Does diversity beget diversity in microbiomes?
- Département de sciences biologiques, Université de Montréal, Canada
- European Centre for Environment and Human Health, University of Exeter, United Kingdom
- Department of Microbiology and Immunology, McGill University, Canada
- McGill Genome Centre, McGill University, Canada
Figures
Figure 1
Contrasting the Diversity Begets Diversity (DBD) and Ecological Controls (EC) models.
(A). In this hypothetical scenario, microbiome sample 1 contains one non-focal genus, and two amplicon sequence variants (ASVs) within the focal genus (point at x = 1, y = 2 in the plot). Sample 2 …
Figure 2 with 26 supplements
Focal-lineage diversity as a function of community diversity in the top two most prevalent taxa at each taxonomic level.
As in Figure 1, the x-axes show community diversity in units of the number of non-focal taxa (e.g. the number of non-Proteobacteria phyla for the left-most column), and the y-axes show the taxonomic …
Figure 2—figure supplement 1
Distributions of diversity slope estimates across different random effects, from the GLMMs predicting focal lineage diversity as a function of community diversity.
(A) Class:Phylum, (B) Order:Class, (C) Family:Order, (D) Genus:Family, and (E) ASV:Genus. Estimation of random effect coefficients from the GLMMs (Table S1), shows that the effect of diversity on …
Figure 2—figure supplement 2
Focal-lineage diversity as a function of community diversity across biomes in Proteobacteria.
Linear models are shown for the number of classes per phylum (y-axis) as a function of community diversity (number of non-focal phyla, x-axis) in each of the 17 environments (EMPO3 biomes). Only …
Figure 2—figure supplement 3
Focal-lineage diversity as a function of community diversity across biomes in Bacteroidetes.
Linear models are shown for the number of classes per phylum (y-axis) as a function of community diversity (number of non-focal phyla, x-axis) in each of the 17 environments (EMPO3 biomes). Only …
Figure 2—figure supplement 4
Focal-lineage diversity as a function of community diversity across biomes in Actinobacteria.
Linear models are shown for the number of classes per phylum (y-axis) as a function of community diversity (number of non-focal phyla, x-axis) in each of the 17 environments (EMPO3 biomes). Only …
Figure 2—figure supplement 5
Focal-lineage diversity as a function of community diversity across biomes in Gammaproteobacteria.
Linear models are shown for the number of orders per class (y-axis) as a function of community diversity (non-focal classes, x-axis) in each of the 17 environments (EMPO3 biomes). Only environments …
Figure 2—figure supplement 6
Focal-lineage diversity as a function of community diversity across biomes in Alphaproteobacteria.
Linear models are shown for the number of orders per class (y-axis) as a function of community diversity (non-focal classes, x-axis) in each of the 17 environments (EMPO3 biomes). Only environments …
Figure 2—figure supplement 7
Focal-lineage diversity as a function of community diversity across biomes in Actinobacteria.
Linear models are shown for the number of orders per class (y-axis) as a function of community diversity (non-focal classes, x-axis) in each of the 17 environments (EMPO3 biomes). Only environments …
Figure 2—figure supplement 8
Focal-lineage diversity as a function of community diversity across biomes in Actinomycetales.
Linear models are shown for the number of families per order (y-axis) as a function of community diversity (non-focal orders, x-axis) in each of the 17 environments (EMPO3 biomes). Only environments …
Figure 2—figure supplement 9
Focal-lineage diversity as a function of community diversity across biomes in Flavobacteriales.
Linear models are shown for the number of families per order (y-axis) as a function of community diversity (non-focal orders, x-axis) in each of the 17 environments (EMPO3 biomes). Only environments …
Figure 2—figure supplement 10
Focal-lineage diversity as a function of community diversity across biomes in Rhizobiales.
Linear models are shown for the number of families per order (y-axis) as a function of community diversity (non-focal orders, x-axis) in each of the 17 environments (EMPO3 biomes). Only environments …
Figure 2—figure supplement 11
Focal-lineage diversity as a function of community diversity across biomes in Flavobacteriaceae.
Linear models are shown for genera per family (y-axis) as a function of community diversity (non-focal families, x-axis) in each of the 17 environments (EMPO3 biomes). Only environments containing …
Figure 2—figure supplement 12
Focal-lineage diversity as a function of community diversity across biomes in Sphingomonadaceae.
Linear models are shown for genera per family (y-axis) as a function of community diversity (non-focal families, x-axis) in each of the 17 environments (EMPO3 biomes). Only environments containing …
Figure 2—figure supplement 13
Focal-lineage diversity as a function of community diversity across biomes in Verrucomicrobiaceae.
