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Research Article | Ecological and Evolutionary Science

pH-Mediated Microbial and Metabolic Interactions in Fecal Enrichment Cultures

Zehra Esra Ilhan, Andrew K. Marcus, Dae-Wook Kang, Bruce E. Rittmann, Rosa Krajmalnik-Brown
Garret Suen, Editor
Zehra Esra Ilhan
aBiodesign Swette Center for Environmental Biotechnology, Arizona State University, Tempe, Arizona, USA
bSchool of Life Sciences, Arizona State University, Tempe, Arizona, USA
cBiodesign Center for Fundamental and Applied Microbiomics, Arizona State University, Tempe, Arizona, USA
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Andrew K. Marcus
aBiodesign Swette Center for Environmental Biotechnology, Arizona State University, Tempe, Arizona, USA
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Dae-Wook Kang
aBiodesign Swette Center for Environmental Biotechnology, Arizona State University, Tempe, Arizona, USA
cBiodesign Center for Fundamental and Applied Microbiomics, Arizona State University, Tempe, Arizona, USA
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Bruce E. Rittmann
aBiodesign Swette Center for Environmental Biotechnology, Arizona State University, Tempe, Arizona, USA
dSchool of Sustainable Engineering and the Built Environment, Tempe, Arizona, USA
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Rosa Krajmalnik-Brown
aBiodesign Swette Center for Environmental Biotechnology, Arizona State University, Tempe, Arizona, USA
cBiodesign Center for Fundamental and Applied Microbiomics, Arizona State University, Tempe, Arizona, USA
dSchool of Sustainable Engineering and the Built Environment, Tempe, Arizona, USA
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Garret Suen
University of Wisconsin—Madison
Roles: Editor
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DOI: 10.1128/mSphere.00047-17
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ABSTRACT

pH and fermentable substrates impose selective pressures on gut microbial communities and their metabolisms. We evaluated the relative contributions of pH, alkalinity, and substrate on microbial community structure, metabolism, and functional interactions using triplicate batch cultures started from fecal slurry and incubated with an initial pH of 6.0, 6.5, or 6.9 and 10 mM glucose, fructose, or cellobiose as the carbon substrate. We analyzed 16S rRNA gene sequences and fermentation products. Microbial diversity was driven by both pH and substrate type. Due to insufficient alkalinity, a drop in pH from 6.0 to ~4.5 clustered pH 6.0 cultures together and distant from pH 6.5 and 6.9 cultures, which experienced only small pH drops. Cellobiose yielded more acidity than alkalinity due to the amount of fermentable carbon, which moved cellobiose pH 6.5 cultures away from other pH 6.5 cultures. The impact of pH on microbial community structure was reflected by fermentative metabolism. Lactate accumulation occurred in pH 6.0 cultures, whereas propionate and acetate accumulations were observed in pH 6.5 and 6.9 cultures and independently from the type of substrate provided. Finally, pH had an impact on the interactions between lactate-producing and -consuming communities. Lactate-producing Streptococcus dominated pH 6.0 cultures, and acetate- and propionate-producing Veillonella, Bacteroides, and Escherichia dominated the cultures started at pH 6.5 and 6.9. Acid inhibition on lactate-consuming species led to lactate accumulation. Our results provide insights into pH-derived changes in fermenting microbiota and metabolisms in the human gut.

IMPORTANCE The human gut is a dynamic environment in which microorganisms consistently interact with the host via their metabolic products. Some of the most important microbial metabolic products are fermentation products such as short-chain fatty acids. Production of these fermentation products and the prevalence of fermenting microbiota depend on pH, alkalinity, and available dietary sugars, but details about their metabolic interactions are unknown. Here, we show that, for in vitro conditions, pH was the strongest driver of microbial community structure and function and microbial and metabolic interactions among pH-sensitive fermentative species. The balance between bicarbonate alkalinity and formation of fatty acids by fermentation determined the pH, which controlled microbial community structure. Our results underscore the influence of pH balance on microbial function in diverse microbial ecosystems such as the human gut.

  • Copyright © 2017 Ilhan et al.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license .

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pH-Mediated Microbial and Metabolic Interactions in Fecal Enrichment Cultures
Zehra Esra Ilhan, Andrew K. Marcus, Dae-Wook Kang, Bruce E. Rittmann, Rosa Krajmalnik-Brown
mSphere May 2017, 2 (3) e00047-17; DOI: 10.1128/mSphere.00047-17

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pH-Mediated Microbial and Metabolic Interactions in Fecal Enrichment Cultures
Zehra Esra Ilhan, Andrew K. Marcus, Dae-Wook Kang, Bruce E. Rittmann, Rosa Krajmalnik-Brown
mSphere May 2017, 2 (3) e00047-17; DOI: 10.1128/mSphere.00047-17
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KEYWORDS

alkalinity
bacterial diversity
lactate utilizers
microbial communities
microbial fermentation
propionate producers
substrate type

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