the fermentative environment. For ruminants, ruminal pH gradually decreases over the first eight weeks, commensurate with increasing SCFA concentrations (94), before stabilizing at approximately ten weeks of age. This corresponds to an increased buffering capacity of the rumen (92). The relative concentrations of the various SCFAs are affected by microbiome composition (88). The microbially produced SCFA, butyrate, positively increases the length and width of GIT papillae (95) along with crypt depth (96). Microbial colonization of the gut also alters the types of mucins produced by GIT goblet cells (97) and plays a critical role in developing and modulating the immune system (77). The colonizing microbiota’s effect on systemic immune function has important implications in the host’s ability to respond to pathogenic challenge (78). Research in humans has shown that following birth, B cells, T cells, and monocytes colonize neonatal lymphoid tissues as the neonate is exposed to new antigens (98). Although the innate immune system is somewhat developed in utero, innate immune cells of the neonate are less capable of eliciting polyfunctional cytokine responses compared with those of a fully developed adult system (99, 100). Mucosal-associated lymphoid tissues of the nose, tear duct, and small intestine (cryptopatches) are formed after birth and are activated by microbial stimulation (101). Further, the maturation and intestinal migration of certain immunological cells are critically dependent on the colonization of specific gut microbes (102, 103). Beyond their role in developing the immune system, commensal gut microbes also play a critical role in limiting the colonizing capabilities of numerous pathogenic bacteria and thereby provide a pseudo immunity that bridges the period of immunological maturation (77, 104). Early colonization events may therefore be the most important to the long-term health and productivity of domestic livestock. Perturbation of these early gut systems, such as through early, or even prenatal, antibiotic exposure, can have long-lasting and serious sequelae and affect the long-term health and performance of the animal (105).

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NUTRITION, GENETICS, AND THE GASTROINTESTINAL TRACT MICROBIOME The composition of the GIT microbiome is primarily shaped by non-neutral niche processes (106) and affected by the animal’s diet (107, 108), age (49, 109, 110), immune function (111), and genetics (112), as well as complex interactions among microbial species (47, 93). These complex features collectively lead to interspecies (113) and interindividual (86) microbiome characteristics. A recent study by Benson and colleagues (112) revealed thirteen individual quantitative trait loci in mice that affected predominantly refined taxonomic bacterial designations, but also broader and disparate taxonomic groups. This study elaborately demonstrated that genetic influences promote microbial community composition. The best elucidated genetic influences appear to involve immunologically active genes, but physiological mechanisms underscoring genetic determinants could involve anything from modifications in GIT anatomy or motility (93) to changes in host mucins. The influence of genetics on the GIT microbiome can be overshadowed by nutrition, for which effects are particularly well described. Of the various nutrients, resistant starches appear to impart one of the most significant modulatory effects on the GIT microbiome of both pre- and postgastric fermenters (108). Starches containing high amylose contents promote microbes and microbial metabolites commonly associated with improved animal health in a range of animal systems (114–116). Both resistant starches and nonstarch polysaccharides increase overall GIT fermentation (117). Simple carbohydrate sources also increase GIT fermentation but, detrimentally, promote an imbalance of GIT microbiota through successional changes in the fermentative environment. In ruminants, a rapid transition to easily fermentable carbohydrate sources leads to the hyperproduction of SCFAs, which overwhelm the buffering capacity of the ruminant’s unique bicarbonate-infused saliva. The salivary infusion of bicarbonate is necessary to enable the rumen microbiome to produce SCFAs at levels sufficient to meet the energy requirements of the animal (58). However, as the SCFAs overwhelm this capacity, ruminal pH decreases below its typical level (∼6.7). This increasing acidity detrimentally reduces the fermentative capabilities of fibrolytic microbes while favoring more acid-tolerant microbes, including Streptococcus bovis and lactobacilli, whose own metabolisms favor increased lactate-driven acidity (118). Physiologically, this leads to subacute ruminal acidosis (pH 5.5–5.8) and may eventually result in acute acidosis (pH < 5), which is associated with severe morbidities and can have mortal consequences (118). Therefore, nutrition and the microbiome must be dually considered in the context of animal health and production. Efforts are being made to breed livestock that are more disease resistant (119), but the overshadowing effects of nutrition on microbiome composition, along with the ability of a healthy GIT microbiome to mitigate or preclude many diseases, may indicate efforts should also be directed toward research that intersects nutrition with microbial function. Such a nutrimetagenomic approach could be critical as the world moves away from antibiotic uses in production animals and toward more sustainable agricultural systems.

