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Theory questions the persistence of nonreciprocal interactions in which one plant has a positive net effect on a neighbor that, in return, has a negative net impact on its benefactor - a phenomenon known as antagonistic facilitation. We develop a spatially explicit consumer-resource model for belowground plant competition between ecosystem engineers, plants able to mine resources and make them available for any other plant in the community, and exploiters. We use the model to determine in what environmental conditions antagonistic facilitation via soil-resource engineering emerges as an optimal strategy. Antagonistic facilitation emerges in stressful environments where ecosystem engineers' self-benefits from mining resources outweigh the competition with opportunistic neighbors. Among all potential causes of stress considered in the model, the key environmental parameter driving changes in the interaction between plants is the proportion of the resource that becomes readily available for plant consumption in the absence of any mining activity. Our results align with theories of primary succession and the stress gradient hypothesis. However, we find that the total root biomass and its spatial allocation through the root system, often used to measure the sign of the interaction between plants, do not predict facilitation reliably.

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Tailings ponds formed by long-term accumulation of mineral processing waste have become a global environmental problem. Even worse, tailings ponds are often simply abandoned or landfilled after they cease to be used. This allows pollution to persist and continue to spread in the environment. The significance of primary succession mediated by biological soil crusts for tailings pond remediation has been illustrated by previous studies. However, the process of primary succession may not be the same at different stages during the lifetime of tailings ponds. Therefore, we investigated the environmental differences and the successional characteristics of microbial communities in the primary successional stage of tailings ponds at three different states. The results showed that the primary succession process positively changed the environment of tailings ponds in any state of tailings ponds. The primary successional stage determined the environmental quality more than the state of the tailings pond. In the recently abandoned tailings ponds, abundant species were more subjected to heavy metal stress, while rare species were mainly limited by nutrient content. We found that as the succession progressed, rare species gradually acquired their own community space and became more responsive to environmental stresses. Rare species played an important role in microbial keystone species groups.

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Despite the extensive research conducted on plant-soil-water interactions, the understanding of the role of plant water sources in different plant successional stages remains limited. In this study, we employed a combination of water isotopes (δ2H and δ18O) and leaf δ13C to investigate water use patterns and leaf water use efficiency (WUE) during the growing season (May to September 2021) in Hailuogou glacier forefronts in China. Our findings revealed that surface soil water and soil nutrient gradually increased during primary succession. Dominant plant species exhibited a preference for upper soil water uptake during the peak leaf out period (June to August), while they relied more on lower soil water sources during the post-leaf out period (May) or senescence (September to October). Furthermore, plants in late successional stages showed higher rates of water uptake from uppermost soil layers. Notably, there was a significant positive correlation between the percentage of water uptake by plants and available soil water content in middle and late stages. Additionally, our results indicated a gradual decrease in WUE with progression through succession, with shallow soil moisture utilization negatively impacting overall WUE across all succession stages. Path analysis further highlighted that surface soil moisture (0- 20 cm) and middle layer nutrient availability (20- 50 cm) played crucial roles in determining WUE. Overall, this research emphasizes the critical influence of water source selection on plant succession dynamics while elucidating underlying mechanisms linking succession with plant water consumption.

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Biological nitrogen fixation (BNF) has important ecological significance in mine tailing by contributing to the initial accumulation of nitrogen. In addition to chemolithotrophic and heterotrophic BNF, light may also fuel BNF in oligotrophic mine tailings. However, knowledge regarding the occurrence and ecological significance of this biogeochemical process in mine tailings remains ambiguous. The current study observed phototrophic BNF in enrichment cultures established from three primary successional stages (i.e., original tailings, biological crusts, and pioneer plants) of tailings. Notably, phototrophic BNF in tailings may be more active at vegetation stages (i.e., biological crusts and pioneering plants) than in bare tailings. DNA-stable isotope probing identified Roseomonas species as potential aerobic anoxygenic phototrophs responsible for phototrophic BNF. Furthermore, metagenomic binning as well as genome mining revealed that Roseomonas spp. contained essential genes involved in nitrogen fixation, anoxygenic photosynthesis, and carbon fixation, suggesting their genetic potential to mediate phototrophic BNF. A causal inference framework equipped with the structural causal model suggested that the enrichment of putative phototrophic diazotrophic Roseomonas may contribute to an elevated total nitrogen content during primary succession in these mine tailings. Collectively, our findings suggest that phototrophic diazotrophs may play important roles in nutrient accumulation and hold the potential to facilitate ecological succession in tailings.