Linear models are shown for genera per family (y-axis) as a function of community diversity (non-focal families, x-axis) in each of the 17 environments (EMPO3 biomes). Only environments containing …
Figure 2—figure supplement 14
Focal-lineage diversity as a function of community diversity across biomes in Pseudomonas.
Linear models are shown for ASVs per genus (y-axis) as a function of community diversity (non-focal genera, x-axis) in each of the 17 environments (EMPO3 biomes). Only environments containing the …
Figure 2—figure supplement 15
Focal-lineage diversity as a function of community diversity across biomes in Planctomyces.
Linear models are shown for ASVs per genus (y-axis) as a function of community diversity (non-focal genera, x-axis) in each of the 17 environments (EMPO3 biomes). Only environments containing the …
Figure 2—figure supplement 16
Focal-lineage diversity as a function of community diversity across biomes in Clostridium.
Linear models are shown for ASVs per genus (y-axis) as a function of community diversity (non-focal genera, x-axis) in each of the 17 environments (EMPO3 biomes). Only environments containing the …
Figure 2—figure supplement 17
Null models based on Neutral Theory.
Results are shown from data simulated under (A) neutral Model 1, (B) neutral Model 2, or (C) neutral Model 3. Model 1 is sampled from the zero-sum multinomial distribution with a single distribution …
Figure 2—figure supplement 18
Lineage diversity (mean ASV:Genus ratio among all lineages) as a function of community diversity (number of genera) in the EMP data.
Samples from different environments (EMPO level 3) are shown in different colours, each with their corresponding linear model fit.
Figure 2—figure supplement 19
Taxonomic ratios estimated from simulated rarefied sequence data.
Each panel simulates a set of microbiome samples that differ in their diversity (number of genera in left panels A and B, number of phyla in right panels C and D) while maintaining a set true …
Figure 2—figure supplement 20
Linear, quadratic, and cubic models for the relationship between focal-lineage diversity and community diversity for varying levels of % nucleotide identity.
Community diversity was estimated as the number of clusters at a focal level (di) and focal-lineage diversity as the mean of the clusters at the rank above (di 1/di). All P-values are <0.001. Linear …
Figure 2—figure supplement 21
Focal clusters at 75% nucleotide identity.
Community diversity was estimated as the number of clusters at a focal level (di) and focal lineage diversity as the mean of the clusters at the rank above (di 1/di). Linear (grey), quadratic (blue) …
Figure 2—figure supplement 22
Focal clusters at 80% nucleotide identity.
Community diversity was estimated as the number of clusters at a focal level (di) and focal lineage diversity as the mean of the clusters at the rank above (di 1/di). Linear (grey), quadratic (blue) …
Figure 2—figure supplement 23
Focal clusters at 85% nucleotide identity.
Community diversity was estimated as the number of clusters at a focal level (di) and focal lineage diversity as the mean of the clusters at the rank above (di 1/di). Linear (grey), quadratic (blue) …
Figure 2—figure supplement 24
Focal clusters at 90% nucleotide identity.
Community diversity was estimated as the number of clusters at a focal level (di) and focal lineage diversity as the mean of the clusters at the rank above (di 1/di). Linear (grey), quadratic (blue) …
Figure 2—figure supplement 25
Focal clusters at 95% nucleotide identity.
Community diversity was estimated as the number of clusters at a focal level (di) and focal lineage diversity as the mean of the clusters at the rank above (di 1/di). Linear (grey), quadratic (blue) …
Figure 2—figure supplement 26
Focal clusters at 97% nucleotide identity.
Community diversity was estimated as the number of clusters at a focal level (di) and focal lineage diversity as the mean of the clusters at the rank above (di 1/di). Linear (grey), quadratic (blue) …
Figure 3
The diversity slope of focal taxa is higher in low-diversity (often host-associated) microbiomes.
The x-axis shows the mean number of non-focal taxa: (A) phyla, (B) classes, and (C) orders in each biome. On the y-axis, the diversity slope was estimated by a GLMM predicting focal lineage …
Figure 4 with 1 supplement
The DBD relationship varies between resident and non-resident genera.
(A) Ordination showing genera clustering into their preferred environment clusters. The matrix of 17 environments (rows) by 1128 genera (columns) by, with the matrix entries indicating the …
Figure 4—figure supplement 1
Resident genera of environment clusters.
Results from indicator species analysis illustrated as a heatmap. Only the 25 resident genera with the highest indval indices and p<0.05 (permutation test) are shown for every environment cluster …
Figure 5
Positive effect of genome size on DBD.