DETERMINANTS OF A HEALTHY GASTROINTESTINAL TRACT MICROBIOME The deployment of a nutrimetagenomic approach requires baseline knowledge as to what constitutes a healthy microbiome. But the variation observed between individual animals makes it difficult to define a healthy GIT microbiota and therefore difficult to delineate natural plasticity of the microbiome from its perturbation. Whereas numerous pathogenic species are well defined and can be identified within samples of the GIT, many are also common residents of the GIT microbiota, and their pathogenic traits are either (a) exhibited only when the GIT microbiota breaks www.annualreviews.org


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down (118, 120) or (b) exhibited by a subset of the strains comprising a pathogenic species (121). We therefore need methods that are less reliant on basic compositional traits to determine the health of the GIT microbial ecosystem. In evaluating the literature, three common features that characterize GIT health are evident. Perhaps the best-described feature of perturbation is reduced species diversity. Reductions in species diversity have been observed in disparate scenarios, such as during subacute ruminal acidosis (122) following gut resection in pigs and associated with inflammation of the colon (123), following antibiotic interventions (124), and in wild mammals exposed to suboptimal habitats (125). These observations correspond with macroecological observations and theory that relate species diversity to ecosystem health. Increased species diversity correlates with increasing functional diversity (126). Eventually, functional diversity will saturate to give functional redundancy (Figure 2). A healthy ecosystem is one that can augment all functions required of it. Better yet, a resilient ecosystem is one that carries these functions redundantly, such that losses of individual species (and their functions) should not impact the overall functionality of the system (127). Consistently, microbial diversity has been shown to enhance resilience in soil microbiomes (128). A functionally redundant system may also be one that is less accessible for nonnative pathogens. Charles Sutherland Elton first developed this concept among macrobial communities. The observed recalcitrance to foreign invaders may be driven by competitive exclusion, such that a diverse community ensures an oligotrophic environment (129). A diverse community is additionally likely to possess direct amensalistic capabilities that kill off pathogenic invaders (93). Direct evidence supporting a role for microbial diversity in preventing pathogenic invasion is sparse but does exist (130), along with strong implicative evidence (125). A second correlate of an unhealthy microbiome is an increase in interindividual community composition. Whereas healthy groups of animals tend to exhibit more similar, albeit distinct, GIT microbial communities, unhealthy animals exhibit much less similarity among individuals (Figure 3) (125). One hypothesis for this observation is increased stochasticity, where the microbiome is less resistant to, and thereby more frequently colonized by, allochthonous microbes through chance environmental encounters.

Functional diversity

Resilience

Resistance

Species diversity Figure 2 Relationship of microbial species diversity to gastrointestinal tract resistance and resilience. Microbial species diversity exhibits a strong correlation with functional diversity. Functional diversity appears to correlate with resistance to invasiveness and upon saturation is hypothesized to increase resilience.

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Similarity

Microbiome composition

Healthy (more similar)

Unhealthy (less similar)

Figure 3 Greater dissimilarity among gastrointestinal tract microbiomes is a sign of dysbiosis. Gastrointestinal tract microbiomes are distinct but become significantly less similar during dysbiosis.

