Metabolism in the Niche: a Large-Scale Genome-Based Survey Reveals Inositol Utilization To Be Widespread among Soil, Commensal, and Pathogenic Bacteria.

Abstract

ABSTRACTPhytate is the main phosphorus storage molecule of plants and is therefore present in large amounts in the environment and in the diet of humans and animals. Its dephosphorylated form, the polyol myo-inositol (MI), can be used by bacteria as a sole carbon and energy source. The biochemistry and regulation of MI degradation were deciphered in Bacillus subtilis and Salmonella enterica, but a systematic survey of this catabolic pathway has been missing until now. For a comprehensive overview of the distribution of MI utilization, we analyzed 193,757 bacterial genomes, representing a total of 24,812 species, for the presence, organization, and taxonomic prevalence of inositol catabolic gene clusters (IolCatGCs). The genetic capacity for MI degradation was detected in 7,384 (29.8%) of all species for which genome sequences were available. IolCatGC-positive species were particularly found among Actinobacteria and Proteobacteria and to a much lesser extent in Bacteroidetes. IolCatGCs are very diverse in terms of gene number and functions, whereas the order of core genes is highly conserved on the phylum level. We predict that 111 animal pathogens, more than 200 commensals, and 430 plant pathogens or rhizosphere bacteria utilize MI, underscoring that IolCatGCs provide a growth benefit within distinct ecological niches.IMPORTANCE This study reveals that the capacity to utilize inositol is unexpectedly widespread among soil, commensal, and pathogenic bacteria. We assume that this yet-neglected metabolism plays a pivotal role in the microbial turnover of phytate and inositols. The bioinformatic tool established here enables predicting to which extent and genetic variance a bacterial determinant is present in all genomes sequenced so far.