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[This corrects the article DOI: 10.3389/fmicb.2023.1284864.].

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Introduction: Biodiversity maintenance and its underlying mechanisms are central issues of ecology. However, predicting the composition turnovers of microbial communities at multiple spatial scales remains greatly challenging because they are obscured by the inconsistent impacts of climatic and local edaphic conditions on the assembly process. Methods: Based on the Illumina MeSeq 16S/18S rRNA sequencing technology, we investigated soil bacterial and eukaryotic communities in biocrusts with different successional levels at a subcontinental scale of Northern China. Results: Results showed that irrespective of spatial scale, bacterial α diversity increased but eukaryotic diversity decreased with the primary succession, whereas both ß diversities decreased at the subcontinental scale compared with smaller scales, indicating that the biogeographic pattern of soil microorganisms was balanced by successional convergence and distance decay effect. We found that the convergence of bacterial and eukaryotic communities was attributed to the turnovers of generalist and specialist species, respectively. In this process, edaphic and climatic factors showed unique roles in the changes of diversity at local/subcontinental scales. Moreover, the taxonomic diversity tended to be more susceptible to climatic and edaphic conditions, while biotic factors (photosynthesis and pigments) were more important to phylogenetic diversity. Conclusion: Taken together, our study provided comprehensive insights into understanding the pattern of microbial diversity at multiple spatial scales of drylands.

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Roads have the potential to alter local environmental conditions, such as the availability of water and nutrients, and rapidly create suitable habitats for the establishment of both native and non-native plant species, transforming the ecosystems. This is a challenge in Timanfaya National Park and Los Volcanes Natural Park on Lanzarote Island, protected areas that have experienced primary succession after recent volcanic eruptions. In arid ecosystems, changes in abiotic conditions along roadsides might facilitate colonization and plant growth. We analyzed the effect of roads and road type on plant species composition and richness at a spatiotemporal scale. Vascular plant species were systematically recorded at three distances from the road edge on both sides, across fourteen zones in the wet and dry seasons, for three years. Results showed that there were slight differences on species composition depending on the distance to the road edge, as well as on the zones. Species richness was also determined by the interaction of the position, zones, and season, being higher at the road edge. Furthermore, zones with higher traffic intensity showed a higher presence of both native and non-native species. This study highlights the importance of the awareness about the road impacts on species composition by enhancing the colonization capacity of species while facilitating the entry of invasive ones. Good management practices regarding infrastructures in natural protected areas are crucial for the conservation of their unique flora, landscapes, and natural succession processes.

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Primary succession and microtopography result in environmental changes and are important processes influencing the community assembly of soil fungi in the Arctic region. In glacier forefields that contain a series of moraine ridges, both processes contribute synchronously to fungal spatial diversity. To reveal the synergistic effects of succession and microtopography, we investigated the fungal community structure and environmental variables in the moraines of the Arklio Glacier, Ellesmere Island. The study sites were established at four locations from the top to the bottom of the ridge slope within each of the three moraine ridges of different post-glacial ages. The location-dependent community composition was equally diverse in both the initial and later stages of succession, suggesting that successional time could alter the effects of microtopography on the fungal community. Moreover, our results suggest that fungal communities at different locations follow different successional trajectories, even if they have passed through the same time lapse. Such a synergistic effect of succession and microtopography of moraines does not allow for parallel changes in fungal communities among moraines or among locations, suggesting that the moraine series contributes substantially to fungal spatial diversity in the glacier forefield.

