Overlapping soil and gut microbiome compound processing potential in a gradient of ecosystem quality and subjects with type 2 diabetes

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Abstract

Background

Type 2 diabetes (T2D) is a complex metabolic disease with uncertain pathogenesis, including recognized influences from gut microbiome-host interactions and environmental factors. Meanwhile, soil microbiomes are known to shift in their composition and functional capacities with ecosystem condition, and represent an important environmental source for priming and resupplying the human gut microbiome.

Objectives

We sought to examine overlapping functional capacities in model case study microbial metagenomes from a gradient of soil ecosystem quality (disturbed to mature/natural sites under forest ecosystem restoration) and gut microbiomes in T2D versus normal health, to investigate plausible conceptual links (via ambient environmental exposures) between ecosystem degradation, soil microbiome disturbance and metabolic anomalies encoded in T2D gut metagenomes.

Methods

We used a novel method to translate metagenome functional capacities (i.e., function potential relative abundances %) to compound processing potential (CPP, %), reflecting potential metabolism at the scale of individual compounds. Soil ecosystem and T2D case study datasets were compared in terms of their potential metabolism for key metabolic compounds, via compound-wide trend analysis and community-wide function and CPP composition analyses.

Results

Potential metabolism of several important groups of compounds in soils and T2D (e.g., sugars, starches, proteins involved in fatty acid biosynthesis, aromatics involved in energy regulation) correlated strongly with soil disturbance and with T2D. Based on our findings, we derived a preliminary gut microbiome index for T2D status informed by consistent CPP trends found in both disturbed soils and T2D gut samples that was capable of discriminating T2D from normal healthy subjects (Wilcox-Mann-Whitney W = 1001, P = <0.001).

Discussion

Our findings support the profound new hypothesis that soil microbiome exposures from disturbed ecosystems, together with starch-rich diets, may bias the functional capacity profile of the human gut microbiome in T2D. Our hypothesis, that ecosystem degradation and exposure to associated disturbed soils contribute to T2D gut microbiomes which have (1) excessive potential to metabolise compounds involved in energy harvesting, and (2) deficient potential to metabolise compounds involved in energy management (e.g., storage, regulation), warrants further investigation.

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