Results are shown from a GLMM predicting focal lineage diversity as a function of the interaction between community diversity and genome size at the ASV:Genus ratio (Supplementary file 1 Section 6). …
Tables
Table 1
Effects of community diversity on focal lineage diversity across taxonomic ratios.
The GLMMs show a statistically significant positive effect of community diversity on focal lineage diversity. Each row reports the effect of community diversity (Div) on focal lineage diversity, as …
| Slope (fixed effects) | Standard deviation on the slope (random effects) | ||||||||
|---|---|---|---|---|---|---|---|---|---|
| Div | SE | z | P | Env | Lin | Lin*Env | Env*Lab | Sample | |
| ASV:Genus | 0.091 | 0.016 | 5.792 | 6.95e-09 | n.s. | 0.074 | 0.142 | 0.114 | 0.067 |
| Genus:Family | 0.047 | 0.008 | 5.911 | 3.41e-09 | n.s. | 0.071 | 0.07 | 0.039 | n.s. |
| Family:Order | 0.119 | 0.017 | 7.001 | 2.54e-12 | 0.023 | 0.094 | 0.092 | 0.106 | n.s. |
| Order:Class | 0.109 | 0.020 | 5.447 | 5.13e-08 | 0.05 | 0.141 | 0.078 | 0.051 | n.s. |
| Class:Phylum | 0.272 | 0.043 | 6.341 | 2.29e-10 | 0.119 | 0.174 | 0.119 | 0.114 | n.s. |
Table 2
GLMMs applied to data simulated under null models.
Null models 1 and 2 were generated under the ZSM distribution, with a single distribution for the whole dataset (Model 1) or one distribution per environment (Model 2). Model 3 is similar to Model …
| Slope (fixed effects) | Stand dev on the slope (random effects) | |||||||
|---|---|---|---|---|---|---|---|---|
| Div | SE | z | P | Env | Lin | Lin*Env | Sample | |
| Model 1 | −0.005 | 0.000 | −9.807 | <2 e −16 | n.t. | 0.639 | n.t. | n.s. |
| Model 2 | n.s. | |||||||
| Model 3 | −0.012 | 0.002 | −6.552 | 5.69e-11 | n.t. | 0.021 | n.t. | n.s. |
| Model 3 + DBD | 0.016 | 0.001 | 11.48 | <2e-16 | n.t. | 0.008 | n.t. | n.s. |
| Model 3 + EC | −0.011 | 0.002 | −6.14 | 8.26e-10 | n.t. | ns | n.t. | n.s. |
Table 3
GLMMs with community diversity measured using Shannon diversity.
Results are shown from GLMMs with Shannon diversity of non-focal taxa (Div) as a predictor of ASVs richness of focal taxa. Each row reports the estimate (Div), as well as its standard error, Wald …
| Fixed effects | Random effects | ||||||||
|---|---|---|---|---|---|---|---|---|---|
| Div | SE | z | p | Env | Lin | Env*Lin | Env*Lab | Sample | |
| Genus | 0.055 | 0.013 | 4.33 | 1.49e-05 | n.s. | 0.08 | 0.15 | 0.085 | 0.054 |
| Family | 0.148 | 0227 | 6.491 | 8.51e-11 | n.s. | 0.184 | 0.268 | 0.16 | 0.134 |
| Order | 0.378 | 0.038 | 9.864 | <2e-16 | n.s. | 0.34 | 0.417 | 0.258 | 0.202 |
| Class | 0.398 | 0.05 | 7.973 | 1.54e-15 | n.s. | 0.369 | 0.46 | 0.326 | 0.262 |
| Phylum | 0.319 | 0.088 | 3.614 | 0.0003 | 0.169 | 0.316 | 0.5 | 0.495 | 0.378 |
Table 4
Community diversity has a stronger effect than abiotic factors on focal lineage diversity (EMP dataset).
