Unravelling the interplay of ecological processes structuring the bacterial rare biosphere

Abstract

Most ecological communities harbor many rare species (i.e., the rare biosphere), however, relatively little is known about how distinct ecological processes structure their existence. Here, we used spatiotemporal data on soil bacterial communities along a natural ecosystem gradient to model the relative influences of assembly processes structuring the rare and common biospheres. We found a greater influence of homogeneous selection (i.e., imposed by spatiotemporally constant variables) mediating the assembly of the rare biosphere, whereas the common biosphere was mostly governed by variable selection (i.e., imposed by spatial and/or temporal fluctuating variables). By partitioning the different types of rarity, we found homogeneous selection to explain the prevalence of permanently rare taxa, thus suggesting their persistence at low abundances to be restrained by physiological traits. Conversely, the dynamics of conditionally rare taxa were mostly structured by variable selection, which aligns with the ability of these taxa to switch between rarity and commonness as responses to environmental spatiotemporal variations. Taken together, our study contributes to the establishment of a link between conceptual and empirical developments in the ecology of the soil microbial rare biosphere. Besides, this study provides a framework to better understand, model, and predict the existence and dynamics of microbial rare biospheres across divergent systems and scales.

Bacterial rarity in a subarctic stream network: Biodiversity patterns, assembly mechanisms and types of rarity

“…In a review across ecosystems, Nyirabuhoro et al (2020) reported CRT to account for 1.5 to 28% of total community membership and 0 to 97% of community variability. The relative importance of this group to overall community variability thus varies widely among ecosystems but their role as reservoirs for community recovery after disturbances, thus potentially supporting community stability, is substantial (Jia et al, 2022; Shade et al, 2014). Direct evidence for such a role for CRT (or CRA in this paper) is rare but in one of the few cases, Liang et al (2020) showed that CRT bacteria contributed more to maize crop yield than did the abundant taxa.…”

“…Indeed, Wang et al (2013) suggested that stochastic processes predominate over deterministic ones if the regional species pool is characterized by environmental generalists. Using soil chronosequence data, Jia et al (2022) showed that permanently rare bacteria possess a specific array of ecological traits (e.g., low growth rate; resource use efficiency) and are consistently under strong homogenous selection; these same taxa typically occupy narrow ecological niches. In our data, transiently rare taxa were the dominant type of rarity in terms of ASV richness.…”

“…A corresponding observation of the rare subcommunity being more controlled by local‐scale environmental sorting and the abundant subcommunity by a wider array of assembly processes has been made for both soil (Ji et al, 2020; Jiao & Lu, 2020b) and freshwater (Liu et al, 2015; Nyirabuhoro et al, 2020) ecosystems. Although there are exceptions to this pattern (e.g., Xue et al, 2018), it seems rather general across ecosystems and is usually explained by the majority of rare bacteria being habitat specialists with restricted distributions, while abundant taxa tend to be tolerant of a wider range of environmental conditions (Jia et al, 2022; Liao et al, 2017; Liu et al, 2015). Indeed, Wang et al (2013) suggested that stochastic processes predominate over deterministic ones if the regional species pool is characterized by environmental generalists.…”

“…We also briefly report some of the key results for the cutoff level of <0.1% ('very rare') to show that our findings were not sensitive to the rarity cutoff level used. We also defined the average sample-specific rarity cutoff using the 'h-index approach' by Jia et al (2022) whereby species are considered rare when their abundances are not higher than their ranks in the rank abundance curve. The cutoff value defined this way was 0.7%.…”

“…The rare and common microbial subcommunities may also be driven by distinct assembly processes, with rare taxa being often controlled by strong environmental selection and the abundant subcommunity by a wider array of assembly processes (Ji et al, 2020; Nyirabuhoro et al, 2020: Jiao & Lu, 2020a). Jia et al (2022) showed homogeneous selection to be the driving force for the rare biosphere in soil bacteria, whereas the common biosphere was assembled through multiple processes, of which variable selection was most important. Conversely, one could hypothesize that, owing to their inherently low abundances, rare taxa might be controlled mainly by ecological drift (i.e., the stochastic loss and replacement of individuals) (see Jiao et al, 2017; Xue et al, 2018).…”