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Tailings ponds resulting from mining operations have led to serious environmental hazards, and their bioremediation is an area of ongoing exploration. Primary succession represents the starting point of biotic community establishment and development, with soil carbon and nitrogen cycling being critical to this process. To investigate the soil microbial-mediated carbon and nitrogen cycling patterns accompanying primary succession, we selected three types of tailings ponds as study areas and set up sampling sites for different stages of primary succession. The results showed that primary succession promoted microbe-mediated carbon and nitrogen cycling. It also led to improvements in soil nutrient availability and enzyme activity. In primary succession, the main pathways of carbon cycling are 3HP and rTCA, and nitrogen cycling is nitrate assimilation. In the early stages, microbes mediated more anaerobic and microaerobic processes. As succession proceeded, the pattern of microbial contributions to the carbon and nitrogen cycles changed. As succession proceeds, the functional metabolic potential of the carbon cycle gradually rises, while the nitrogen cycle shows a dramatic increase after the accumulation of autotrophic biomass. In addition, we found a positive coupling pattern between the carbon and nitrogen cycles. These findings support the optimization of bioremediation strategies for tailings ponds.

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The elevation of the snowline of the No. 1 Glacier in the Tianshan Mountains is increasing due to global warming, which has created favorable conditions for moss invasion and offers an opportunity to investigate the synergistic effects of incipient succession by mosses, plants, and soils. In this study, the concept of altitude distance was used instead of succession time. To investigate the changes of bacterial-community diversity in moss-covered soils during glacial degeneration, the relationship between bacterial community structure and environmental factors was analyzed and valuable microorganisms in moss-covered soils were explored. To do so, the determination of soil physicochemical properties, high-throughput sequencing, the screening of ACC-deaminase-producing bacteria, and the determination of ACC-deaminase activity of strains were performed on five moss-covered soils at different elevations. The results showed that the soil total potassium content, soil available phosphorus content, soil available potassium content, and soil organic-matter content of the AY3550 sample belt were significantly different compared with those of other sample belts (p < 0.05). Secondly, there was a significant difference (p < 0.05) in the ACE index or Chao1 index between the moss-covered-soil AY3550 sample-belt and the AY3750 sample-belt bacterial communities as the succession progressed. The results of PCA analysis, RDA analysis, and cluster analysis at the genus level showed that the community structure of the AY3550 sample belt and the other four sample belts differed greatly and could be divided into two successional stages. The enzyme activities of the 33 ACC-deaminase-producing bacteria isolated and purified from moss-covered soil at different altitudes ranged from 0.067 to 4.7375 U/mg, with strains DY1-3, DY1-4, and EY2-5 having the highest enzyme activities. All three strains were identified as Pseudomonas by morphology, physiology, biochemistry, and molecular biology. This study provides a basis for the changes in moss-covered soil microhabitats during glacial degradation under the synergistic effects of moss, soil, and microbial communities, as well as a theoretical basis for the excavation of valuable microorganisms under glacial moss-covered soils.

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Climate change is resulting in accelerated retreat of glaciers worldwide and much nitrogen-poor debris is left after glacier retreats. Asymbiotic dinitrogen (N2) fixation (ANF) can be considered a 'hidden' source of nitrogen (N) for non-nodulating plants in N limited environments; however, seasonal variation and its relative importance in ecosystem N budgets, especially when compared with nodulating symbiotic N2-fixation (SNF), is not well-understood. In this study, seasonal and successional variations in nodulating SNF and non-nodulating ANF rates (nitrogenase activity) were compared along a glacial retreat chronosequence on the eastern edge of the Tibetan Plateau. Key factors regulating the N2-fixation rates as well as the contribution of ANF and SNF to ecosystem N budget were also examined. Significantly greater nitrogenase activity was observed in nodulating species (0.4-17,820.8 nmol C2H4 g-1 d-1) compared to non-nodulating species (0.0-9.9 nmol C2H4 g-1 d-1) and both peaked in June or July. Seasonal variation in acetylene reduction activity (ARA) rate in plant nodules (nodulating species) and roots (non-nodulating species) was correlated with soil temperature and moisture while ARA in non-nodulating leaves and twigs was correlated with air temperature and humidity. Stand age was not found to be a significant determinant of ARA rates in nodulating or non-nodulating plants. ANF and SNF contributed 0.3-51.5 % and 10.1-77.8 %, respectively, of total ecosystem N input in the successional chronosequence. In this instance, ANF exhibited an increasing trend with successional age while SNF increased only at stages younger than 29 yr and then decreased as succession proceeded. These findings help improve our understanding of ANF activity in non-nodulating plants and N budgets in post glacial primary succession.

