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The Evolution of Stomach Acidity and Its Relevance to the Human Microbiome.

Beasley DE, Koltz AM, Lambert JE, Fierer N, Dunn RR - PLoS ONE (2015)

Bottom Line: Conversely, species feeding on a lower trophic level or on food that is distantly related to them (e.g. herbivores) should require the least restrictive filter, as the risk of pathogen exposure is lower.Comparisons of stomach acidity across trophic groups in mammal and bird taxa show that scavengers and carnivores have significantly higher stomach acidities compared to herbivores or carnivores feeding on phylogenetically distant prey such as insects or fish.Together these results highlight the importance of including measurements of gastric pH when investigating gut microbial dynamics within and across species.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, North Carolina State University, Raleigh, North Carolina, United States of America.

ABSTRACT
Gastric acidity is likely a key factor shaping the diversity and composition of microbial communities found in the vertebrate gut. We conducted a systematic review to test the hypothesis that a key role of the vertebrate stomach is to maintain the gut microbial community by filtering out novel microbial taxa before they pass into the intestines. We propose that species feeding either on carrion or on organisms that are close phylogenetic relatives should require the most restrictive filter (measured as high stomach acidity) as protection from foreign microbes. Conversely, species feeding on a lower trophic level or on food that is distantly related to them (e.g. herbivores) should require the least restrictive filter, as the risk of pathogen exposure is lower. Comparisons of stomach acidity across trophic groups in mammal and bird taxa show that scavengers and carnivores have significantly higher stomach acidities compared to herbivores or carnivores feeding on phylogenetically distant prey such as insects or fish. In addition, we find when stomach acidity varies within species either naturally (with age) or in treatments such as bariatric surgery, the effects on gut bacterial pathogens and communities are in line with our hypothesis that the stomach acts as an ecological filter. Together these results highlight the importance of including measurements of gastric pH when investigating gut microbial dynamics within and across species.

No MeSH data available.


Related in: MedlinePlus

Comparison of stomach pH (mean ± S.E.) across trophic groups with gastrointestinal tracts of representative birds and mammals.Different letters above error bars represent statistically significant differences (P < 0.05) using ANOVA and Tukey-Kramer post-hoc test. Obligate scavengers (1.3 ± 0.08), facultative scavengers (1.8 ± 0.27), generalist carnivore (2.2 ± 0.44), omnivore (2.9 ± 0.33), specialist carnivore (3.6 ± 0.51), hindgut herbivore (4.1 ± 0.38) and foregut herbivore (6.1 ± 0.31).
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pone.0134116.g001: Comparison of stomach pH (mean ± S.E.) across trophic groups with gastrointestinal tracts of representative birds and mammals.Different letters above error bars represent statistically significant differences (P < 0.05) using ANOVA and Tukey-Kramer post-hoc test. Obligate scavengers (1.3 ± 0.08), facultative scavengers (1.8 ± 0.27), generalist carnivore (2.2 ± 0.44), omnivore (2.9 ± 0.33), specialist carnivore (3.6 ± 0.51), hindgut herbivore (4.1 ± 0.38) and foregut herbivore (6.1 ± 0.31).

Mentions: Here we focus on two taxonomic groups, mammals and birds, in which the ecology of stomachs has been best studied. Within these taxa, we focus on the first chamber of the gastrointestinal tract, a chamber with different names depending on the organisms and context. In mammals, gastric acid production and temporary food storage both occur in the stomach. In birds, acid production occurs in the proventriculus and food storage occurs in the gizzard (Fig 1). We focus on the stomachs of mammals and, technically, the proventriculus of birds, but hereafter use the term “stomach” for simplicity. Stomachs vary greatly in their structural complexity and size among vertebrates [27], particularly mammals, yet in most of these cases, stomachs are the most acidic component of the digestive tract [28]. The exception to this pattern are forestomach-fermenting species in which microbial fermentation precedes digestion and absorption [22]. Mammalian herbivore clades can be characterized on the basis of where in the gastrointestinal tract most alloenzymatic (microbial) fermentation of dietary carbohydrate occurs. In foregut fermenters, microbes reside in one to several sections of a sacculated stomach. Among primates, only one lineage (subfamily Colobinae) has evolved this system, but analogous digestive strategies are found in several lineages of Artiodactyla as well as sloths, and kangaroos [18–22]. Among birds, only one species is known to rely on such a fermentation system (hoatzin, Opisthocomus hoazin) although microbes are housed in a specialized two-chambered crop, and not, technically, in the stomach [29]. Regardless of morphology, because communities of cellulolytic microorganisms and healthy fermentation occur most productively in an alkaline environment, the proximal portion of the foregut-fermenting stomach has a pH of approximately 5.5 to 7, while the distal portions have a pH of about 3. The need to maintain a particular pH in the forestomach no doubt influences feeding decisions: when the production of volatile fatty acids from fermentation exceeds absorption, the overabundance of acids can cause a drop in forestomach pH, resulting in a sometimes fatal affliction known as acidosis.