Results are shown from GLMMs with community diversity (Div), four abiotic factors (temperature, elevation, pH, and latitude), and their interactions with community diversity, as predictors of focal …
| Predictor | Est | SE | P | |
|---|---|---|---|---|
| ASV:Genus | Div | 0.128 | 0.013 | <2e-16 |
| Temperature | 0.04 | 0.014 | 0.00479 | |
| Div*Temperature | 0.043 | 0.014 | 0.00175 | |
| Div*Latitude | 0.031 | 0.013 | 0.02119 | |
| Div*Elevation | −0.031 | 0.014 | 0.02829 | |
| Genus:Family | Div | 0.094 | 0.009 | <2e-16 |
| Temperature | 0.026 | 0.009 | 0.00268 | |
| pH | −0.042 | 0.009 | 5.88e-06 | |
| Family:Order | Div | 0.131 | 0.01 | <2e-16 |
| Order:Class | Div | 0.184 | 0.01 | <2e-16 |
| Div*Temperature | 0.032 | 0.009 | 0.000827 | |
| Div*Latitude | 0.023 | 0.008 | 0.005403 | |
| Class:Phylum | Div | 0.236 | 0.011 | <2e-16 |
| Div*Temperature | 0.059 | 0.014 | 2.15e-05 | |
| Div*Latitude | 0.03 | 0.011 | 0.00884 |
Table 5
GLMMs applied to a soil dataset.
Each row reports the taxonomic ratio, the predictors used in the GLMM (fixed effects only), their estimate (Est), standard error (SE) and P-value (P) (Wald test). Left columns: GLMM with community …
| GLMMs with abiotic variables | GLMMs with the 3 first PCs | |||||||
|---|---|---|---|---|---|---|---|---|
| Predictor | Est | SE | P | Predictor | Est | SE | P | |
| ASV:Genus | Div | n.s. | Div | 0.064 | 0.016 | 9.47e-05 | ||
| Latitude | 0.294 | 0.025 | <2e-16 | PC1 | −0.065 | 0.007 | <2e-16 | |
| UV_light | −0.177 | 0.016 | <2e-16 | PC2 | −0.03 | 0.006 | 1.98e-05 | |
| MDR | 0.028 | 0.006 | 7.12e-06 | |||||
| NPP2003_2015 | −0.066 | 0.005 | <2e-16 | |||||
| Latitude^2 | −0.3 | 0.029 | <2e-16 | |||||
| Clay_silt^2 | −0.012 | 0.004 | 0.003 | |||||
| Soil_N^2 | −0.007 | 0.001 | 1.66e-06 | |||||
| Soil_C_N_ratio^2 | 0.003 | 0.001 | 0.004 | |||||
| PSEA^2 | 0.01 | 0.002 | 4.84e-06 | |||||
| MDR^2 | 0.017 | 0.003 | 2.40e-08 | |||||
| NPP2003_2015^2 | −0.016 | 0.004 | 0.0001 | |||||
| Genus:Family | Div | 0.032 | 0.01 | 0.0011 | Div | 0.033 | 0.01 | 0.001 |
| Latitude | −0.035 | 0.006 | 2.04e-09 | PC1 | −0.016 | 0.006 | 0.02 | |
| PC2 | 0.02 | 0.006 | 0.00089 | |||||
| Family:Order | Div | n.s. | Div | n.s. | ||||
| Latitude | −0.0005 | 0.0002 | 0.0105 | PC1 | −0.026 | 0.007 | 0.00032 | |
| Div*PC1 | 0.04 | 0.006 | 2.14e-12 | |||||
| Div*PC3 | 0.023 | 0.005 | 1.68e-06 | |||||
| Order:Class | Null model with no predictor was significant | |||||||
| Class:Phylum | Div | 0.032 | 0.01 | 0.00174 | Div | 0.032 | 0.01 | 0.003 |
| pH | 0.074 | 0.01 | 4.37e-13 | PC1 | −0.051 | 0.01 | 3.54e-07 | |
| PC2 | −0.028 | 0.01 | 0.006 | |||||
Additional files
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Supplementary file 1
Full GLMM outputs for the EMP data.
- https://cdn.elifesciences.org/articles/58999/elife-58999-supp1-v3.pdf
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Supplementary file 2
Goodness of fit for the GLMMs.
- https://cdn.elifesciences.org/articles/58999/elife-58999-supp2-v3.docx
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Supplementary file 3
Full GLMM output for simulated data under Neutral Theory models.
- https://cdn.elifesciences.org/articles/58999/elife-58999-supp3-v3.pdf
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Supplementary file 4
Full GLMM output for soil data (Delgado-Baquerizo et al., 2018).
- https://cdn.elifesciences.org/articles/58999/elife-58999-supp4-v3.pdf
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Supplementary file 5
Indicator species analysis.
The table shows the assignment of each genus to one of three environment types.
- https://cdn.elifesciences.org/articles/58999/elife-58999-supp5-v3.xlsx
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Supplementary file 6
Genome size assignment.
The table shows genome sizes assigned to each genus.
- https://cdn.elifesciences.org/articles/58999/elife-58999-supp6-v3.xlsx
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Transparent reporting form
- https://cdn.elifesciences.org/articles/58999/elife-58999-transrepform-v3.pdf