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Glacier retreat raises global concerns but brings about the moment to study soil and ecosystem development. In nutrient-limited glacier forelands, the adaptability of pioneering plant and microbial species is facilitated by their interactions, including rhizosphere effects, but the details of this adaptability are not yet understood. In the rhizosphere of five pioneering plants, we comprehensively deciphered the microbial taxonomic and functional compositions. Two nitrogen-fixing microbial genera, Bradyrhizobium and Mesorhizobium, were among the most abundant taxa in the rhizomicrobiome. Moreover, several rhizobial genera, including Rhizobium, Pararhizobium, Allohrizobium, and Sinorhizobium, head the list of major modules in microbial co-occurrence networks, highlighting the vital roles of nitrogen-cycling taxa in the rhizomicrobiome of pioneering plants. Microbial genes involved in nitrogen, sulfur, phosphorus, and methane cycles were simultaneously correlated with microbial community dissimilarity, and 12 functional pathways were detected with distinct relative abundances among soils. Zooming in on the nitrogen-cycling genes, nifW, narC, nasA, nasB, and nirA were mainly responsible for the significant differences between soils. Furthermore, soil pH and the carbon/nitrogen ratio were among the topsoil properties interacting with nitrogen and sulfur cycling gene dissimilarity. These results explicitly linked biogeochemical cycling genes to the rhizomicrobiome and soil properties, revealing the roles of these genes as microbial drivers in mediating rhizosphere soil-plant-microbiome interactions.

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Plant nitrogen (N) uptake preference is a key factor affecting plant nutrient acquisition, vegetation composition and ecosystem function. However, few studies have investigated the contribution of different N sources to plant N strategies, especially during the process of primary succession of a glacial retreat area. By measuring the natural abundance of N isotopes (δ15N) of dominant plants and soil, we estimated the relative contribution of different N forms (ammonium-NH4+, nitrate-NO3- and soluble organic N-DON) and absorption preferences of nine dominant plants of three stages (12, 40 and 120 years old) of the Hailuogou glacier retreat area. Along with the chronosequence of primary succession, dominant plants preferred to absorb NO3- in the early (73.5%) and middle (46.5%) stages. At the late stage, soil NH4+ contributed more than 60.0%, In addition, the contribution of DON to the total N uptake of plants was nearly 19.4%. Thus, the dominant plants' preference for NO3- in the first two stages changes to NH4+ in the late stages during primary succession. The contribution of DON to the N source of dominant plants should not be ignored. It suggests that the shift of N uptake preference of dominant plants may reflect the adjustment of their N acquisition strategy, in response to the changes in their physiological traits and soil nutrient conditions. Better knowledge of plant preferences for different N forms could significantly improve our understanding on the potential feedbacks of plant N acquisition strategies to environmental changes, and provide valuable suggestions for the sustainable management of plantations during different successional stages.

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Soil microbial carbon use efficiency (CUE) is a vital physiological parameter in assessing carbon turnover. Yet, how the microbial assemblies with distinct trophic strategies regulate the soil microbial CUE remains elusive. Based on the oligotrophic-copiotrophic framework, we explored the role of microbial taxa with different trophic strategies in mediating microbial CUE (determined by a 13C-labeled approach) along the vegetation primary succession in Hailuogou glacier retreat area of the southeastern Tibetan Plateau. Results showed that soil microbial CUE ranged from 0.54 to 0.72 (averaging 0.62 ± 0.01 across all samples) and increased staggeringly along the vegetation succession. Microbial assemblies with distinct trophic strategies were crucial regulators of soil microbial CUE. Specifically, microbial CUE increased with microbial oligotroph: copiotroph ratios, oligotroph-dominated stage had a higher microbial CUE than copiotroph-dominated ones. The prevalence of oligotrophic members would be the underlying microbial mechanism for the high microbial CUE. Given that oligotrophs predominate in more recalcitrant carbon soils and their higher microbial CUE, we speculate that oligotrophs are likely to potentially enhance carbon sequestration in soils. In addition, the responses of the microbial CUE to fungal oligotroph: copiotroph ratios were higher than bacterial ones. Fungal taxa may play a dominant role in shaping microbial CUE relative to bacterial members. Overall, our results constructed close associations between microbial trophic strategies and CUE and provide direct evidence regarding how microbial trophic strategies regulate microbial CUE. This study is a significant step forward for elucidating the physiological mechanisms regulating microbial CUE and has significant implications for understanding microbial-mediated carbon cycling processes.

