Using Structural Equation Modeling to Understand Interactions Between Bacterial and Archaeal Populations and Volatile Fatty Acid Proportions in the Rumen.

Veronica Kaplan-Shabtai,Dipti Wilhelmina Pitta,Camila Flavia De Assis Lage,Addison Spitzer,Nagaraju Indugu,Joseph Samuel Bender,Alexander Nikolov Hristov,Molly Elizabeth Fetter,Susanna Elisabeth Räisänen,Darko Stefanovski,Bonnie Vecchiarelli,Andrea Fernandez,Krum Nedelkov,Audino Melgar,Meagan Leslie Hennessy

doi:10.3389/fmicb.2021.611951

Veronica Kaplan-Shabtai, Dipti Wilhelmina Pitta + Show 13 more

Open Access

https://doi.org/10.3389/fmicb.2021.611951

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Abstract

Microbial syntrophy (obligate metabolic mutualism) is the hallmark of energy-constrained anaerobic microbial ecosystems. For example, methanogenic archaea and fermenting bacteria coexist by interspecies hydrogen transfer in the complex microbial ecosystem in the foregut of ruminants; however, these synergistic interactions between different microbes in the rumen are seldom investigated. We hypothesized that certain bacteria and archaea interact and form specific microbial cohorts in the rumen. To this end, we examined the total (DNA-based) and potentially metabolically active (cDNA-based) bacterial and archaeal communities in rumen samples of dairy cows collected at different times in a 24 h period. Notably, we found the presence of distinct bacterial and archaeal networks showing potential metabolic interactions that were correlated with molar proportions of specific volatile fatty acids (VFAs). We employed hypothesis-driven structural equation modeling to test the significance of and to quantify the extent of these relationships between bacteria-archaea-VFAs in the rumen. Furthermore, we demonstrated that these distinct microbial networks were host-specific and differed between cows indicating a natural variation in specific microbial networks in the rumen of dairy cows. This study provides new insights on potential microbial metabolic interactions in anoxic environments that have broader applications in methane mitigation, energy conservation, and agricultural production.

Highlights

Anaerobic microbial ecosystems are ubiquitous on the planet, contributing significantly to the recycling of nutrients such as carbon, nitrogen, and sulfur (Whitman et al, 1998; Mori and Kamagata, 2014), and play important roles in deconstruction of organic biomass, the global carbon cycle, agricultural production, and the health of animals and humans
Because sampling time, sampling methods, and nucleic acid extraction (DNA-based vs. RNAbased analysis) can influence microbial community composition, we considered the possible factors from sample collection, processing, and analysis to reduce the bias introduced by these factors and to enable us to identify the significant potential microbial metabolic networks in the rumen from a cohort of dairy cows that were adapted to a standard diet
We identified specific potential microbial metabolic interactions between bacteria and methanogenic archaea in the complex rumen microbial ecosystem (RME) of dairy cows

Summary

Introduction

Anaerobic microbial ecosystems are ubiquitous on the planet, contributing significantly to the recycling of nutrients such as carbon, nitrogen, and sulfur (Whitman et al, 1998; Mori and Kamagata, 2014), and play important roles in deconstruction of organic biomass, the global carbon cycle, agricultural production, and the health of animals and humans. Syntrophic Ruminal Bacteria-Archaea Associations conditions, anaerobic microorganisms exchange metabolic products for mutual benefit to survive and maintain a stable microbial community structure (Lovley, 2017). A known concept of microbial syntrophy, established in pure and mixed cultures, is the obligatory mutualism reported between bacteria and archaea for metabolic hydrogen (H2). This syntrophy, in which carbon is reduced to methane (CH4), is the hallmark of most anaerobic environments such as those found in freshwater sediments, swamps, paddy fields, landfills, and the intestinal tracts of ruminants and termites (Morris et al, 2013; Pitta et al, 2018). While there have been several theoretical and empirical reports on microbial syntrophy, information on the presence of microbial metabolic interactions in anaerobic microbial ecosystems, their functional relevance, how they change in temporal scales, and whether there is a natural selection for specific microbial metabolic interactions in anoxic environments is not completely understood

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