Chemical Links Between Redox Conditions and Estimated Community Proteomes from 16S rRNA and Reference Protein Sequences

Abstract

Environmental influences on community structure are often assessed through multivariate analyses in order to relate microbial abundances to separately measured physicochemical variables. However, genes and proteins are themselves chemical entities; in combination with genome databases, differences in microbial abundances directly encode for chemical variability. We predicted that the carbon oxidation state of inferred community proteomes, obtained by combining taxonomic abundances from published 16S rRNA gene sequencing datasets with predicted microbial proteomes from the NCBI Reference Sequence (RefSeq) database, would reflect environmental oxidation-reduction conditions in various natural and engineered settings including shale gas wells. Our analysis confirms the geobiochemical predictions for environmental redox gradients within and between hydrothermal systems and stratified lakes and marine environments. Where they are present, a common set of taxonomic groups (Gamma-and Deltaproteobacteria and Clostridia) act as drivers of the community-level differences in oxidation state, whereas Flavobacteria most often oppose the overall changes. The geobiochemical signal is largest for the steep redox gradients associated with hydrothermal systems and between surface water and produced fluids from shale gas wells, demonstrating the ability to determine the magnitude of redox effects on microbial communities from 16S sequencing alone.

Two dimensions of chemical variation of the human microbiome across body sites and in COVID-19 patients

“…In the first chemical dimension, the finding that community reference proteomes for skin and nasal communities are more oxidized than those for oral and gut communities (see also Fig. 2A) is congruent with previous analyses of metagenomic data from the Human Microbiome Project (HMP) by this laboratory [74] and another group [10]. This finding supports the notion that oxygenated habitats on the skin and in the airway are environmental filters for the evolution and growth of bacteria with genomes that code for relatively oxidized proteins.…”

“…On the whole, community reference proteomes and proteins predicted from metagenomes show similar ranges of Z C and (see Fig. 2D and [74]), but metaproteomes are relatively oxidized (Fig. 1C–E and Fig.…”

“…Reference proteomes of archaeal and bacterial taxa were made as described previously (Dick and Tan, 2023), except that GTDB was used instead of the NCBI Reference Sequence database (RefSeq). Briefly, for each genome in GTDB, the amino acid composition of all proteins was summed and divided by the number of proteins.…”

Using thermodynamics to obtain geochemical information from genomes

“…However, for optimal growth temperatures within a few degrees of 37 °C (where data for most mesophiles are available), the range of Z C of reference proteomes for Class I methanogens is lower than that for Class II methanogens (Figure 1b). Similarly, analysis of data from stratified water bodies, where variations of temperature are smaller than in hot springs, provides evidence for a link between oxygen concentrations and estimated Z C of reference proteomes for microbial communities (Dick & Tan, 2022). Therefore, although the effects of other variables cannot be discounted, available datasets support a primary effect of environmental redox potential on the carbon oxidation state of biomolecules.…”

“…Estimating the amino acid composition of community proteomes by combining reference proteomes with taxonomic abundances inferred from high‐throughput 16S rRNA gene sequencing provides another view of the chemical differences between communities. This method was used to identify large differences in Z C of community reference proteomes for hydrothermal systems as well as for redox gradients created by injection of oxidized surface water into reduced organic‐rich shales; in comparison, the differences in Z C are smaller in some stratified water bodies, but they are still aligned with the vertical oxygen gradients (Dick & Tan, 2022). While these examples from microbial ecology suggest that Z C is a useful indicator of chemical adaptation that is easily obtained from chemical formulas of biomolecules, relatively little is known about the chemical differences between genomes of organisms adapted to different redox conditions.…”