Indicators of butyrate production are a third strong correlate with microbiome health. The increased presence or prevalence of butyrate-producing taxa (131), butyrate-producing genes (125), or butyrate itself (132) has been linked to GIT health. The importance of butyrate to host GIT epithelia and host physiology is well described (95, 96, 117, 132), and its contribution to maintaining a healthy GIT microbiome may relate to ensuring homeostatic host-microbiome interactions, such as through maintenance of the epithelial interface.

PROBIOTICS The critical importance of a healthy GIT microbiota to animal health has led researchers to explore the use of inoculating livestock with health-promoting microbes. These live microbial probiotics are provided as dietary supplements, and their use has been linked in numerous studies to improved animal health, increased disease resistance (133), greater reproductive performance (134), enhanced growth promotion (135), and a better product quality (133, 136). For neonatal animals, probiotics administered directly or maternally have been linked to reduced perinatal mortality (137) and improvements to immune function (138) and GIT morphology (139). But other studies have reported contrasting results (140, 141), and debate persists as to the true efficacy of probiotics. In November 2012, the term probiotic was banned from food labels in the European Union because the European Food Safety Authority determined there remains a lack of evidence to prove their efficacy. This decision appears to focus on a few contentious findings and ignore a more substantial amount of positive peer-reviewed research. Nevertheless, variable findings in probiotic research exist. One source of these variable outcomes in probiotic trials likely reflects the nutritional environment the probiotic is inoculated into. As described above, nutrition plays a strong modulatory role in the GIT microbiome. It is for this reason that probiotics have been and should continue to be developed alongside appropriate nutritional interventions (prebiotics) that not only promote an optimal GIT microbiome but support the probiotic (synbiotics). www.annualreviews.org


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A further source of variation likely reflects the choice of probiotic organism. Lactobacilli are the preeminent probiotic microbes and are most frequently selected as probiotic inocula. Lactobacilli were initially chosen based on an observational link between Bulgarian peasants, yogurt consumption, and longevity (142). By good fortune, lactobacilli have subsequently been linked to numerous health-promoting traits (76, 133) and, by virtue of their production of lactic acid, bacteriocins, and hydrogen peroxide, to the inhibition of multiple pathogens (143). Lactobacilli also appear to colonize GIT epithelia, promoting tight junctions and thereby reducing intestinal permeability (144) along with physically precluding attachment by potentially pathogenic microbes (144, 145). However, lactobacilli strains have also been shown to exhibit host-species specificity in their ability to colonize all but severely perturbed microbiomes (146). Probiotic strains should, therefore, be selected on their ability to colonize the GIT of the animal in question. They should also be selected in light of the host’s own physiology. Although lactobacilli may be beneficial to postgastric microbial ecosystems, their proliferation in the rumen is a key feature of ruminal acidosis (122). While the initiation of acidosis depends on providing the appropriate GIT environment to favor lactobacilli proliferation, Lettat et al. (147) demonstrated that supplementation of lactobacilli under nutritional conditions conducive to acidosis further increases ruminal lactate concentrations and thereby drives ruminal pH down. Under these circumstances, lactobacilli would exacerbate acidosis-related morbidities and could thereby expedite mortality. The development of probiotics need not be limited to lactobacilli (or other common human probiotic taxa). For maximum efficacy, probiotic development should be based on mechanistically established, health-promoting host-microbe interactions. Further, these health-promoting interactions need not be narrowly focused on the preclusion of pathogens. It is noteworthy that not all probiotic trials in animals have focused on lactobacilli; a few have even used polymicrobial concoctions. However, only a handful of probiotics have been selected for reasons other than pathogen inhibition. Although pathogenic resistance is important, in light of the numerous and significant contributions microbes make to the mutualism they share with their host (nutritionally, immunologically, and morphologically), as well as technological advances that enable us to holistically examine microbe-microbe and microbe-host interactions, it seems surprising that we are not more savvy in our design of probiotic concoctions. To their credit, rumen researchers have developed probiotics using organisms that reduce lactate concentrations (119). But with a wealth of nutritional information and an elaborated understanding of microbial contributions to host health, it seems there is much room for further probiotic developments that exploit the numerous other important contributions microbes make to host health. To achieve this with true efficacy, it may be necessary to explore polymicrobial host-specific concoctions.

