Flooding-related Distribution of Abundant and Rare taxa
Generally, the diversity and structure of both the abundant and rare communities were influenced by flooding. Compared to higher elevations, riparian soils at lower elevations were more frequently affected by flooding, which significantly increased the alpha diversity of the microbial community. This may be related to the higher nutrient availability of frequently-flooded soils which have greater exchange rate with the aquatic system and thus more extensive nutrients cycling [32]. Indeed, flooding can carry large amounts of nutrients from upland soils to later deposit in lower elevation soil [6]. Periodic flooding can also create a heterogeneous environmental gradient in the riparian zone by altering soil biogeochemical cycles [1, 6]. Therefore, the community structures of both abundant and rare taxa exhibited elevation-related distributions. Notably, soils with more frequent flooding (i.e., 155 m and 150 m with RFE > 1) harbored significantly different bacterial and archaeal communities from sites in higher elevations (≥ 165 m). This suggests that there may be a threshold for the frequency of dry-wet alternation which causes significant changes to the microbial communities in soil, such as an RFE equal to 1 in the present study.
Periodic flooding also acts as one of the most stressful environmental transitions known to soil microbial systems [33, 34]. The effective utilization of resources, high growth rate and better adaptability to changing environments [10] allows abundant taxa to play a stable and key role in the biogeochemical cycle in a disturbed environment [8]. Compared to abundant taxa, rare taxa may play a more active role during fluctuating environmental conditions (i.e., dry-wet alternation) due to their sturdiness and continuous regrowth [35]. Meanwhile, the high diversity of rare communities underlines their importance as ‘seed banks’ to the diversity of microbial species [9, 13]. This entitles the rare taxa with a prominent metabolic potential under appropriate conditions [36]. In this study, most of the rare taxa (97.1% for bacteria and 69.5% for archaea) could shift to abundant given the right environmental conditions. It implies that rare taxa remain latent until favorable conditions are met, based on the heterogeneous habitats in riparian soils. This may allow for an enhanced functional redundancy within an ecosystem and thus resilience to environmental disturbance triggered by flooding [8].
Water Flooding Determines the Assembly Processes of a Community
In the present study, the community assembly of the abundant bacteria was mainly governed by stochastic processes (i.e., dispersal limitation), whereas the rare bacterial subcommunity was primarily driven by deterministic processes (i.e., variable selection). For archaeal communities, both the abundant and the rare subcommunities was governed by stochastic processes (i.e., dispersal limitation and undominated processes) although with an indispensable contribution of deterministic processes (i.e., homogeneous selection, 40%) on the community assembly of the rare archaea (Fig. 3). These observed discrepancies in the assembly processes of abundant vs. rare communities were largely attributed to the ability of different individual microorganism to cope with changing environments [37]. Here, the niche breadth of the abundant taxa was observed to be wider than that of the rare taxa (Fig. S1). Abundant taxa are deemed to be more abundant in a given environment due to their efficient utilization of a wider range of resources [10], meaning that stochasticity is more likely to influence abundant taxa [9]. On the contrary, rare taxa with a narrow niche breadth are more sensitive to environmental changes, which thus attributes to a low growth rate and greater competition [21, 23, 26]. Therefore, rare taxa are more easily restricted to limited locations by environmental filtering. Moreover, the different community assembly processes of bacteria and archaea might be explained by their differences in metabolic activity, dispersal capability, and growth habit [38, 39].