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Coastal dunes are sensitive indicators of climate change: it is expected that higher precipitation and warmer temperature will promote vegetation growth and sand stabilization. Alternatively, dunes may become active during severe droughts, which would reduce plant cover and increase sand mobility. Consequently, it is relevant to explore community shifts and self-organization processes to better understand how coastal dunes vegetation will respond to these projected changes. Primary succession allows the exploration of community assembly and reorganization processes. We focused on three environmental variables (bare sand, temperature, and precipitation) and five successional groups (facilitators, colonizers, sand binders, nucleators, and competitors). For 25 years (from 1991 to 2016), species turnover was monitored in 150 permanent plots (4 × 4 m) placed on an initially mobile dune system located on the coast of the Gulf of Mexico. The spatiotemporal dynamics observed during primary succession were consistent with the facilitation nucleation model. As late colonizers grew and expanded, psammophytes became locally extinct. The spatial patterns revealed that ecological succession did not occur evenly on the dunes. In addition, the increased mean yearly temperature during the last decades seemed to be associated with the accelerated increment in plant cover and species richness, which had not been registered before in Mexico.

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Plants alter soil biological communities, generating ecosystem legacies that affect the performance of successive plants, influencing plant community assembly and successional trajectories. Yet, our understanding of how microbe-mediated soil legacies influence plant establishment is limited for primary successional systems and forest ecosystems, particularly for ectomycorrhizal plants. In a two-phase greenhouse experiment using primary successional mine reclamation materials with or without forest soil additions, we conditioned soil with an early successional shrub with low mycorrhizal dependence (willow, Salix scouleriana) and a later-successional ectomycorrhizal conifer (spruce, Picea engelmannii × glauca). The same plant species and later-successional plants (spruce and/or redcedar, Thuja plicata, a mid- to late-successional arbuscular mycorrhizal conifer) were grown as legacy-phase seedlings in conditioned soils and unconditioned control soils. Legacy effects were evaluated based on seedling survival and biomass, and the abundance and diversity of root fungal symbionts and pathogens. We found negative intraspecific (same-species) soil legacies for willow associated with pathogen accumulation, but neutral to positive intraspecific legacies in spruce associated with increased mycorrhizal fungal colonization and diversity. Our findings support research showing that soil legacy effects vary with plant nutrient acquisition strategy, with plants with low mycorrhizal dependence experiencing negative feedbacks and ectomycorrhizal plants experiencing positive feedbacks. Soil legacy effects of willow on next-stage successional species (spruce and redcedar) were negative, potentially due to allelopathy, while ectomycorrhizal spruce had neutral to negative legacy effects on arbuscular mycorrhizal redcedar, likely due to the trees not associating with compatible mycorrhizae. Thus, positive biological legacies may be limited to scenarios where mycorrhizal-dependent plants grow in soil containing legacies of compatible mycorrhizae. We found that soil legacies influenced plant performance in mine reclamation materials with and without forest soil additions, indicating that initial restoration actions may potentially exert long-term effects on plant community composition, even in primary successional soils with low microbial activity.

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Arbuscular mycorrhiza (AM) and ectomycorrhiza (EcM) are the most abundant and widespread types of mycorrhizal symbiosis, but there is little and sometimes conflicting information regarding the interaction between AM fungi (AMF) and EcM fungi (EcMF) in soils. Their competition for resources can be particularly relevant in successional ecosystems, which usually present a transition from AM-forming herbaceous vegetation to EcM-forming woody species. The aims of this study were to describe the interaction between mycorrhizal fungal communities associated with AM and EcM hosts naturally coexisting during primary succession on spoil banks and to evaluate how this interaction affects growth and mycorrhizal colonization of seedlings of both species. We conducted a greenhouse microcosm experiment with Betula pendula and Hieracium caespitosum as EcM and AM hosts, respectively. They were cultivated in three-compartment rhizoboxes. Two lateral compartments contained different combinations of both host plants as sources of fungal mycelia colonizing the middle compartment, where fungal biomass, diversity, and community composition as well as the growth of each host plant species' seedlings were analyzed. The study's main finding was an asymmetric outcome of the interaction between the two plant species: while H. caespitosum and associated AMF reduced the abundance of EcMF in soil, modified the composition of EcMF communities, and also tended to decrease growth and mycorrhizal colonization of B. pendula seedlings, the EcM host did not have such effects on AM plants and associated AMF. In the context of primary succession, these findings suggest that ruderal AM hosts could hinder the development of EcM tree seedlings, thus slowing the transition from AM-dominated to EcM-dominated vegetation in early successional stages.