SUMMARY AND NEW DIRECTIONS Technological advances enabling microbial community-wide profiling of phylogenetic composition (16S rRNA gene profiling), functional capability (metagenomics), functional intent (metatranscriptomics), and the resulting metabolic impact (metabolomics) have provided researchers unprecedented access to the GIT microbiome. Through these investigations, we continue to uncover the increasingly humbling mutualistic relationship animals share with their GIT microbiome. The GIT microbiome is not only indispensable to animal nutrition but also critical to animal health and development. In recognition of the microbiome’s immense importance, probiotic, prebiotic, and other nutritional interventions have been and continue to be developed with the express goal of improving animal health and productivity. Although individual animals may show somewhat distinct GIT microbiomes driven by multiple factors, including host genetics, diet, immune function, and exposure (93), key features of healthy GIT 478

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microbiomes are beginning to emerge. These include microbial diversity, which appears to be a reflection of functional diversity. However, which of the many functions GIT microbiomes provide to their hosts are critical remains to be elucidated. Current technologies enable us to more precisely, and globally, interrogate the functional contributions of the GIT microbiome. A comprehensive understanding of functional diversity is needed to truly understand the critical features of the GIT microbiome that underscore animal health and productivity. Defining key microbial consortia, developing polymicrobial polyfunctional probiotics, and integrating the modulatory effects of nutrition with present-day technological advancements that enable us to explore the GIT microbial ecosystem’s functional capacity lend themselves to an emerging field of nutrimetagenomics. An integrated probiotic and nutrimetagenomic endeavor would enable the field to determine the key modulatory nutrients and microbiota necessary for the development of designer microbiomes that not only support animal health but also meet the productivity goals (including improved feed efficiency, greater average daily gain, shorter time to market, and improved product yields) necessary to meet the growing demands on world agriculture, while minimizing livestock’s environmental impact.

DISCLOSURE STATEMENT The authors are not aware of any affiliations, memberships, funding, or financial holdings that might be perceived as affecting the objectivity of this review.

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Annual Review of Animal Biosciences Volume 2, 2014

Contents


From Germ Cell Preservation to Regenerative Medicine: An Exciting Research Career in Biotechnology Ian Wilmut . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 Genomic Imprinting in Farm Animals Xiuchun (Cindy) Tian . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 23 Recent Advances in Primate Phylogenomics Jill Pecon-Slattery . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 41 Domestication Genomics: Evidence from Animals Guo-Dong Wang, Hai-Bing Xie, Min-Sheng Peng, David Irwin, and Ya-Ping Zhang . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 65 Behavior Genetics and the Domestication of Animals Per Jensen . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 85 Applied Animal Genomics: Results from the Field Alison L. Van Eenennaam, Kent A. Weigel, Amy E. Young, Matthew A. Cleveland, and Jack C.M. Dekkers . . . . . . . . . . . . . . . . . . . . 105 Pestiviruses Matthias Schweizer and Ernst Peterhans . . . . . . . . . . . . . . . . . . . . . . . . . 141 Pathogenesis and Molecular Biology of a Transmissible Tumor in the Tasmanian Devil Hannah S. Bender, Jennifer A. Marshall Graves, and Janine E. Deakin . . . 165 Animal Models of Bovine Leukemia Virus and Human T-Lymphotrophic Virus Type-1: Insights in Transmission and Pathogenesis Michael D. Lairmore . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 189 Malignant Catarrhal Fever: Inching Toward Understanding Hong Li, Cristina W. Cunha, Naomi S. Taus, and Donald P. Knowles . . . 209