Notably, the assembly processes of both abundant bacterial and archaeal subcommunities, driven by dispersal limitation, were enhanced with the influence of flooding. Dispersal limitation, belonging to the stochastic processes, is defined as a limited exchange of species between different communities due to their low dispersal rates [40], and is thus a process which is predicted to increase dissimilarities in community composition. Classically, a dispersal process is usually a combination of the source community and physical mediators (e.g., wind or water) that transfer individual species [41]. Wind is an ideal medium for species dispersal [42], and especially bacteria and archaea of high abundance are often dispersed though prevailing winds [39, 42]. Obviously, flooding confines microbes to soil or water environments, reducing the processes of wind-blown propagules, and thus limiting the dispersal of soil microorganisms particularly from sites of lower elevations. Moreover, the effect of dispersal also depends on the taxonomic composition [41]. Abundant taxa with high local abundance have strong environmental adaptability and thus often exhibit ample changes. They are therefore less likely to be excluded from a given habitat [9]. Habitat differentiation, such as differences in soil oxygen availability at lower and higher elevations caused by periodic flooding, spatially restricts microorganisms to suitable environments, challenging their dispersal to unfavorable habitats [43]. Therefore, dispersal limitation is to some extent deterministic since the capacities of species to disperse can be influenced by environmental conditions [44]. Particularly, the assembly process of abundant archaea was also significantly affected by undominated processes, and flooding showed opposite effects on this group compared to dispersal limitation. Generally, the undominated processes of dispersal limitation and drift, demonstrated equal contribution to community composition [40]. The diminishing contribution of undominated processes at lower elevations suggests that the role of drift relative to dispersal limitation lessened as elevation decreased. It follows that the effects of stochastic processes (such as undominated processes and dispersal limitation) on abundant archaea may be closely associated with flooding. This was demonstrated by the substantial association between the βNTI of abundant archaea and soil moisture, and RFE (Fig. 4), which suggests that increases in soil moisture and RFE may promote stochastic processes.
For the rare taxa, the community assembly was dominated by two opposing deterministic processes, namely variable selection for bacteria and homogeneous selection for archaea. Variable selection often results in dissimilar community compositions due to divergent selective environments, while homogeneous selection promotes convergent community compositions through a consistent environmental filtering [40]. In this study, 97.1% of the rare bacteria belonged to conditionally rare taxa which could periodically shift between abundant and rare in response to environmental fluctuations [13]. It is clear that periodic flooding can create such fluctuating environmental conditions, thereby making variable selection the primary driver of the assembly of rare bacteria [10]. This was further supported by the substantial relationship between the βNTI of rare bacteria and soil Fe2+ content, Fe2+/Fe3+, moisture and RFE. It suggests that changes in these soil parameters, as triggered by flooding, may be the source of variable selection for rare bacteria. Unlike rare bacteria, a large part of rare archaea (30.5%) permanently persists at low abundances, that is, they always remain rare. Given that these rare species occupy specialized niches and frequently interact with other species, it has been shown that such rarity results from strong homogeneous selection [10]. The community assembly of rare archaea was governed by homogeneous selection, enabling a large convergence and a weak distance-decay relationship [45]. This in line with the relatively low variation of the rare archaeal subcommunity along the riparian elevation (R2 = 0.257). Meanwhile, the βNTI of rare archaea was significantly correlated with soil C/N and TC, suggesting the role of C/N and TC as consistent environmental filters in driving the community assembly of rare archaea. Our previous study has proven that C/N and TC in the riparian soil does not vary along the elevation [6].
Linkage between Community Assembly and Riparian Ecosystems
Riparian zones, characterized by their aquatic-terrestrial ecotone ecosystems, have long been regarded as biogeochemical hotspots of nutrient cycling because of the fluctuating environmental conditions and intensive material exchange between soil and water trigged by flooding [46]. Here, microbial communities contribute immense biomass, underpinning integral biogeochemical processes and ecosystem functioning [11], where abundant and rare taxa each play a vital role. In this study, abundant taxa exhibited a ubiquitous distribution mainly driven by stochastic processes. This indicated that abundant taxa can persist at relatively high abundances across the riparian soils with a low probability of extinction, which ensures the stability of an abundant taxa-mediated ecosystem functioning [8, 9]. For example, abundant taxa are regarded to be the most crucial species in carbon cycling [8]; the stochasticity-driven assembly keeps their roles in carbon cycling from changing substantially as a result of great environment fluctuations caused by flooding. In contrast, rare communities often consists of functionally relevant taxa [10]. Given the predominance of deterministic processes in rare communities, many rare taxa sustain a low growth rate or even adopt a type of dormancy to cope with unfavorable or harsh local environmental conditions, such as long-term periodic flooding [47]. Undoubtedly, these unfavorable environments may be suitable conditions for other rare taxa to bloom, thus promoting the relevant ecosystem functions [10]. This may explain why riparian zones are deemed biogeochemical hotspots. Overall, in the context of climate change, which foresees increased flooding and precipitation in certain areas, uncovering the patterns of microbial community assembly processes in response to flooding can provide insight into their ecological functional roles.