Evaluating the Assembly Dynamics in the Human Vaginal Microbiomes With Niche-Neutral Hybrid Modeling

Using 2,733 longitudinal vaginal microbiome samples (representing local microbial communities) from 79 individuals (representing meta-communities) in the states of healthy, BV (bacterial vaginosis) and pregnancy, we assess and interpret the relative importance of stochastic forces (e.g., stochastic drifts in bacteria demography, and stochastic dispersal) vs. deterministic selection (e.g., host genome, and host physiology) in shaping the dynamics of human vaginal microbiome (HVM) diversity by an integrated analysis with multi-site neutral (MSN) and niche-neutral hybrid (NNH) modeling. It was found that, when the traditional “default” P-value = 0.05 was specified, the neutral drifts were predominant (≥50% metacommunities indistinguishable from the MSN prediction), while the niche differentiations were moderate (<20% from the NNH prediction). The study also analyzed two challenging uncertainties in testing the neutral and/or niche-neutral hybrid models, i.e., lack of full model specificity – non-unique fittings of same datasets to multiple models with potentially different mechanistic assumptions – and lack of definite rules for setting the P-value thresholds (also noted as Pt-value when referring to the threshold of P-value in this article) in testing null hypothesis (model). Indeed, the two uncertainties can be interdependent, which further complicates the statistical inferences. To deal with the uncertainties, the MSN/NNH test results under a series of P-values ranged from 0.05 to 0.95 were presented. Furthermore, the influence of P-value threshold-setting on the model specificity, and the effects of woman’s health status on the neutrality level of HVM were examined. It was found that with the increase of P-value threshold from 0.05 to 0.95, the overlap (non-unique) fitting of MSN and NNH decreased from 29.1 to 1.3%, whereas the specificity (uniquely fitted to data) of MSN model was kept between 55.7 and 82.3%. Also with the rising P-value threshold, the difference between healthy and BV groups become significant. These findings suggested that traditional single P-value threshold (such as the de facto standard P-value = 0.05) might be insufficient for testing the neutral and/or niche neutral hybrid models.

Biogeographic Drivers of Evolutionary Radiations

Some lineages radiate spectacularly when colonizing a region, but others do not. Large radiations are often attributed to species’ adaptation into niches, or to other drivers, such as biogeography including dispersal ability and spatial structure of the landscape. Here we aim to disentangle the factors determining radiation size, by modeling simplified scenarios without the complexity of explicit niches. We build a spatially structured neutral model free from niches and incorporating a form of protracted speciation that accounts for gene flow between populations. We find that a wide range of radiation sizes are possible in this model depending on the combination of geographic isolation and species’ dispersal ability. At extremely low rates of dispersal between patches, each patch maintains its own endemic species. Intermediate dispersal rates foster larger radiations as they allow occasional movement between patches whilst sufficiently restricting gene flow to support further speciation in allopatry. As dispersal rates increase further, a critical point is reached at which demographically identical lineages may vary greatly in radiation size due to rare and stochastic dispersal events. At the critical point in dispersal frequency, some lineages remain a single species for a comparatively long time, whilst others with identical characteristics produce the largest radiations of all via a new mechanism for rapid radiation that we term a ‘radiation cascade’. Given a single species covering many patches connected with gene flow, a radiation cascade is triggered when stochastic dispersal is unusually low for a period, leading to an initial speciation event. This speciation means there are fewer individuals per species and thus further reduced gene flow between conspecifics. Reduced gene flow in turn makes it easier for further speciation to occur. During a radiation cascade, dispersal of individuals between patches continues at the same rate as before, but due to the increasing diversity it primarily introduces novel species that will later speciate, rather than adding to gene flow of existing species. Once a radiation cascade begins, it continues rapidly until it is arrested by a new equilibrium between speciation and extinction. We speculate that such radiation cascades may occur more generally and are not only present in neutral models. This process may help to explain rapid radiation, and the extreme radiation sizes of certain lineages with dispersing ancestors. Whilst niches no doubt play a role in community assembly, our findings lead us to question whether diversification and adaptation into niches is sometimes an effect of speciation and rapid radiation, rather than its cause.

Succession comprises a sequence of threshold-induced community assembly processes towards multidiversity

Research on ecological successions and community assembly shaped our understanding of community establishment, co-existence, and diversity. Although both lines of research address the same processes such as dispersal, species sorting, and biotic interactions, they lack unifying concepts. However, recent theoretical advances proposed to integrate both research lines and thus provided hypotheses on how communities assemble over time and form complex ecological systems. This framework predicts a sequence of stochastic and niche-based processes along successional gradients. Shifts in these assembly processes are assumed to occur abruptly once abiotic and biotic factors dominate over dispersal as main driver of community assembly. Considering the multidiversity composed of five organismal groups including plants, animals, and microbes, we empirically show that stochastic dispersal-dominated community assembly is replaced by environmental filters and biotic interactions after around 60 years of succession in a glacier forefield. The niche-based character of later successional processes is further supported by a pronounced decline in multi-beta-diversity after the shift in assembly processes. Our results support recent theories and provide new insights into the emergence of multidiverse and complex ecosystems. Our study will stimulate updates of concepts of community assembly considering multiple taxa with unique and complementary ecological roles and help to bridge the gap between research on successions and community assembly.

