Alternative stable states, nonlinear behavior, and predictability of microbiome dynamics

Abstract

Microbiome dynamics are both crucial indicators and drivers of human health, agricultural output, and industrial bio-applications. However, predicting microbiome dynamics is notoriously difficult because communities often show abrupt structural changes, such as dysbiosis in human microbiomes. We here integrate theoretical and empirical bases for anticipating drastic shifts of microbial communities. We monitored 48 experimental microbiomes for 110 days and observed that various community-level events, including collapse and gradual compositional changes, occurred according to a defined set of environmental conditions. We then confirmed that the abrupt community changes observed through the time-series could be described as shifts between alternative stable states or dynamics around complex attractors. Furthermore, collapses of microbiome structure were successfully anticipated by means of the diagnostic threshold defined with the energy landscape analysis of statistical physics or that of a stability index of nonlinear mechanics. These results indicate that abrupt microbiome events in complex microbial communities can be forecasted by extending classic ecological concepts to the scale of species-rich microbial systems.

Metagenomic analysis of ecological niche overlap and community collapse in microbiome dynamics

“…2; Supplementary Table 1). As indicated in the amplicon sequencing analysis 19 (Fig. 1a), drastic shifts from taxon-rich community states to oligopolistic states was observed around Day 20 in the shotgun sequencing analysis (Fig.…”

“…Target microbiome. We focused on the experimental microbiome showing drastic shifts in taxonomic compositions 19 . In a previous study 19 , a 110-day monitoring of microbiomes was performed with six experimental settings.…”

“…It is essential to examine whether such competition-driven population-level phenomena underly drastic ecological events observed at the community level. Microbial communities sometimes show sudden and substantial changes in species and/or taxonomic compositions [17][18][19] . Human gut microbiomes, for example, have been reported to show drastic shifts from species-rich states to "imbalanced" states with low a-diversity and overrepresentation of pathogenic species [20][21][22][23] (e.g., Clostridium difficile).…”

“…We here show how degree of gene-repertoire overlap changes through dynamics of species-rich microbial communities. By targeting an experimental microbial system showing rapid and substantial changes in taxonomic compositions 19 , we reconstruct niche space depicting species' gene repertoires. Based on a whole-genome shotgun metagenomic analysis at 13 time points within the 110-day time-series of the microbiome experiment, we reveal temporal shifts in the magnitude of gene repertoire overlap among microbial species.…”

Core species and interactions prominent in fish-associated microbiome dynamics

“…For the analyses of microbiome dynamics, water was sampled from each aquaculture tank every 24 hours during 128 days. By applying a quantitative amplicon sequencing approach for estimating 16S ribosomal RNA gene (16S rRNA) copy concentrations of respective microbes 22,23 , we obtained time-series datasets representing the increase/decrease of 9,605 bacterial and 303 archaeal ASVs representing 618 genera and 325 families (Fig. 1a).…”