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Hayashi, I.

Publications and source records attributed to Hayashi, I..

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Environmental filtering and host identity collectively shape root-associated microbiomes of Ericaceae and ectomycorrhizal plants in fumarole fields

Background Symbiosis with microbes is a key strategy that has enabled plants to colonize extreme environments. Since the benefits conferred by root-associated microbes depend on both environmental conditions and host-microbe combinations, plant adaptation to harsh environments is closely linked to the assembly of root microbial communities. Understanding how environmental and host filtering jointly shape these communities is therefore fundamental to elucidating the mechanisms underlying plant adaptation to extreme environments. Results In this study, we investigated the differentiation of root-associated prokaryotic and fungal communities and individual operational taxonomic units (OTUs) across two contrasting habitats surrounding fumaroles, solfatara-field and forest-edge habitats, and six dominant Ericaceae and ectomycorrhizal plant taxa. Prokaryotic and fungal OTUs rarely exhibited strong preferences for both habitat and host identity. Instead, many of prokaryotic and fungal OTUs specialized to one of these niches, collectively generating root microbial communities differentiated by both factors. Nonetheless, striking specializations in habitat and host niches were observed in the fungal family Hyaloscyphaceae (Helotiales). To gain insight into the evolutionary basis of microbial specialization, we examined phylogenetic signals in preference phenotypes. The resulting weak phylogenetic signals in these preference phenotypes further suggest that this fungal clade has undergone substantial ecological divergence. Conclusion Overall, our findings indicate that root-associated microbial communities in extreme environments are assembled through the accumulation of microbial taxa specialized to either habitat or host, and that strong ecological specialization in fungi can arise with little phylogenetic constraint.

microbiology↗

Stochastic Forces in Microbial Community Assembly: Founding Community Size Governs Divergent Ecological Trajectories

Biological community dynamics are organized by the interplay of deterministic and stochastic processes. While species responses to biotic and abiotic environments determine the attractors of community compositions, stochastic processes, especially those in early stages of community assembly, can drastically influence the direction of temporal ecological dynamics. Nonetheless, establishing quantitative insights into the roles of stochastic processes has remained a major challenge. By developing a multi-replicated experimental system for tracking community assembly, we quantitatively evaluated the extent to which stochasticity could cause the divergence of community dynamics. We constructed soil- and freshwater-derived experimental microbial assemblages (microbiomes) with varying foundation community size, thereby controlling variation in initial community compositions among replicate communities (i.e., initial stochasticity). An analysis of > 3,000 community samples across four time points then indicated that higher levels of initial stochasticity could result in greater divergence of population- and community-level consequences. From the quantitative perspective, conspicuous differentiation into alternative trajectories of community assembly occurred when the absolute number of founding prokaryotic cells was less than the order of 104. Furthermore, the replicate microbiomes differed in dominant Pseudomonas species, suggesting divergence into alternative transient/stable states through competitive exclusion between species occupying similar niches. Overall, our experiment showed that quantitative differences in stochasticity could result in qualitative differences in the fate of ecological communities. Further quantitative insights into stochasticity in community assembly will reorganize our views on biological invasions, agroecosystem microbiome management, and therapeutics of human-associated microbiomes.

ecology↗

Deterministic and stochastic processes generating alternative states of microbiomes

The structure of microbial communities is often classified into discrete or semi-discrete compositions of taxa as represented by "enterotypes" of human gut microbiomes. Elucidating mechanisms that generate such "alternative states" of microbiome compositions has been one of the major challenges in ecology and microbiology. In a time-series analysis of experimental microbiomes, we here show that both deterministic and stochastic ecological processes drive divergence of alternative microbiome states. We introduced species-rich soil-derived microbiomes into eight types of culture media with 48 replicates, monitoring shifts in community compositions at six time points (8 media x 48 replicates x 6 time points = 2,304 community samples). We then confirmed that microbial community structure diverged into a few discrete states in each of the eight medium conditions as predicted in the presence of both deterministic and stochastic community processes. In other words, microbiome structure was differentiated into a small number of reproducible compositions under the same environment. This fact indicates not only the presence of selective forces leading to specific equilibria of community-scale resource use but also the influence of demographic drift (fluctuations) across basins of such equilibria. A reference-genome analysis further suggested that the observed alternative states differed in ecosystem-level functions. These findings will help us examine how microbiome structure and functions can be controlled by changing the "stability landscapes" of ecological community compositions.