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Comparative Immune Systems in Animals Shaochun Yuan, Xin Tao, Shengfeng Huang, Shangwu Chen, and Anlong Xu . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 235 Origin and Evolution of Adaptive Immunity Thomas Boehm and Jeremy B. Swann . . . . . . . . . . . . . . . . . . . . . . . . . . . 259


The Functional Significance of Cattle Major Histocompatibility Complex Class I Genetic Diversity Shirley A. Ellis and John A. Hammond . . . . . . . . . . . . . . . . . . . . . . . . . . 285 Incidence of Abnormal Offspring from Cloning and Other Assisted Reproductive Technologies Jonathan R. Hill . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 307 Preadipocyte and Adipose Tissue Differentiation in Meat Animals: Influence of Species and Anatomical Location G.J. Hausman, U. Basu, S. Wei, D.B. Hausman, and M.V. Dodson . . . . . 323 Serotonin: A Local Regulator in the Mammary Gland Epithelium Nelson D. Horseman and Robert J. Collier . . . . . . . . . . . . . . . . . . . . . . . 353 Evolution of the Modern Broiler and Feed Efficiency Paul B. Siegel . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 375 Amino Acid Nutrition in Animals: Protein Synthesis and Beyond Guoyao Wu, Fuller W. Bazer, Zhaolai Dai, Defa Li, Junjun Wang, and Zhenlong Wu . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 387 The Suckling Piglet as an Agrimedical Model for the Study of Pediatric Nutrition and Metabolism Jack Odle, Xi Lin, Sheila K. Jacobi, Sung Woo Kim, and Chad H. Stahl . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 419 Cattle Production Systems: Ecology of Existing and Emerging Escherichia coli Types Related to Foodborne Illness David R. Smith . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 445 Gastrointestinal Tract Microbiota and Probiotics in Production Animals Carl J. Yeoman and Bryan A. White . . . . . . . . . . . . . . . . . . . . . . . . . . . . 469 Biodiversity of Cone Snails and Other Venomous Marine Gastropods: Evolutionary Success Through Neuropharmacology Baldomero M. Olivera, Patrice Showers Corneli, Maren Watkins, and Alexander Fedosov . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 487 Ecological Risk Analysis and Genetically Modified Salmon: Management in the Face of Uncertainty Darek T.R. Moreau . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 515 Contents

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The Modern Feedlot for Finishing Cattle John J. Wagner, Shawn L. Archibeque, and Dillon M. Feuz . . . . . . . . . . . 535 The Nexus of Environmental Quality and Livestock Welfare Sara E. Place and Frank M. Mitloehner . . . . . . . . . . . . . . . . . . . . . . . . . . 555 Errata


An online log of corrections to Annual Review of Animal Biosciences articles may be found at http://www.annualreviews.org/errata/animal

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Contents

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New From Annual Reviews:

Annual Review of Statistics and Its Application Volume 1 • Online January 2014 • http://statistics.annualreviews.org


Editor: Stephen E. Fienberg, Carnegie Mellon University

Associate Editors: Nancy Reid, University of Toronto Stephen M. Stigler, University of Chicago The Annual Review of Statistics and Its Application aims to inform statisticians and quantitative methodologists, as well as all scientists and users of statistics about major methodological advances and the computational tools that allow for their implementation. It will include developments in the field of statistics, including theoretical statistical underpinnings of new methodology, as well as developments in specific application domains such as biostatistics and bioinformatics, economics, machine learning, psychology, sociology, and aspects of the physical sciences.