Coupling Bacterial Community Assembly to Microbial Metabolism across Soil Profiles

ABSTRACT Soil microbial community assembly is crucial for understanding the mechanisms of microbial communities that regulate ecosystem-level functioning. The relative contributions of stochastic and deterministic processes to microbial community assembly remain poorly defined, and major questions exist concerning the soil organic carbon (SOC) dynamics of microbial community assembly in deep soil. Here, the bacterial community assembly processes were explored across five soil profile depths (up to 80 cm) during a 15-year field experiment involving four fertilization regimes. We found that the bacterial community assembly was initially governed by deterministic selection in topsoil but was progressively structured by increasing stochastic dispersal with depth. The migration rate (m) and β-null deviation pattern supported the hypothesis of a relatively greater influence of dispersal in deep soil, which was correlated with bacterial community assembly by stochastic processes. These changes in the entire community assembly reflected consistent assembly processes of the two most dominant phyla, Acidobacteria and Chloroflexi. Structural equation modeling showed that soil features (pH and total phosphorus) and bacterial interactions (competition and network complexity) were significantly related to bacterial community assembly in the 0-to-10-cm and 10-to-20-cm layers. Partial Mantel tests, structural equation modeling, and random forest modeling consistently indicated a strong and significant correlation between bacterial community assemblages and SOC dynamics, implying that bacterial assembly processes would potentially suppress SOC metabolism and mineralization when the contributions of stochastic dispersal to communities increased in deeper layers. Our results have important implications for integrating bacterial community assembly processes into the predictions of SOC dynamics. IMPORTANCE We have provided a framework to better understand the mechanisms governing the balance between stochastic and deterministic processes and to integrate the shifts in community assembly processes with microbial carbon metabolism. Our study reinforced that environmental filtering and bacterial cooccurrence patterns influence the stochastic/deterministic continuum of soil bacterial community assembly and that stochasticity may act through deeper soil layers to influence carbon metabolism. Delineating theoretically the potential linkages between community assembly and SOC dynamics across a broad range of microbial systems represents an interesting topic for future research.

Fungal community assembly in drought-stressed sorghum shows stochasticity, selection, and universal ecological dynamics

Community assembly of crop-associated fungi is thought to be strongly influenced by deterministic selection exerted by the plant host, rather than stochastic processes. Here we use a simple, sorghum system with abundant sampling to show that stochastic forces (drift or stochastic dispersal) act on fungal community assembly in leaves and roots early in host development and when sorghum is drought stressed, conditions when mycobiomes are small. Unexpectedly, we find no signal for stochasticity when drought stress is relieved, likely due to renewed selection by the host. In our experimental system, the host compartment exerts the strongest effects on mycobiome assembly, followed by the timing of plant development and lastly by plant genotype. Using a dissimilarity-overlap approach, we find a universality in the forces of community assembly of the mycobiomes of the different sorghum compartments and in functional guilds of fungi.

The Chthonomonas calidirosea Genome Is Highly Conserved across Geographic Locations and Distinct Chemical and Microbial Environments in New Zealand's Taupō Volcanic Zone

ABSTRACTChthonomonas calidiroseaT49Tis a low-abundance, carbohydrate-scavenging, and thermophilic soil bacterium with a seemingly disorganized genome. We hypothesized that theC. calidiroseagenome would be highly responsive to local selection pressure, resulting in the divergence of its genomic content, genome organization, and carbohydrate utilization phenotype across environments. We tested this hypothesis by sequencing the genomes of fourC. calidiroseaisolates obtained from four separate geothermal fields in the Taupō Volcanic Zone, New Zealand. For each isolation site, we measured physicochemical attributes and defined the associated microbial community by 16S rRNA gene sequencing. Despite their ecological and geographical isolation, the genome sequences showed low divergence (maximum, 1.17%). Isolate-specific variations included single-nucleotide polymorphisms (SNPs), restriction-modification systems, and mobile elements but few major deletions and no major rearrangements. The 50-fold variation inC. calidirosearelative abundance among the four sites correlated with site environmental characteristics but not with differences in genomic content. Conversely, the carbohydrate utilization profiles of theC. calidiroseaisolates corresponded to the inferred isolate phylogenies, which only partially paralleled the geographical relationships among the sample sites. Genomic sequence conservation does not entirely parallel geographic distance, suggesting that stochastic dispersal and localized extinction, which allow for rapid population homogenization with little restriction by geographical barriers, are possible mechanisms ofC. calidiroseadistribution. This dispersal and extinction mechanism is likely not limited toC. calidiroseabut may shape the populations and genomes of many other low-abundance free-living taxa.IMPORTANCEThis study compares the genomic sequence variations and metabolisms of four strains ofChthonomonas calidirosea, a rare thermophilic bacterium from the phylumArmatimonadetes. It additionally compares the microbial communities and chemistry of each of the geographically distinct sites from which the fourC. calidiroseastrains were isolated.C. calidiroseawas previously reported to possess a highly disorganized genome, but it was unclear whether this reflected rapid evolution. Here, we show that each isolation site has a distinct chemistry and microbial community, but despite this, theC. calidiroseagenome is highly conserved across all isolation sites. Furthermore, genomic sequence differences only partially paralleled geographic distance, suggesting thatC. calidiroseagenotypes are not primarily determined by adaptive evolution. Instead, the presence ofC. calidiroseamay be driven by stochastic dispersal and localized extinction. This ecological mechanism may apply to many other low-abundance taxa.