Suppression of common species enables bacterial rarity in dry soils

A chosen few, common species are globally widespread. On the other hand, rare bacterial species display high sensitivity to environmental conditions at low relative abundances. Predictable shifts in soil bacterial rarity occur across biomes primarily driven by soil hydration conditions.
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Soils host some of the most diverse microbiomes, yet only a few phylotypes (or “species” for simplicity) occur consistently across environments. The increasing recognition of subterranean biodiversity's importance for global ecosystem functioning is motivated by studies elucidating the mechanisms that shape microbial habitats1. Climatic drivers, such as the expected rainfall frequency and average soil water contents, determine the distribution of resource fluxes that directly affect bacterial diversity and abundance across spatial scales2. Many properties of soil (micro-) environments result from a climatic water balance that determines a biome's primary productivity (e.g., carbon input flux) and chemistry (e.g., the soil buffering capacity and soil pH).

Statistical analysis has demonstrated that the richness of bacterial taxa with low relative abundance is sensitive to environmental factors, notably climatic water content3. Such changes in the shape of the relative abundance distribution (RAD) could be caused by soil water content that alters the diffusion of nutrients. Hence, we expected rainfall frequency and soil type to govern the composition of soil bacterial communities by shaping the distribution and availability of resources.

To detect changes in rarity, we developed a classification scheme that labels bacteria as "common" and “rare” using only the global RAD. This approach revealed that dry soils from environments characterized by low rainfall frequencies contain around seven times more rare species than wetter soils. The relative abundance of rare species also systematically declined towards high climatic water contents contrasting the disproportionate increase in biomass.

Observed proportion and richness of common and rare bacteria across biomes.
a Global relative abundance distribution (RAD) of bacterial species (n = 844). The dashed line indicates the threshold based on minimum cross-entropy that distinguishes common and rare species using only the global RAD (shown in blue and red, respectively). b, c Bacterial richness and relative abundance (RA) for common and rare bacteria vary across biomes. Stacked bars indicate the median ± IQR. The number of samples for each biome is reported (G = grassland, F = forest). b Richness of rare bacteria varies more strongly among biomes compared to common bacteria, while, c their RA seldom exceeds the RA of common species.

To understand why the ratio of bacterial diversity to biomass changes4 (i.e., how the distribution of resources among species varies), we used a detailed model to simulate multi-species bacterial communities for different soil moisture conditions. Findings support the systematic increase of rare species proportion and richness towards drier soils with low carrying capacity5. The model results suggest that fast growth characterizes common species that lose their physiological advantage in drier environments where the resource fluxes are limiting6. This suppression of globally common species enables local communities with higher evenness in terms of RADs and growth rates5.

In addition to direct physiological limitations, we expect reduced interactions among different species in dry soils with fragmented aqueous phase that also restricts motility of bacterial cells. The soil hydration conditions affect habitat connectivity and bacterial biomass that underlie the patterns of bacterial rarity. Bacterial rarity varies predictably across terrestrial biomes with systematic shifts in RADs between communities from different environments. Dry regions harbor more even and species-rich communities at very low biomass; providing a rich genetic pool that is sensitive to climatic shifts5.

References

  1. FAO, ITPS, GSBI, SCBD and EC. State of knowledge of soil biodiversity - Status, challenges and potentialities. (FAO, 2020). doi:10.4060/cb1928en.
  2. Bickel, S. & Or, D. Soil bacterial diversity mediated by microscale aqueous-phase processes across biomes. Nat. Commun. 11, 1–9 (2020) doi:10.1038/s41467-019-13966-w.
  3. Bickel, S., Chen, X., Papritz, A. & Or, D. A hierarchy of environmental covariates control the global biogeography of soil bacterial richness. Sci. Rep. 9, 1–10 (2019) doi:10.1038/s41598-019-48571-w.
  4. Bastida, F. et al. Soil microbial diversity–biomass relationships are driven by soil carbon content across global biomes. ISME J. 1–11 (2021) doi:10.1038/s41396-021-00906-0.
  5. Bickel, S. & Or, D. The chosen few—variations in common and rare soil bacteria across biomes. ISME J. (2021) doi:10.1038/s41396-021-00981-3.
  6. Šťovíček, A., Kim, M., Or, D. & Gillor, O. Microbial community response to hydration-desiccation cycles in desert soil. Sci. Rep. 7, 1–9 (2017) doi:10.1038/srep45735.