The Evolution of Stomach Acidity and Its Relevance to the Human Microbiome.

Beasley DE, Koltz AM, Lambert JE, Fierer N, Dunn RR - PLoS ONE (2015)

Comparison of stomach pH (mean ± S.E.) across trophic groups with gastrointestinal tracts of representative birds and mammals.Different letters above error bars represent statistically significant differences (P < 0.05) using ANOVA and Tukey-Kramer post-hoc test. Obligate scavengers (1.3 ± 0.08), facultative scavengers (1.8 ± 0.27), generalist carnivore (2.2 ± 0.44), omnivore (2.9 ± 0.33), specialist carnivore (3.6 ± 0.51), hindgut herbivore (4.1 ± 0.38) and foregut herbivore (6.1 ± 0.31).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4519257&req=5

pone.0134116.g001: Comparison of stomach pH (mean ± S.E.) across trophic groups with gastrointestinal tracts of representative birds and mammals.Different letters above error bars represent statistically significant differences (P < 0.05) using ANOVA and Tukey-Kramer post-hoc test. Obligate scavengers (1.3 ± 0.08), facultative scavengers (1.8 ± 0.27), generalist carnivore (2.2 ± 0.44), omnivore (2.9 ± 0.33), specialist carnivore (3.6 ± 0.51), hindgut herbivore (4.1 ± 0.38) and foregut herbivore (6.1 ± 0.31).
Mentions: Here we focus on two taxonomic groups, mammals and birds, in which the ecology of stomachs has been best studied. Within these taxa, we focus on the first chamber of the gastrointestinal tract, a chamber with different names depending on the organisms and context. In mammals, gastric acid production and temporary food storage both occur in the stomach. In birds, acid production occurs in the proventriculus and food storage occurs in the gizzard (Fig 1). We focus on the stomachs of mammals and, technically, the proventriculus of birds, but hereafter use the term “stomach” for simplicity. Stomachs vary greatly in their structural complexity and size among vertebrates [27], particularly mammals, yet in most of these cases, stomachs are the most acidic component of the digestive tract [28]. The exception to this pattern are forestomach-fermenting species in which microbial fermentation precedes digestion and absorption [22]. Mammalian herbivore clades can be characterized on the basis of where in the gastrointestinal tract most alloenzymatic (microbial) fermentation of dietary carbohydrate occurs. In foregut fermenters, microbes reside in one to several sections of a sacculated stomach. Among primates, only one lineage (subfamily Colobinae) has evolved this system, but analogous digestive strategies are found in several lineages of Artiodactyla as well as sloths, and kangaroos [18–22]. Among birds, only one species is known to rely on such a fermentation system (hoatzin, Opisthocomus hoazin) although microbes are housed in a specialized two-chambered crop, and not, technically, in the stomach [29]. Regardless of morphology, because communities of cellulolytic microorganisms and healthy fermentation occur most productively in an alkaline environment, the proximal portion of the foregut-fermenting stomach has a pH of approximately 5.5 to 7, while the distal portions have a pH of about 3. The need to maintain a particular pH in the forestomach no doubt influences feeding decisions: when the production of volatile fatty acids from fermentation exceeds absorption, the overabundance of acids can cause a drop in forestomach pH, resulting in a sometimes fatal affliction known as acidosis.

Bottom Line: Conversely, species feeding on a lower trophic level or on food that is distantly related to them (e.g. herbivores) should require the least restrictive filter, as the risk of pathogen exposure is lower.Comparisons of stomach acidity across trophic groups in mammal and bird taxa show that scavengers and carnivores have significantly higher stomach acidities compared to herbivores or carnivores feeding on phylogenetically distant prey such as insects or fish.Together these results highlight the importance of including measurements of gastric pH when investigating gut microbial dynamics within and across species.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, North Carolina State University, Raleigh, North Carolina, United States of America.

ABSTRACT
Gastric acidity is likely a key factor shaping the diversity and composition of microbial communities found in the vertebrate gut. We conducted a systematic review to test the hypothesis that a key role of the vertebrate stomach is to maintain the gut microbial community by filtering out novel microbial taxa before they pass into the intestines. We propose that species feeding either on carrion or on organisms that are close phylogenetic relatives should require the most restrictive filter (measured as high stomach acidity) as protection from foreign microbes. Conversely, species feeding on a lower trophic level or on food that is distantly related to them (e.g. herbivores) should require the least restrictive filter, as the risk of pathogen exposure is lower. Comparisons of stomach acidity across trophic groups in mammal and bird taxa show that scavengers and carnivores have significantly higher stomach acidities compared to herbivores or carnivores feeding on phylogenetically distant prey such as insects or fish. In addition, we find when stomach acidity varies within species either naturally (with age) or in treatments such as bariatric surgery, the effects on gut bacterial pathogens and communities are in line with our hypothesis that the stomach acts as an ecological filter. Together these results highlight the importance of including measurements of gastric pH when investigating gut microbial dynamics within and across species.

No MeSH data available.


Related in: MedlinePlus