ecology↗

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

Species utilizing the same resources often fail to coexist for extended periods of time. Such competitive exclusion mechanisms potentially underly microbiome dynamics, causing breakdowns of communities composed of species with similar genetic backgrounds of resource utilization. Although genes responsible for competitive exclusion among a small number of species have been investigated in pioneering studies, it remains a major challenge to integrate genomics and ecology for understanding stable coexistence in species-rich communities. Here, we show that community-scale analyses of functional gene redundancy can provide a useful platform for interpreting and predicting collapse of bacterial communities. Through 110-day time-series of experimental microbiome dynamics, we analyzed the metagenome-assembled genomes of co-occurring bacterial species. We then inferred ecological niche space based on the multivariate analysis of the genome compositions. The analysis allowed us to evaluate potential shifts in the level of niche overlap between species through time. We hypothesized that community-scale pressure of competitive exclusion could be evaluated by quantifying overlap of genetically determined resource-use profiles (metabolic pathway profiles) among coexisting species. We found that the degree of community compositional changes observed in the experimental microbiome was explained by the magnitude of gene-repertoire overlaps among bacterial species. The metagenome-based analysis of genetic potential for competitive exclusion will help us forecast major events in microbiome dynamics such as sudden community collapse (i.e., dysbiosis).

microbiology↗

Core species and interactions prominent in fish-associated microbiome dynamics

In aquatic ecosystems, the health of fish depends greatly on the dynamics of microbial community structure in the background environment. Nonetheless, finding microbes with profound impacts on fishs performance out of thousands of candidate species remains a major challenge. We here show that time-series analyses of microbial population dynamics illuminate core components and structure of fish-associated microbiomes. By targeting eel aquaculture microbiomes as model systems, we reconstructed the population dynamics of 9,605 bacterial and 303 archaeal species/strains across 128 days. Due to the remarkable increase/decrease of constituent microbial populations, the taxonomic compositions of microbiomes changed drastically through time. We then found that some specific microbial taxa showed positive relationship with eels activity level even after excluding cofounding effects of environmental parameters (pH and dissolved oxygen level) on population dynamics. In particular, a vitamin B12-producing bacteria, Cetobacterium somerae, consistently showed strong positive associations with eels activity level across the replicate time-series of the five aquaculture tanks. Network theoretical and metabolic modeling analyses further suggested that the highlighted bacterium formed compartments of close microbe-to-microbe interactions with some other bacterial taxa, forming potential core microbiomes with positive impacts on eels. Overall, these results suggest that integration of microbiology, ecological theory, and network science allows us to explore core species and interactions embedded within complex dynamics of fish-associated microbiomes.

ecology↗

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

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.

ecology↗

CLASP2 lattice-binding near microtubule plus ends stabilizes kinetochore attachments

The fine regulation of kinetochore microtubule dynamics during mitosis ensures proper chromosome segregation by promoting error correction and spindle assembly checkpoint (SAC) satisfaction. CLASPs are widely conserved microtubule plus-end-tracking proteins that regulate microtubule dynamics throughout the cell cycle and independently localize to kinetochores during mitosis. Thus, CLASPs are ideally positioned to regulate kinetochore microtubule dynamics, but the underlying molecular mechanism remains unknown. Here we found that human CLASP2 can dimerize through its C-terminal kinetochore-targeting domain, but kinetochore localization was independent of dimerization. CLASP2 kinetochore localization, microtubule plus-end-tracking and microtubule lattice binding through TOG2 and TOG3 (but not TOG1) domains, independently sustained normal spindle length, timely SAC satisfaction, chromosome congression and faithful segregation. Measurements of kinetochore microtubule half-life in living cells expressing RNAi-resistant mutants revealed that CLASP2 kinetochore localization, microtubule plus-end-tracking and lattice binding cooperatively modulate kinetochore microtubule stability during mitosis. Thus, CLASP2 regulates kinetochore microtubule dynamics by integrating distinctive microtubule-binding properties at the kinetochore-microtubule interface to ensure chromosome segregation fidelity.

cell biology↗