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Dissolved organic matter (DOM), the most active type of soil organic matter, plays a key role in soil biogeochemical cycling. Therefore, exploring the source, composition, environmental response, and accumulation mechanism of DOM during vegetation succession has great significance for predicting soil carbon cycling. In this study, DOM was extracted from topsoil and subsoil at plots after 12, 30, 40, 50, 80, and 120 years of primary succession along the Hailuogou Glacier retreat area. The concentrations and spectral characteristics of DOM were analyzed via a combination of elemental analysis, ultraviolet-visible spectroscopy, and three-dimensional fluorescence excitation-emission matrix spectroscopy. The results showed that concentrations of soil dissolved organic carbon and dissolved organic nitrogen of both topsoil and subsoil increased significantly during vegetation succession. Along the chronosequence, the protein-like components and optical indices were significantly enhanced, humic-like components and the optical indices decreased, the aromaticity degree of DOM increased first and then decreased. Soil pH and NH4+-N content explained 62.2% of the total variation of surface soil DOM components, while soil moisture and pH explained 64.3% of that of subsurface soil DOM, indicating that environmental conditions were key factors affecting the concentrations and composition of soil DOM in the Hailuogou Glacier retreat area.

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Cyanobacteria are key organisms in the Antarctic ecosystem, but the primary succession of its communities in recently deglaciated soils remains poorly understood. In this study, we surveyed the primary succession of cyanobacterial communities with an in-depth Next Generation Sequencing approach in three Antarctic recently glacier forefields. Despite the similar physicochemical characteristics of the soils, we did not find a common pattern in the distribution of the cyanobacterial communities at the finest level of taxonomic resolution. However, the metabarcoding analysis revealed a common community of 14 cyanobacterial identical sequences in all the studied soils, whose lineages were not restricted to polar or alpine biotopes. These ASVs comprised a relative abundance within the cyanobacterial community of 51.5%-81.7% among the three locations and were also found in two cyanobacterial mats from the Antarctic Peninsula. Our results suggest that (micro)biotic interactions act as a key driver of the community composition and dynamics of Cyanobacteria during the early stages of succession in recently deglaciated soils of Antarctica. A few common genera might play a key role in the ecosystem, due to its ubiquitous presence not only in these soils but also in microbial mats, conforming probably the most widely disperse and dominant single genotypes in Antarctic soils.

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Ecosystems are complex structures with interacting abiotic and biotic processes evolving with ongoing succession. However, limited knowledge exists on the very initial phase of ecosystem development and colonization. Here, we report results of a comprehensive ecosystem development monitoring for twelve floodplain pond mesocosms (FPM; 23.5 m × 7.5 m × 1.5 m each) located in south-western Germany. In total, 20 abiotic and biotic parameters, including structural and functional variables, were monitored for 21 months after establishment of the FPMs. The results showed evolving ecosystem development and primary succession in all FPMs, with fluctuating abiotic conditions over time. Principal component analyses and redundancy analyses revealed season and succession time (i.e., time since ecosystem establishment) to be significant drivers of changes in environmental conditions. Initial colonization of both aquatic (i.e., water bodies) and terrestrial (i.e., riparian land areas) parts of the pond ecosystems occurred within the first month, with subsequent season-specific increases in richness and abundance for aquatic and terrestrial taxa over the entire study period. Abiotic environmental conditions and aquatic and terrestrial communities showed increasing interpond variations over time, that is, increasing heterogeneity among the FPMs due to natural environmental divergence. However, both functional variables assessed (i.e., aquatic and terrestrial litter decomposition) showed opposite patterns as litter decomposition rates slightly decreased over time and interpond differences converged with successional ecosystem developments. Overall, our results provide rare insights into the abiotic and biotic conditions and processes during the initial stages of freshwater ecosystem formation, as well as into structural and functional developments of the aquatic and terrestrial environment of newly established pond ecosystems.