Complimentary online access to the first volume will be available until January 2015. table of contents:

• What Is Statistics? Stephen E. Fienberg • A Systematic Statistical Approach to Evaluating Evidence from Observational Studies, David Madigan, Paul E. Stang, Jesse A. Berlin, Martijn Schuemie, J. Marc Overhage, Marc A. Suchard, Bill Dumouchel, Abraham G. Hartzema, Patrick B. Ryan

• High-Dimensional Statistics with a View Toward Applications in Biology, Peter Bühlmann, Markus Kalisch, Lukas Meier • Next-Generation Statistical Genetics: Modeling, Penalization, and Optimization in High-Dimensional Data, Kenneth Lange, Jeanette C. Papp, Janet S. Sinsheimer, Eric M. Sobel

• The Role of Statistics in the Discovery of a Higgs Boson, David A. van Dyk

• Breaking Bad: Two Decades of Life-Course Data Analysis in Criminology, Developmental Psychology, and Beyond, Elena A. Erosheva, Ross L. Matsueda, Donatello Telesca

• Brain Imaging Analysis, F. DuBois Bowman

• Event History Analysis, Niels Keiding

• Statistics and Climate, Peter Guttorp

• Statistical Evaluation of Forensic DNA Profile Evidence, Christopher D. Steele, David J. Balding

• Climate Simulators and Climate Projections, Jonathan Rougier, Michael Goldstein • Probabilistic Forecasting, Tilmann Gneiting, Matthias Katzfuss • Bayesian Computational Tools, Christian P. Robert • Bayesian Computation Via Markov Chain Monte Carlo, Radu V. Craiu, Jeffrey S. Rosenthal • Build, Compute, Critique, Repeat: Data Analysis with Latent Variable Models, David M. Blei • Structured Regularizers for High-Dimensional Problems: Statistical and Computational Issues, Martin J. Wainwright

• Using League Table Rankings in Public Policy Formation: Statistical Issues, Harvey Goldstein • Statistical Ecology, Ruth King • Estimating the Number of Species in Microbial Diversity Studies, John Bunge, Amy Willis, Fiona Walsh • Dynamic Treatment Regimes, Bibhas Chakraborty, Susan A. Murphy • Statistics and Related Topics in Single-Molecule Biophysics, Hong Qian, S.C. Kou • Statistics and Quantitative Risk Management for Banking and Insurance, Paul Embrechts, Marius Hofert

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Probiotics and microbiota composition.

Bifidobacteria from the gastrointestinal tract of animals: differences and similarities.

News in livestock research - use of Omics-technologies to study the microbiota in the gastrointestinal tract of farm animals.

Highly variable microbiota development in the chicken gastrointestinal tract.

Dietary Probiotics Affect Gastrointestinal Microbiota, Histological Structure and Shell Mineralization in Turtles.

Metabolic Interactions in the Gastrointestinal Tract (GIT): Host, Commensal, Probiotics, and Bacteriophage Influences.

Interactions between Innate Immunity, Microbiota, and Probiotics.

Development of putative probiotics as feed additives: validation in a porcine-specific gastrointestinal tract model.

Gut microbiota, probiotics, and human health.

Effect of probiotics on enrofloxacin disposition in gastrointestinal tract of poultry.

Characterization and comparison of the bacterial microbiota in different gastrointestinal tract compartments in horses.

Gut microbiota modulation: probiotics, antibiotics or fecal microbiota transplantation?

Effects of PGA and PGB compounds on gastrointestinal tract smooth muscle from man and laboratory animals.

Recent advances and future perspective in microbiota and probiotics.

Microbiota and probiotics in canine and feline welfare.

Microbiota and Probiotics in Health and HIV Infection.

Review on microbiota and effectiveness of probiotics use in older.

Oral Probiotics Alter Healthy Feline Respiratory Microbiota.

Intestinal microbiota, probiotics and prebiotics in inflammatory bowel disease.

The Dynamic Interactions between Salmonella and the Microbiota, within the Challenging Niche of the Gastrointestinal Tract.

The dynamic distribution of porcine microbiota across different ages and gastrointestinal tract segments.

Anti-infective activities of lactobacillus strains in the human intestinal microbiota: from probiotics to gastrointestinal anti-infectious biotherapeutic agents.

Characterization of the most abundant Lactobacillus species in chicken gastrointestinal tract and potential use as probiotics for genetic engineering.

Probiotics normalize the gut-brain-microbiota axis in immunodeficient mice.